2012 COURSE DATES: AUGUST 4 – 17, 2012 - Sirenian International

ECOLOGY, BEHAVIOR & CONSERVATION OF MANATEES & DOLPHINS AND THE 

COMPLEX MANGROVE-SEAGRASS-CORAL HABITATS WE SHARE WITH MARINE 

MEGAFAUNA WITHIN THE BELIZE BARRIER REEF LAGOON SYSTEM 

2012 COURSE DATES: AUGUST 4 – 17, 2012 

OVERVIEW & BACKGROUND 

Antillean manatees (Trichechus manatus manatus) are found throughout Central America and the Caribbean, but 

are Red Listed by the IUCN as endangered, in continuing decline, with severely fragmented populations. The UN 

Caribbean Environmental Programme considers them an endangered and protected species of regional concern, 

threatened by poaching, boat strikes, entanglement in fishing gear, and habitat degradation. Belize may be the last 

stronghold for Antillean manatees in the Caribbean; and the Drowned Cayes area is one of the most important 

activity centers in Belize. However, the existing body of knowledge is inadequate to develop and implement sitespecific 

management and recovery plans. Because manatees are elusive, endangered, and have slow reproductive 

rates, long-term studies in this area are necessary to evaluate and monitor the population status and develop practical 

conservation plans to ensure survival of the population, and ultimately, the sub-species. Our comprehensive and 

collaborative project began in October 1998 and hopefully, will continue indefinitely into the future!

Bottlenose dolphins (Tursiops truncatus) are not 

endangered, but their stocks are considered depleted 

by the U.S. Marine Mammal Protection Act. A 

study of the local population was started in the 

Drowned Cayes by Oceanic Society Expeditions 

(OSE) in 1997, however it was abandoned in 2001 

when OSE moved their base to Turneffe, an atoll 

approximately 10 miles east of the Belize Barrier 

Reef. We re-started a photo-id project in 2005 with 

the hope of additional collaboration with OSE and 

other dolphin researchers in the region. 

Although this project does not specifically 

investigate sea turtles in Belize, loggerhead, 

hawskbill, and green sea turtles are occasionally 

sighted during our expeditions. And, in 2011, our 

visiting scientist is a turtle expert! 

Students and volunteers have been an integral component of the project since its conception. We rely on you to 

assist us with a wide range of data collection and processing during each survey. During this course, half-day (3-4 

hours) manatee & dolphin surveys will be conducted from a small boat on 10 of your 14-day expedition. 

Additionally, each student will undertake an individual research project to investigate another component of our 

field site, exposing students the broader Conservation Biology issues (see syllabus for suggested research topics. 

WELCOME LETTER 

While in Belize, be warned, “If ya drink de watter, ya mus com bok.” This old Belizean Creole proverb is true! On 

my first trip to Belize in 1998, I drank the water and fell in love with both the people and the place…and the 

manatees, dolphins, and other wildlife of 

course! Since that first trip, Belize has been 

my 2 nd home. Hopefully, you will soon be 

equally enthusiastic about the opportunities and 

challenges that await you in this tropical 

paradise. 

This is no ordinary field course! During the 

course, you will be collecting data on 

manatees, dolphins, and their habitat that my 

research partners and I actually use for our 

long-term studies of Antillean manatees and 

bottlenose dolphins in the Drowned Cayes 

(pronounced "keys") area of Belize. Although 

our project focuses primarily on manatees and 

dolphins, you will also experience the 

mangrove-seagrass-coral reef system in which 

we live and work. Perhaps most importantly, 

the data are also used by Belizeans, local 

NGOs, agencies, and decision-makers, to 

better develop marine conservation strategies. 

The Drowned Cayes is a complex maze of 

mangrove islands, just east of Belize City, 

surrounded by the Caribbean Sea. Since we 

are just two miles inside the Belize Barrier 

Reef, we are quite well protected from severe 

wave action, but if a tropical storm or hurricane threatens the western Caribbean, we will implement our Hurricane 

Plan, which includes evacuation. The Caribbean Sea and sunshine are breathtaking, but they can cause great 

Belize Field Course Briefing Page 1 4/4/2012

discomfort without proper protection, so you must pay close attention to the Packing Checklist in this briefing. 

Photo above: (c) C. Self-Sullivan: “Mario” a friendly, unmarked manatee videoed at North Gallows in 2001. 

You should be prepared to spend long periods of time outdoors, on the island and on the water in a small boat, 

searching for and observing manatees and dolphins. If you wish, you will have an opportunity to snorkel in the 

seagrass beds, mangrove bogues, or on coral patches. But please don’t expect to swim with manatees and dolphins – 

our wild animals are not acclimated to humans and intentional swimming with manatees & dolphins is not permitted 

in Belize. After a few days in the field, you will understand why we refer to manatees as elusive. We can pretty 

much guarantee that you will see both manatees & dolphins in the wild, but we can’t predict how many or how close 

they will come to our research boat. However, the more you read about manatee & dolphin ecology and behavior 

prior to your arrival, the more rewarding your observations will be. 

You should also be prepared for total immersion into private island living. As field researchers, we spend much of 

our time innovating and problem solving. On this 

expedition, you will experience the unique lifestyle 

of wildlife researchers under moderate conditions. 

While we live comfortably compared to most cayedwellers, 

it’s quite different from life in the northern 

hemisphere. Spanish Lookout Caye, a 184-acre 

mangrove island, is shared by Spanish Bay 

Conservation and Research Center, the Hugh Parkey 

Foundation for Marine Awareness and Education, 

and Hugh Parkey’s Belize Dive Connection and 

Adventure Lodge. During your two recreational 

days, we will be using Belize Dive Connections to 

experience an inland adventure to a Maya site, and 

a sea adventure on kayaks, snorkel or SCUBA (you 

may SCUBA only if you are a certified diver...bring 

your sea card & dive log). Photo (c) C. Self- 

Sullivan: “Dubya” a dolphin we’ve observed in our 

study area since 2004. 

Evening entertainment includes good conversation, 

star gazing, and a few old fashioned board and card 

games. So bring your favorite stories to share with us as we create some new stories to take back to your friends! 

Feel free to bring non-electronic musical instruments and games, too. Hopefully, participating on this expedition 

will leave you with a new perspective on sustainable living – are you up to the challenge? 

Cheers, 

Caryn Self-Sullivan, Ph.D. 

Adjunct Faculty, Nova Southeastern University 

President & Co-founder, Sirenian International 

200 Stonewall Drive, Fredericksburg, VA 22401-2110 

Email: cselfsullivan@sirenian.org 

Voice: 540.287.8207 | Fax: 888.371.4998 


TABLE OF CONTENTS PAGE 

BACKGROUND & PROJECT OVERVIEW Cover - 1 

WELCOME LETTER 1-2 

REGISTRATION FORM APPENDIX 

COURSE SYLLABUS (REQUIRES SIGNATURE) APPENDIX 

COURSE POLICY AND LIABILIT RELEASE FORM (REQUIRES SIGNATURE) APPENDIX 

REGISTRATION CHECK LIST 3 (BELOW) 

ABOUT BELIZE 4 

PRINCIPAL INVESTIGATOR, CO-PI, VISITING SCIENTISTS 4-5 

FIELD TRAINING AND ASSIGNMENTS 6-7 

ACCOMMOATIONS & FOOD 7-8 

ENVIRONMENTAL CONDITIONS 8 

POTENTIAL HAZARDS 9 

MEDICAL CONDITIONS OF SPECIAL CONCERN 9 

HEALTH INFORMATION 10 

PACKING CONSIDERATIONS 10 

EMERGENCIES IN THE FIELD 10-12 

OTHER USEFUL INFORMATION 12 

PACKING CHECK LIST 13-14 

APPENDIX (Forms, Data Sheets, Background Readings, Course Flyer, CVs) 15 

REGISTRATION & Pre-FIELDING CHECK LIST Session I 

Sessions II & III 1 st Group of items is due 90 days prior to fielding 

2 nd group of items is due 60 days prior to fielding Sent Date 

1 May 2012 Completed Registration Form _________ 

1 May 2012 Deposit Invoice Paid _________ 

1 May 2012 Signed Course Policy & Liability Release Form _________ 

1 May 2012 Signed Syllabus & Unofficial Copy of Transcripts _________ 

1 May 2012 Low-income Country Scholarship Essay _________ 

1 May 2012 1 st, 2 nd, and 3 rd Choice of Belize: Sea to Stars Topic _________ 

1 May 2012 1 st, 2 nd, and 3 rd Choice of Independent Research Topic _________ 

1 June 2012 Balance Due Invoice Paid _________ 

1 June 2012 Copy of Passport & Current Photo (Head Shot) _________ 

1 June 2012 Copy of DAN Preferred Membership Card _________ 

1 June 2012 Copy of SCUBA Certification Card (if diving) _________ 

1 June 2012 Copy of Airline Travel Itinerary & Receipt _________ 

1 June 2012 Proposed Presentation Format for Belize: Sea to Stars _________ 

1 June 2012 Literature Review & Citations for Independent Research Topic _________ 


ABOUT BELIZE 

Research Site: The project is based on Spanish Lookout Caye, a 184-acre twin-mangrove island located in the 

Drowned Cayes, about 10 miles east-southeast of Belize City. The Drowned Cayes are a maze of mangrove islands 

inside the Belize Barrier Reef. Approximately 10 acres of Spanish Lookout Caye have been filled and developed, 

leaving over 170-acres of pristine mangroves and 

mangrove swamps divided by a fast flowing channel 

of water commonly known as Gilroy’s Creek. 

Mangrove islands are famous for their wildlife and 

you will share this island home with birds, crabs, 

mosquitoes, and sandflies; you might even be lucky 

enough to sight an American crocodile or boa 

constrictor. Thirty to forty hours will be spent on our 

research boat, and marine hazards in the area include 

jellyfish and fire coral. The tropical sun is strong and 

the humidity is very high. Among the best reasons for 

visiting Belize are its long-standing and rapidly 

expanding conservation ethic and the incredible 

diversity of natural habitats. The spectacular Belize 

Barrier Reef, which is the second largest barrier reef in the world and runs along the entire 280 km coastline 

(Beletsky 1999), is perhaps its most celebrated natural treasure. 

Cultural, Social and Political Environment: Belize is a small country located between Mexico and Guatemala on 

the Yucatan Peninsula and was formally known as British Honduras. Because Belize was a British protectorate, 

English is taught and spoken at all school levels and is the official language. The more common language spoken 

between Belizeans is Creole – an unwritten language that combines English with African, Maya, and Spanish words. 

Most Belizeans speak at least two languages: English and at least one other such as Creole, Garifuna, Spanish, Maya 

Mopan, Kechi Maya, German (Menonites), etc. 

Belize is a politically stable democracy, with a Parliamentary system of government and elections every five years. 

Elections were held in spring of 2008, and the United Democratic Party (UDP) currently holds the majority of 

governmental seats. The People’s United Party (PUP) is the dominate opposition, having just lost their first election 

in 10 years. There are a few independents in office. The current Prime Minister is the Honorable Dean Barrow (also 

father of Rapper Jamal “Shyne” Barrow). Belizeans are quite vocal about their political opinions; almost everyone 

turns out to vote, and local taxi drivers are a good source of information about the current issues. Christianity is the 

predominant religion with many churches serving both Catholic and Protestant congregations. 

Like any large urban area, Belize City has its share of crime. The relatively small population of less than 300,000 

people consists of predominantly five unique cultures: Maya, Mistiso, Creole, Garifuna, and European. More 

recently Mennonites, Chinese, and Taiwanese populations are growing in Belize. 

PRINCIPAL INVESTIGATOR 

Caryn Self-Sullivan, Ph.D., is currently adjunct faculty at Nova 

Southeastern University, President of Sirenian International, 

Scientific Advisor to the NCRC West African manatee project in 

Volta Lake, Ghana, and Marine Science Advisor to the Hugh 

Parkey Foundation for Marine Awareness and Education in Belize. 

She graduated from Coastal Carolina University in 1997 with a 

B.S. in Marine Science and minors in Mathematics and Biology. 

She was an NSF Graduate Fellow from 1999-2001, and received 

her Ph.D. in Wildlife & Fisheries Sciences in 2008. Additionally, 

Dr. C serves on the IUCN Species Survival Commission Sirenia 

Specialist Group, the Belize National Manatee Working Group, and 

the Belize Marine Mammal Stranding Network. She has taught 

university level courses in Environmental Education, General 

Biology and Conservation Biology. She has taught professional 

level workshops focused on the order Sirenia in the Dominican 

Dr. Self-Sullivan 


Republic, Belize, Ghana, and the USA. Her research interests include marine biology, animal behavior, endangered 

marine species, and conservation biology, with a focus on marine mammals. In the field, Dr. C is responsible for 

supervising the students and staff, field training, coordinating the lecture/learning/discussion series, overseeing 

experimental design and data collection methods, capturing manatees with underwater video camera equipment, and 

capturing dolphins with above water digital camera equipment. During this course, Dr. C will be your primary 

expert on the local research project, manatees, and dolphins. 

CO-PI AND VISITING SCIENTISTS (CVS ARE IN THE APPENDIX SECTION) 

Katherine S. LaCommare, Ph.D., Co-PI will receive her 

PhD from the Environmental Biology Program, Department of 

Biology, University of Massachusetts, Boston, in May 2011! 

She is adjunct faculty at Lansing Community College in 

Michigan. Her previous degrees include a M.S. in Forestry, 

Conservation Biology Program, Department of Forestry and 

Natural Resources, Purdue University; and a B.S. in 

Anthropology/Zoology, University of Michigan. Katie cofounded 

Sirenian International with Dr. C and has been the co- 

PI on our long-term manatee research project since its 

inception in 1998. Unfortunately, Katie may not be able to 

join us during the 2001 field course. 

Heather J. Kalb, Ph.D., Visiting Scientist is an Assistant 

Dr. LaCommare 

Profession of Biology at West Liberty University in Wheeling, 

WV. She received her Ph.D. in Zoology from Texas A&M 

University in 1999. Dr. Kalb specializes in the reproductive 

physiology of turtles. She has taught university level courses in Zoology, Animal Diversity, General 

Biology, Scientific Communication, Comparative Vertebrate Anatomy & Physiology, Animal Behavior, 

Vertebrate Zoology, Conservation Biology, and Vertebrae Ecology. During this course, Dr. Kalb will be 

your primary expert on sea turtles and the fields of zoology, vertebrate anatomy, physiology. 

Bruce A. Schulte, Ph.D. Visiting Scientist, is the Biology Department Head at Western Kentucky 

University. He received his Ph.D. from the State University of New York, College of Environmental 

Science and Forestry in 1993; his M.S. in Biology from University of Southern California, and his B.S. 

from the College of William and Mary. He has regularly taught courses in Animal Behavior, Behavioral 

Ecology, Chemical Ecology, Conservation, and Environmental Biology. His research interests include 

communication and social behavior of herbivorous mammals, such as elephants, manatees, beavers and 

horses. His research group also examines how an understanding of behavior can facilitate positive 

human-animal interactions, such as reducing human-wildlife conflict. When in the field, Dr. Schulte will 

be your primary expert in the fields of animal behavior, chemical ecology, and conservation behavior. 

Jessica R. Young, Ph.D., Visiting Scientist is Associate Professor of Biology and Associate Vice 

President for Academic Affairs at Western State College of Colorado. She received her Ph.D. in 

Population Biology and 

Behavioral Ecology from Purdue University in 1994; and her B.A. in Ecology, Behavior, and Evolution 

from UC San Diego in 1988. Her general research interests integrate evolutionary theories of behavioral 

ecology and animal communication with applied aspects of conservation biology and wildlife 

management. For the past two decades, she has been working with a unique species of grouse, the 

Gunnison Sage-grouse, which was recognized by the AOU in 2000 as a distinct species based on 

physical, behavioral, and genetic traits and the first new bird species described in over 100 years. In the 

field, Dr. Young will be your primary expert in the fields of behavioral ecology and ornithology. 


FIELD TRAINING AND ASSIGNMENTS 

During each field course, students are encouraged to 

become proficient in at least one aspect of the long-term 

research project and will have input on the assignments 

in which they would like to participate. For example, 

one participant might become proficient recording 

behavioral data, while another might be better at 

operating the Global Positioning System (GPS) or 

recording environmental data. Most days, students will 

spend 1/2 day (3-4 hours) on a small boat conducting 

surveys and observing manatee & dolphin behavior. 

Our data collection is generally done from 25-foot 

fiberglass research boats, equipped with a single 115 HP 

Yamaha four-stroke engine. We carry a mobile phone, a 

magnetic compass, GPS unit, fire extinguisher, First Aid 

kit, and life jackets for 13 passengers, including the 

captain. Other standard safety equipment includes an 

anchor with anchor line, swim ladder, pole, bailing 

bucket, and bimini top for shade. There is no head 

(toilet facility) on board. We relieve ourselves in the 

water or in a bucket. 

Skills and talents extremely helpful to the project 

include patience, flexibility, attentiveness, a love for 

watching animals, a passion for learning, a passion for 

living sustainably in an outdoor environment, 

swimming, snorkeling, good handwriting, positive 

problem solving, positive attitude, strong team spirit, respect for low-tech data collection methods, and the ability to 

design and create something from nothing. 

Students will be expected to participate in most of the following tasks: 

• Continuous scanning surveys: These include both boat surveys and point scans designed to search for manatees 

& dolphins within the study area. During boat surveys and point scans students are needed to actively watch for 

manatees, dolphins and signs of their presence, and to record survey and sighting data. During sightings, 

students will record additional data, including behavioral states, breath cycles, and movements, as well as data 

about other boats in the scan area. 

• Environmental variable recording: Air and water temperature, salinity, wind direction and speed, sea state, 

turbidity, water depth, and bottom type will all be recorded. During boat surveys, point scans, and/or whenever 

a manatee or dolphin is sighted, locations will be marked with a GPS unit and general location will be plotted 

on the field map. At the end of each point scan students will use field equipment to take these measurements. 

• Focal follows: During focal follows, which are 40-minute increments of time during which we focus on a single 

manatee or group of dolphins, students record manatee or dolphin behavioral states, breath cycles, movements, 

and any other activity in the area. 

• Underwater ID captures: These are attempted by the Principal Investigator (PI) only, using a digital video 

camera and underwater housing. During an underwater attempt, students record both the manatee and the PI 

movements on a focal follow data sheet. 

• Surface photo-identification: During dolphin focal follows, the PI photographs dolphins from the bow of the 

research vessel; students document details on data sheets. Students will have an opportunity to photo dolphins 

when conditions are appropriate. 

Note: Students should NOT expect to swim with the manatees and dolphins, as commercial swimming with these 

endangered animals is prohibited in Belize. The PI has special permission to get into the water to photograph and 

video-tape animals, but this permission does not extend to students. 


ACCOMMODATIONS 

At Spanish Bay, students and staff will share dormitory style housing. Each room will consist of a combination of 

bunk beds, sleeping up to 12 per room. Shared bathroom facilities include conventional toilets, showers and sinks. 

Room assignments will be determined by gender. Private rooms for couples are not available. Rooms have 

screened windows to allow for ocean breezes and limit nocturnal insect visitors; however we recommend you 

consider bringing your own personal mosquito netting, as well as duct tape and string for hanging net over your 

bunk. 

Spanish Lookout Caye is powered by solar, wind, and diesel 

generators. Fresh water is precious and we mandate water 

conservation. We capture rainwater and recycle all waste water 

using a state-of-the-art tertiary recycling plant. Volunteers are 

taught to conserve water by taking one quick (island) shower 

per day, turning off the faucet while lathering soap, brushing 

teeth, etc. Drinking water is purchased from Belize and 

available 24-7 at designated dispensers. 

There is sufficient power to recharge batteries. We encourage 

students to bring digital cameras. We rely on you to take 

pictures of the project and we like to download them during the 

expedition. Please bring the appropriate charging devices (110 

volts AC, 60 Hz, flat two-pin plugs) and your data cable to 

share images with your classmates and instructors. Also, please 

bring rechargeable batteries; used disposable batteries must 

return home with you! Note that there is NOT adequate electricity for high voltage appliances such as curling irons, 

blow dryers, or coffee makers. Internet access and phone usage on the caye is limited to emergency use by the 

instructors. Many US and UK cell phones (except Sprint) work in Belize, but the international fees are generally 

expensive. SMS Texting works well and costs about $0.50 per message. 

NOTE: In 2012, we will also spend a few days on Corozal Bay in northern Belize with the 

Sarteneja Alliance for Conservation & Development Home Stay Program and may visit other 

conservation sites. 

FOOD 

At Spanish Bay, we will eat in the Belize Adventure Lodge dining area. Due to the logistics of living on a 

mangrove island, there is a limited amount of food variety during the expedition. Some special diets may be 

accommodated if advanced notice is given. Generally we eat a lot of chicken! BE SURE TO RECORD ANY 

DIETARY RESTRICTIONS ON YOUR REGISTRATION FORM…INCLUDING, BUT NOT LIMITED TO 

VEGETARIAN, VEGAN, LACTOSE INTOLERANT, GLUTEN INTOLERANT, FOOD OR OTHER 

ALLERGIES. The goal is to make our diet as traditional as possible, in order to make food a part of your 

experience! Weekly menus may include eggs and chicken, beef, pork, and local seafood (rarely), seasonal fruits and 

vegetables, tortillas, rice and beans, beans and rice (there is a difference), and pasta dishes. Water is the staple drink, 

supplemented with fruit juices, coffee, and tea. Also, if there are foods you do not eat for any reason please let us 

know so we don’t waste food by putting items on your plate that you won’t eat. For example, tomatoes are 

expensive so if you don’t eat them, just let us know and the staff will not put them on your plate! 

Comfort foods/drinks such as chips, cookies, candy, sodas, beer, rum, and wine are available (at your own expense) 

on the caye. A Gift Shop with limited supplies is located on our caye and is generally open daily from 9-4. Below 

are examples of the foods you might expect during the expedition. Please bear in mind that variety depends on 

availability. 

Breakfast: Eggs, beans, breakfast meats, tortillas, pancakes, oatmeal, fresh fruits 

Lunch: Tortillas, pasta, fresh veggies, rice, beans, chicken, boiled eggs, fresh fruit 

Dinner: Rice, beans, chicken, beef, pasta, veggies 

Snacks: Oranges, bananas, papaya, pineapple, watermelon 

Beverages: Water, coffee, tea, fruit juices 


ENVIRONMENTAL CONDITIONS 

SBCRC is situated on a 184-acre twin mangrove island, partially cleared and filled, but with over 

80% of the mangrove ecosystem intact, including the mosquitoes and sand flies. A mangrove 

island harbors many little hazards such as broken shells to cut your feet, and mangrove roots to 

trip you up, so it’s important to pay close attention to this rustic environment, which is free of 

paved roads and sidewalks. 

The sun is very strong here, and 

brief periods of intense rain are not 

uncommon during the field season. 

More extreme tropical storms and 

hurricanes traditionally occur from 

June through November with late- 

August, September, and October as 

the most active periods. 

In the event of a hurricane, we may 

evacuate the island and move inland 

for the duration of the storm. This 

has occurred three times during the 

14 years of this project. 


Potential Hazards 

We take pride in our experience, training, and track record with respect to students’ health and safety. So even when 

it seems that we are “mothering” you too much, we do expect you to follow our advice regarding your healthy and 

safety at all times! 

Hazard Type Associated Risks and Precautions 

Climate Students must be prepared to spend long hours in hot, humid, and wet conditions. The 

tropical sun is very strong. Dehydration, sunburn, and other heat related illnesses are a risk. 

Insects Sand flies and mosquitoes can be problematic. Sand flies are believed to be a vector for 

leishmaniasis in some regions. Mosquitoes may transmit a number of diseases (see 

Diseases below). Bot flies are also found in Belize, and mosquitoes may transmit their 

larvae to human hosts where the larvae will grow and develop. This is not life threatening, 

but can be painful and unpleasant. 

Marine life Fire corals, several species of stinging jellyfish, sharks, sea urchins, lionfish, and other 

potentially dangerous marine organisms can be found in the study area. These can all give 

painful and occasional severe stings or bites, which may become infected if untreated. 

Those with a dangerous allergy to bee or wasp stings may have a similarly dangerous 

reaction to corals and jellyfish. The best prevention is to avoid and not touch the animals. 

Please bring your epi-pen if you are allergic to anything. 

Snorkeling All the inherent risks of snorkeling are obviously present, including the effects of 

environmental conditions, marine life and other risks specific to your own physical/medical 

history. Snorkeling is optional and will be conducted in seagrass beds and on coral 

patches. Volunteers who chose to snorkel should know how to do so safely without 

hyperventilating or kicking up the substrate. 

Boats We will be aboard a boat for most fieldwork. All the fiberglass boats should have ladders 

and a bimini cover for sun protection. However, in some instances we may use a boat that 

lacks a ladder or shade. Deck surfaces of boats will become slippery and may place you at 

risk of slips, falls, and injuries that result from these accidents. 

Disease Diseases found in tropical regions include malaria, dengue fever, filariasis, leishmaniasis, 

onchocerciasis, trypanosomiasis (Chaga’s disease), schistosomiasis, leptospirosis, rabies, 

brucellosis, hepatitis, and typhoid. Most diseases are prevented with basic safety cautions. 

Driving Driving conditions are considered poor by western standards and pose inherent risks. 

Students will not be permitted to drive during the expedition. 

Medical Conditions of Special Concern 

Students should be physically fit, competent swimmers, and comfortable spending 3-4 hours on a boat. Those with 

chronic back problems or seasickness will find working and riding in small boats very uncomfortable. If you suffer 

from seasickness and intend to treat this with either over-the-counter or prescribed medication, please discuss the 

use and side effects with your physician and notify the PI before fielding. Be sure to tell your doctor that you will 

be spending all day in the sun! Please also let the PI know what medications, if any, you are taking for seasickness 

and/or malaria prevention. Some prophylactics have severe interactions with sun exposure and must be avoided. 

Any conditions that interfere with or limit stamina in the water, balance, swimming, or breathing should be carefully 

considered. If you have a current ear or sinus infection, it should be fully healed prior to participation in snorkeling 

or SCUBA. If you are allergic to bee stings, you may be allergic to Cnidaria stings (jellyfish and corals) and must 

bring an Epi-kit. Visual acuity (corrected via glasses or contacts is fine) and good hearing are important. 

Conditions or medications that increase one’s light sensitivity or sunburn risk should be discussed with a physician. 


HEALTH INFORMATION 

Routine Immunizations 

All volunteers should make sure to have the following up-to-date immunizations: DPT (diphtheria, pertussis, 

tetanus), polio, MMR (measles, mumps, rubella) and varicella (if you have not already had chicken pox). Please be 

sure your tetanus shot is current. 

Project Inoculations & Prophylactics 

The following are recommendations only. Medical decisions are the responsibility of each student and their doctor. 

Note that health conditions around the world are constantly changing, so keep informed and consult your physician, 

a local travel health clinic, the US Center for Disease Control (www.cdc.gov), the World Health Organization 

(www.who.int). Please consult your physician for guidance on inoculations if you intend to travel to other parts of 

the country. 

Typhoid 

Hepatitis A 

Hepatitis B 

These inoculations are recommended by the CDC for health reasons whenever you are 

traveling outside the USA. 

Malaria A malaria prophylaxis that allows exposure to the sun is recommended by the CDC 

Other Advice / Information 

• Malaria: Malaria is not present at the research site, but it is found within Belize. A prophylaxis is 

recommended by the CDC for all areas except Belize City. The risk is highest in the western and southern 

regions of the country, which you may visit on a recreational day. 

PACKING CONSIDERATIONS 

Remember to review the Packing Checklist at the end of this briefing. 

General Considerations 

Do not bring more luggage than you can carry and handle on your own. Space is also extremely limited in the dorm 

rooms. We recommend that you pack a carry-on bag with an extra set of field clothing (shorts, t-shirt, hat, swim 

suit, mask and snorkel) and personal essentials in the event that your luggage is lost and/or takes several days to 

catch up with you. 

Remember to bring old t-shirts and shorts that you don’t mind getting dirty and possibly ruining. Expect to wear the 

same shorts and t-shirts repeatedly due to lack of laundry facilities. Clothes get ruined in the field; you will NOT 

need any good/nice clothes at the research camp. You might want to save a clean t-shirt and shorts for visiting 

inland sites, but, you don’t need dress slacks or skirts. If you have side trips planned before/after your research trip, 

plan accordingly. 

We have found some diversity among our previous students as to what they think should be mandatory. It varies not 

only with temporal conditions on the island, but also with student comfort when traveling within the developing 

world. The Packing Checklist at the end of this briefing contains recommendations based on our experience with 

over 500 previous students & volunteers. Some folks will require more creature comforts, and others can do without 

some of the recommended items. All volunteers should read this entire briefing carefully, and those who have done 

a lot of traveling can use the information to pack according to their experience. Less experienced travelers should 

bring everything we recommend! 

Note: As the project is stationed on a mangrove island, any trash produced must be burned. There are few recycling 

facilities in Belize. Please help protect the environment by leaving disposable products and plastic packaging at 

home. 


Cultural Considerations 

Belize is predominately a Christian culture. Shorts and t-shirts are fine for both men and women. Swimwear is 

appropriate for beaches, but not for Belize City, where shirts and shoes are recommended at all times. 

Essential Items 

While it is recommended that you pack as light as possible, the following items are essential for participation: bug 

repellent for mosquitoes, oil (Avon Skin-so-Soft , baby oil, or olive oil is recommended) for sand flies, sunscreen 

(15-45 SPF), hat, long-sleeved shirt/cover up for boat, swimsuit, 1-2mm wetsuit or dive skin, and field clothes. 

Please see the Packing Checklist for a complete list of what you will need to take with you. We recommend 

going through the list with a pen or pencil and marking off each required item right before you leave for your 

expedition. 

EMERGENCIES IN THE FIELD 

The researchers and their host, Hugh Parkey’s Belize Dive Connection, are concerned with your health and safety 

during the field course. Minor injuries will be treated onsite using Red Cross First Aid and DAN Marine First Aid 

procedures. We take a precautionary approach to minor illnesses and injuries and will insist on scheduling an 

appointment with a local doctor if the situation does not improve within 24-48 hours after First Aid treatment. 

Volunteers with major illnesses or injuries will be transported to Belize City for medical advice and treatment. 

There is always a boat available for transport in case of an emergency. In case of a life-threatening illness/injury, 

we will take the following steps: 

1) Insure that all students/staff are safe from further injury 

2) Give First Aid/CPR as necessary to stabilize the victim(s) 

3) Contact HP's Belize Dive Connection to report the situation 

4) Transport the victim(s) by boat to Belize City or Contact DAN if indicated 

5) Notify victim’s Emergency Contact at first opportunity 

6) Arrange transportation from the dock in Belize City directly to an emergency care facility, Belize Medical 

Associates 

7) Follow up with HP's Belize Dive Connection as soon as the victim is under professional medical care 

8) Follow up with the rest of the class to keep them informed 

9) Follow-up with victim’s Emergency Contact 

OTHER USEFUL INFORMATION 

• Our Host: Ms. Teresa Parkey, Hugh Parkey's Belize Adventure Lodge, PO Box 1818, Belize City, Belize, 

Central America. Tel: ++501-223-4526 or ++501.223-5086 Fax: ++501-610-5235, E-mail: 

hugh@belizediving.com 

• Do not book your flight until your registration and the course has been confirmed! Expected confirmation date: 

60 days prior to fielding. 

• Airport Code BZE: American Airlines and Continental Airlines fly into Philip S. W. Goldson International 

Airport in Belize City daily; Delta and US Airways also have a more limited schedule. If you are flying from 

the West Coast of the US, you might consider TACA. Round-trip airfare is currently running between US$600- 

$800. 

• You must have a Passport for entry into Belize; if you are a US Citizen you will automatically be granted a 30day 

tourist VISA upon arrival. If you are not a US Citizen, or for additional information, visit the Belize 

Tourism Board Website for additional information: http://www.travelbelize.org/ 

• Consult the US State Department Website for current information regarding travel to Belize: 

http://www.state.gov/p/wha/ci/bh/index.htm 


• Consult the CDC for immunization recommendations: http://wwwnc.cdc.gov/travel/destinations/belize.aspx 

• If you plan to arrive before the rendezvous date or remain in Belize after the departure date, please contact Dr. 

Self-Sullivan, for additional information on travel and accommodations in Belize. You may find the Moon 

Handbook Belize 8 th Edition, by my friend and colleague Josh Berman, a valuable resource, available online at 

Amazon.com. 

• Recommended Field and Travel Guides: 

Birds of Belize (The Corrie Herring Hooks Series), By H. Lee Jones 

Moon Handbooks Belize, 8 th Edition, by Joshua Berman 

Travellers' Wildlife Guides Belize & Northern Guatemala, By Les Beletsky 

Reef Creature Identification: Florida, Caribbean, Bahamas by Paul Humann and Ned DeLoach 

Reef Coral Identification: Florida, Caribbean, Bahamas (Reef Set, Vol. 3) by Paul Humann and Ned 

DeLoach 

Reef Fish Behavior: Florida, Caribbean, Bahamas by Paul Humann and Ned DeLoach 

Reef Fish Identification: Florida, Caribbean, Bahamas by Paul Humann and Ned DeLoach 

• BELIZE time zone: GMT/UTC -6:00; Daylight Savings Time is NOT observed in Belize. 

• Local currency: Belize dollars, however, US dollars are accepted everywhere for a fixed exchange rate of 

US$1 = BZ$2. There is NO NEED to change US$ into BZ$. 

• Electricity: 110 volts AC, 60 Hz, flat two-pin plugs (same as USA). Electricity is only minimally available at 

the project site, although charging of laptops, digital cameras and some small electronics is fine. Students DO 

NOT have Internet access during the course! 

• Language: English, also spoken: Spanish, Maya, Garifuna, Creole 

• Telephone dialing codes: When calling Belize from another country, dial the country’s international dialing 

code (e.g., 011 in the USA), followed by 501 (Belize Country Code) and the number (e.g., 223.4526). When 

calling within Belize, omit the 501, and just dial the number. When calling another country from Belize, dial 

00, followed by the other country’s country code and the number. For example, to call the USA, dial 001+area 

code+number. I will rent a local cell phone upon arrival and text you the number so you can contact me during 

your travel is necessary! 

• Personal conduct: The field course and project are able to remain in Belize due to the courtesy of the people 

and government of Belize. As such, you will be expected to conduct yourselves in a manner that is respectful of 

local sensitivities, customs, and laws. Any violations of Belizean law will be prosecuted in Belize with no 

recourse to foreign laws and attorneys. Any conduct that reflects negatively on project will be grounds for 

immediate deportation at the expense of those involved. 

• Personal funds: Past students have spent a wide range of funds during the course. You will have opportunities 

to shop on at least one of your recreational days. The airport also offers many gift shops in the departure area. 

Small bills are useful (US$1, US$5, US$10) as change will be given in BZ dollars. Traveler’s checks and credit 

cards are more difficult to use, but OK at more and more locations each year. Debit cards may be problematic, 

but VISA and MasterCard credit cards have been used to get cash advances from banks in Belize City. There 

are ATMs, but they appear tied to VISA credit cards only. Larger stores, restaurants and hotels take VISA and 

MasterCard credit cards, but few take American Express. Smaller shops and street vendors only take cash. 

• Tips: As a visitor, it is customary to tip for services in Belize. You are responsible for tipping anyone you think 

gave exceptional service, including but not limited to the field assistants, housekeepers, restaurant staff, 

bartenders, dive master, drivers, tour guides, and boat captains during recreational activities. We generally 

“pass the basket” for tips at the end of each team. 


Essential Items 

PACKING CHECKLIST 

Photocopies of your passport, flight itinerary and credit cards in case the originals are lost or stolen; the 

copies should be packed separately from the original documents 

Passport and Driver’s License and other Photo ID such as your Student ID 

Required Items Necessary for Successful Completion of Coursework 

Laptop Computer with USB port (for pen drive) 

Digital Camera and Underwater Housing 

Copies of articles from your Literature Review 

Copies of all journal articles (included in this briefing) 

Clothing/Footwear for Fieldwork 

Old shorts & old t-shirts 

Lightweight, breathable long–sleeved shirts/pants for protection from sun/bugs 

Sweatshirt, sweatpants, socks in case you get chilled from being in water all day 

2-3 bathing suits (things don’t always dry over-night in the tropics) 

Well worn-in and comfortable walking shoes (sneakers or Teva-like sandals) 

Boat shoes (water shoes or bare feet are recommended on the boat) 

Rain gear or rain poncho 

Hat with wide brim to protect head from sun (very important!) 

Clothing/Footwear for Leisure 

One set of clothing to keep clean for day-off and end of expedition 

Field Supplies 

*****Polarized***** sunglasses with retaining strap 

Bound Field Journal & Copies of Journal Articles 

Small daypack/rucksack/backpack for inland trip 

Dry bag or heavy duty plastic “zip lock” bags for boat (for protecting equipment such as camera from sand, 

humidity, and water) 

Water bottle - 1 liter refillable, such as Nalgene 

Mask, snorkel, and fins if you want to participate in tasks requiring snorkeling, or for snorkeling during free 

time (we encourage you to invest in good quality mask and fins, not the department store variety) 

Dive skin or 1-2mm wetsuit 

Mosquito repellent (with Deet) 


Oil or oil-based repellant (e.g. olive oil, AVON Skin-so-Soft Original Bath Oil, citronella oil repellent, Bit 

Blocker) for sandflies (oil creates a physical barrier from the sand flies; the researchers have found NOTHING 

except oil prevents the sand flies from feasting on you when/if the wind dies) 

A box of mosquito coils (commonly called “fish” in Belize) and a lighter for burning in your room at night to 

keep both mosquitoes and sandflies away 

Waterproof sunscreen with SPF 30 or higher 

Lip balm with SPF 30 or higher, also Blistex ointment if you are prone to fever blisters 

A notebook for your personal field notes and a couple of pencils (unlike ink pens, pencils continue to write even 

if they get wet) 

Personal Supplies 

Toiletries, such as a bar biodegradable soap, deodorant, toothpaste, toothbrush, shampoo, conditioner, and 

moisturizing lotion (no-fragrance types may help reduce the attraction of mosquitoes) 

Antibacterial wipes or lotion (good for “washing” hands while in the field) 

Personal medications, such as vitamins, prescription drugs, emergency allergy injections (Epi-kit), inhalants, 

motion sickness medication and over-the-counter antihistamines and anti-itch products 

Extra contact lenses and saline solution and/or spare glasses (you will need your reading glasses if you wear 

them) 

Miscellaneous 

Cash for snacks, gifts, tips, etc. 

Camera, film/memory cards, extra camera battery/battery charger, and computer cable for downloading images 

from digital cameras 

Laptop computer, power cord, power strip, flash drive or pen drive 

Cell phone with SMS Text Capability if you want to send and receive messages from home 

Optional Items 

Flashlight/torch or headlamp with extra batteries and extra bulb 

Earplugs (your roommates might snore!) 

Duct tape and roll of heavy string 

Very fine gauge mosquito net for hanging over your bunk (also to keep the sandflies out) 

Snack food 

Paperback books/field guides 

Small battery-operated fan with additional batteries 

Battery-operated tape/CD/MP3 player/recorder with headphones (NOT allowed on research boat) 

Binoculars 

Playing cards, board games, musical instruments, etc. 


APPENDIX 

2012 Course Flyer, Syllabus, Registration, & Policy Forms 

Field Journal Requirements 

Final Project Sample Fact Sheets 

Red Mangrove Root Crab 

Cushion Sea Star 

Fiddler Crab 

Patch Reef Habitats 

Brown Pelican 

Variegated Sea Urchin 

Red Fin Needlefish 

Fiddler and Hermit Crabs 



Magnificent Feather-Duster 

Marine Hermit Crab 


Data Sheets for Manatee and Dolphin Research Project 

Faculty Curriculum Vitae 

Journal Club Readings 

Mortimer et al. 2007. Whose turtles are they, anyway? Molecular Ecology 16:17-18 

Blumenthal et al. 2009. Turtle groups or turtle soup: dispersal patterns of hawksbill turtles in 

the Caribbean. Molecular Ecology 18:4841-4853. 

Self-Sullivan. 2000. The Elusive Manatee: An ethological approach to understand behavior of 

the West Indian manatee in Belize. 

Self-Sullivan et al. 2003. Seasonal occurrence of male Antilllean manatees on the Belize 

Barrier Reef. Aquatic Mammals 29.3:342-354. 

Grimm. 2010. Is a Dolphin a Person? News Briefs, Science Magazine, 18-22 February 2010. 

Noren. 2008. Infant carrying behaviour in dolphins. Functional Ecology 22:284-288 

Miksis-Olds et al. 2007. Simulated vessel approaches elicit differential responses from 

manatees. Marine Mammal Science 23.3:629-649. 

Mann. 1999. Behavioral sampling methods for cetaceans: a review and critique. Marine 

Mammal Science 15.1:102-122. 

LaCommare et al. 2008. Distribution and habitat use of Antillean manatees in the Drowned 

Cayes, Belize. Aquatic Mammals 34.1:35-43. 

Kerr et al. 2005. Bottlenose dolphins in the Drowned Cayes, Belize. Caribbean Journal of 

Science 41.1:172-177. 

Jackson. 1997. Reefs since Columbus. Coral Reefs 16:S23-S32 

Harper & Schulte. 2005. Social interactions in captive female Florida manatees. Zoo Biology 

24:135-144. 


Ecology, Behavior, and Conservation of Manatees & Dolphins 

A Unique Field Course in the Belize Barrier Reef Lagoon System 

2012 Session III ~ 4 - 17 August 2012 

Lead Instructor & Principal Investigator: Caryn Self-Sullivan, Ph.D. 1,2 

Co-PI: Katie LaCommare, Ph.D. 2,3 | Visiting Faculty: TBA 

1 Nova Southeastern University, 2 Sirenian International, 3 Lansing Community College 

Want to be a Conservation Biologist, Behavioral Ecologist or Marine Mammalogist? 

Here's your chance to join our research team for two intense weeks of total immersion 

into the world of animal behavior, ecology & conservation, Antillean manatees, 

bottlenose dolphins, coral reefs, mangroves and seagrass beds in Belize! 

Course Overview: This is an experiential learning field course where you will live, work, and study 

from a marine science field station on a pristine, private island off the coast of Belize. Additionally, you 

will visit one or more Community Conservation Sites in Belize. Data collected during the course will 

contribute to our long-term manatee/dolphin research project. You will learn through a variety of 

learning activities, literature review and discussion, independent research projects, and actual field 

research. Be prepared to rise with the sun and spend 8-10 hours outdoors, including 3-4 hours on the 

water each day learning about the tropical Caribbean environment as we explore a maze of mangrove 

islands, seagrass beds, and coral patches searching for elusive manatees and charismatic dolphins. 

Location: Spanish Bay Conservation & Research Center at Hugh Parkey's Belize Adventure Lodge, 

http://belizeadventurelodge.com/ and Sarteneja Alliance for Conservation & Development, 

http://sartenejaconservation.org/. Passport required, immunizations as recommended by CDC 

Your Share of the Costs: US$2995 includes housing, meals, ground & water transfer fees, research & 

materials fees; DOES NOT include airfare, books, tips, and credit hours. 

Credit Hours: The course provides 100 experiential learning and lecture hours in the field, plus 

approximately 35 hours of pre-fielding research and preparation, is comparable to a 3 credit hour 

university course and meets the US DOE criteria in 34 CFR, §600.2. Deadlines: Early registration & 

and deposit due February 1st, 2012; regular registration & deposit due March 1st, 2012; balance due at 

least 60 days prior to field dates. Late payments and late registrations (if space available) incur a $100 

late fee. 

Information Contact: Caryn Self-Sullivan, Ph.D. | +1.540.287.8207 | cselfsullivan@sirenian.org 

========================================================================= 

cselfsullivan@sirenian.org 

540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207 


540.287.8207

Ecology, Behavior, and Conservation of Manatees & Dolphins in Belize 

A Unique Field Course in the Drowned Cayes, Belize 

Summer 2012 SYLLABUS & TENTATIVE SCHEDULE 

Session III: ~ 4 – 17 August, 2012 

Visit us on Facebook: http://www.facebook.com/event.php?eid=370432825564 

Lead Instructor & PI 

Caryn Self-Sullivan PhD 

NSU & Sirenian International 

Phone: 540.287.8207 

Email: cselfsullivan@sirenian.org 

or cs1733@nova.edu 

Co-PI: Katherine LaCommare PhD 

Lansing Community College & 

Sirenian International 

Phone: 248-756-3985 

Email: kslacommare@gmail.com 

or katie.lacommare@umb.edu 

Want to be a Conservation Biologist, Behavioral Ecologist or Marine Mammalogist? Here's your chance to 

join our research team for two intense weeks of total immersion into the world of animal behavior, ecology & 

conservation, Antillean manatees, bottlenose dolphins, coral reefs, mangroves and seagrass beds in Belize! 

Course Overview: This is a total immersion, experiential learning, field course where you will live, work, and 

study from a marine science field station on a pristine, private island off the coast of Belize. Additionally, you 

will visit one or more Community Conservation Sites in Belize. Data collected during the course will contribute 

to our long-term manatee/dolphin research project established in 1998. You will learn through a variety of 

learning activities, literature review and discussion, independent research projects, and actual field research. Be 

prepared to rise with the sun and spend 8-10 hours outdoors, including 3-4 hours on the water each day learning 

about the tropical Caribbean environment as we explore a maze of mangrove islands, seagrass beds, and coral 

patches searching for elusive manatees and charismatic dolphins. Optional SCUBA dives are available as time 

and weather permits; NOTE: additional costs are involved for SCUBA diving. 

PRIMARY LOCATION: Spanish Bay Conservation & Research Center at Hugh Parkey's Belize Adventure 

Lodge, http://belizeadventurelodge.com/ (Passport required, immunizations as recommended by CDC) 

SECONDARY LOCATION(s): Corozal Bay Wildlife Sanctuary, co-managed by the Sarteneja Alliance for 

Conservation & Development, Sarteneja. Alternative 2ndary locations include: Swallow Caye Wildlife 

Sanctuary, co-managed by Friends of Swallow Caye, Caye Caulker; Gales Point Wildlife Sanctuary, Gales Point 

Manatee & Southern Lagoon; South Water Caye Marine Reserve (& Placencia Lagoon), co-managed by SEA 

Belize (formerly Friends of Nature & TASTE); Port Honduras Marine Reserve, co-managed by the Toledo 

Institute for Development and the Environment. 

COSTS: US$2995 includes housing, meals, ground & water transfer fees, research & materials fees; DOES NOT 

include airfare, books, tips, and credit hours. 

OPTIONAL CREDIT HOURS: The course provides 100 experiential learning and lecture hours in the field, 

plus approximately 35 hours of pre-fielding research and preparation; at least 45 of the 135 total hours include 

direct instruction by faculty. This is comparable to a 3 credit hour university course and meets the US DOE 

criteria in 34 CFR, §600.2. You must make arrangements IN ADVANCE with BOTH your advising faculty and 

Dr. Self-Sullivan for credit to be earned through your home university. Credit hour fees must be paid directly to 

your school and you must fulfill any study abroad requirements of your school. This course is divided into 4 

major components: short lectures and learning activities (~1 hour per day), independent reading and assignments 

(~2 hour per day), supervised data collection in the field (~3 hours per day), independent project development & 

implementation (~2 hours per day), presentation of pre-field research (~1 hour per day), and debate/group 

discussion of reading materials (~1 hour per day). 

DEADLINES: Early registration & and deposit due February 1st, 2012; regular registration & deposit due March 

1st, 2012; balance due at least 60 days prior to field dates. Late payments and late registrations (if space 

available) incur a $100 late fee. If you are registering through your home university, earlier deadlines may 

exist—see your academic advisor! 

Marine Mammal Ecology, Behavior, Conservation Field Course, Summer 2012, Page 1 of 5, Revised 4/4/2012

MINIMUM / MAXIMUM CLASS SIZE: 6-24 students 

WEBPAGE: http://www.sirenian.org/2012FieldCourse.html 

Course Objectives: The objectives of this course are to introduce you to the basic concepts animal behavior, 

ecology, and conservation through participation in an ongoing research project, development and implementation 

of your own independent research project; research and presentation on Belizean culture or natural history, 

reading and thinking critically about peer reviewed literature related to course content, and participation in a 

Service-Learning Project. 

COURSE CONTENT (Readings, Lectures, Learning Activities) SUBJECT TO CHANGE DEPENDING ON 

FACULTY 

• Introduction to Trichechus manatus & Tursiops truncatus 

• Participation in long-term research project, results to date, questions for the future 

• Introduction to coral reef, mangrove & seagrass ecology 

• Introduction to Animal Behavior & Conservation 

RESEARCH ACTIVITES 

• Manatees and Dolphins: point transect scans, focal follows, reconnaissance surveys, photo-id 

• Habitat Sampling: seagrass identification to species level, percent cover, density, comparison of 

epibionts, core sampling, feeding scars. 

• Individual or team research project: select from list of approved study subjects and topics below 

Daily schedule: Our schedule is closely tied to sunrise/sunset and tides, with a tentative schedule, below. You 

will be actively engaged from 06:00 until 21:00, daily. Morning and afternoon learning activities and research 

will be rotated as necessary. 

Time Daily Schedule 

6:00 Observing Wildlife, Individual Project Data Collection 

7:30 Breakfast 

8:30 Learning Activities (alternating AM & PM) 

12:30 Lunch 

13:30 Field Research (alternating AM & PM) 

18:00 Journal Club & Happy Hour 

19:00 Dinner 

20:00 Belize Sea to Stars Presentations (20-40 minutes) 

22:00 Quiet Time in the Dorms (Reading/Writing OK) 

23:00 Curfew and Lights Out 

Books & Tools 

We recommend the following books, which are available from Amazon.com: 

The Florida Manatee: Biology and Conservation, by Roger L. Reep and Robert K. Bonde, University Press of 

Florida 

The Bottlenose Dolphin: Biology and Conservation, by John E. Reynolds, Samantha D. Eide, and Randall S. 

Wells, University Press of Florida 

A selection of primary literature is included in the Field Briefing Document. Students are required to print 

out and read this document prior to fielding AND bring it with you to Belize. We encourage you to have this 

done at a print shop, such as FedExOffice-Kinkos and bound with a 1” wire ring (~$35). There is also a library of 

books and archived journals, including Marine Mammalogy, Animal Behavior, and Conservation Biology 

journals, in our library onsite in Belize. 

Marine Mammal Ecology, Behavior, Conservation Field Course, Summer 2011 Page 2 of 5, Revised 4/4/2012

Communication: If you have any questions or concerns, it is your responsibility to communicate with us via 

email or phone prior to travel and in person while at the field site. As your professors, we are here to help you 

learn. But learning is your responsibility. 

CONTACT: Dr. Caryn Self-Sullivan, cselfsullivan@sirenian.org, US +1.540.287.8207, BZ +501.636.3849 

Student Expectations: You should expect us to be enthusiastic about the course material and to be available for 

one-on-one help and feedback. You should expect us to challenge you to think about how & why the course 

material is relevant to you and your career goals. You should expect us to respect you as a person, regardless of 

your academic performance. 

Our Expectations: We expect you to complete all pre-field requirements and readings by the due dates posted in 

the briefing. We expect you to give respect to everyone in Belize, especially at our field site. We expect you to 

fully participate in every course activity, including being present and on time for all meals. We expect you to 

demonstrate enthusiasm and respect for all living organisms in the tropical marine environment. 

Grading Structure: Your final grade is based on a 500 point scale. To determine your “letter” grade, divide 

points earned by possible points: A > 90%; B > 80%; C > 70%; D > 60%. 

• *Independent Research Project (100 pts): Select a topic from approved list** before fielding; do 

background research before departure; design and implement a short-term research project during field 

course; write up results in format of Fact Sheet (see examples from previous students). 

• Field Journal & Reflections (100 pts): Purchase and bring a bound notebook to be used as a field 

journal during the course. Make daily entries following guidelines presented in course; include a 101 

species list. 

• Participation in field and course activities (100 pts): Includes evaluation of your participation in all 

course activities, including discussions, quiz bowls, and personal essay “Why Marine Mammals?” Be on 

time and demonstrate enthusiasm for learning for full points. 

• *Paper discussion and leading (100 pts): Read all papers prior to coming into the field; review in field 

and participate in all discussions; present and lead the discussion as assigned. 

• Service-Learning (50 pts): Either as a class or in mini-groups we will contribute the improvement of the 

island or regional environment. Projects could include picking up garbage in the mangroves, creating 

signage material for education, helping in the Swallow Caye refuge, participating in stranding or 

necropsy, giving a presentation at a local school or civic group, giving a talk to island staff. 

• *Belize from Sea to Stars (50 pts): Each student will prepare a presentation before arrival on some 

aspect of Belize. Topics could include the following**: Art, Astronomy, Culture, Economics, Ecology, 

Geology, History, Languages, Music, Politics and others. After dinner, a student will give an oral 

presentation on their topic. They may prepare handouts but this will not be a power point talk. For full 

points, there should be some interactive activity such as a quiz bowl, role playing, or crossword puzzle. 

These should be informative and interesting to a general audience. The island staff will be invited to join 

us when this is feasible. 

* Requires pre-course reading, research, and communication **See suggested topics at end of syllabus 

Missed and Late Assignments: Each Assignment (pre-fielding and in the field) will have a firm due date and 

time. If you miss the due date/time, you may turn in your assignment late. However, your grade will be reduced 

by 10% per day until the last day of the course. Any assignments not completed by the last day of the course will 

receive zero credit. 

Academic Dishonesty & Plagiarism: Students found violating the conditions of academic honesty will 

receive an F in the course. DO NOT copy & paste text from the Internet or other sources into your 

assignments; DO NOT copy work from your peers; DO NOT paraphrase someone's ideas without giving 

appropriate credit to the source. Plagiarism is a serious offense and will be treated as such. For more 

information on plagiarism see http://en.wikipedia.org/wiki/Plagiarism. 


COURSE FEE & ADDITIONAL INFORMATION 

The course fee of $2995 includes all transportation, meals, and accommodations from your arrival at the PWG 

airport in Belize on the first day of the course to your departure on the last day of the course. Additionally, you 

are responsible for tips, insurance, credit hours, and round-trip airfare to Belize (airport code BZE). 

EARLY REGISTRATION DEADLINE: 1 February 2012 

REGULAR REGISTRATION DEADLINE: 1 March 2012 

LATE PAYMENTS OR LATE REGISTRATION: $100 Late Fee 

To register for course, complete, sign, and send these forms: http://sirenian.org/2012BelizeRegistration.pdf 

http://sirenian.org/2012BelizeSyllabus.pdf 

http://sirenian.org/2012BelizePolicy.pdf 

Download, print, bind, READ, and bring to Belize: http://sirenian.org/2012BelizeBriefing.pdf 

Recruit a friend: http://sirenian.org/2012BelizeFlyer.pdf 

For more information on the course, please email: cselfsullivan@sirenian.org 

For more information on the facilities, please visit: http://belizeadventurelodge.com 

http://sartenejaconservation.org/ 

PRINT STUDENT NAME: ___________________________________________________________________ 

I HEREBY CERTIFY THAT I HAVE READ AND FULLY UNDERSTAND THIS SYLLABUS AND THE 

ADDITIONAL REQUIRED DOCUMENTS LISTED ABOVE. 

STUDENT SIGNATURE: ____________________________________________________________________ 

MY CHOICES FOR BELIZE SEA TO STARS AND INDEPENDENT RESEARCH TOPICS ARE: 

RESEARCH 1 ST CHOICE: 

RESEARCH 2 ND CHOICE: 

RESEARCH 3 RD CHOICE: 

BELIZE 1 ST CHOICE: 

BELIZE 2 ND CHOICE: 

BELIZE 3 RD CHOICE: 

Questions, Concerns, Feedback, Comments: 


Topics for Independent Research Project (100 pts): Select a species and/or ecosystem from list below & get 

approved by Dr. C BEFORE fielding; do background research (primary literature search) in advance so 

that you can design and implement a short-term research project during field course; write up results in 

format of Fact Sheet (see examples from previous students). 

Seagrass ecosystem: Abundant seagrass beds dominated by Thalassia testudinum, with Syringodium filiform, 

Halodule spp., surround the caye, providing an excellent environment for snorkel based investigations. Potential 

projects include ecology or behavior of various organisms within these systems. Suggested species include sea 

stars (Oreaster reticulates), sea urchins (Lytechinus spp.), grunts (Haemulon spp.), needle fish (Strongylura spp.). 

Shallow subtidal mangrove peat banks surround the caye and have well-developed communities of fleshy algae 

(e.g., Caulerpa spp., Dictyota spp.) and calcified algae (e.g., Halimeda spp., Jania spp.) with sparse T. 

testudinum, rose corals (Manicina areolata), and corkscrew anemones (Bartholomea annulata) with symbiotic 

cleaner shrimp (Periclimenes spp.). 

Mangrove ecosystem: The caye is dominated by large perimeter and dwarf central red mangroves (Rhizophora 

mangle) and 2 significant black mangrove (Avicennia germinans) forests, with a scattering of white mangroves 

(Laguncularia racemosa), a few buttonwoods (Conocarpus erectus), and planted coconut palms, providing 

abundant habitat for hermit crabs (Coenobita clypeatus) and fiddler crabs (Uca spp.); we also sight mangrove 

crabs (Aratus pisonii), snails (Littoraria angulifera), mangrove root crabs (Goniopsis cruentata), and ghost crabs 

(Ucides cordatus), mangrove rivulus fish (Rivulus marmoratus), and giant termite nests (Nasutitermes spp.), 

unidentified bat species locally called rat bats that are thought to roost in the coconut palms during the day but can 

be observed foraging on insects at dusk and dawn, and many birds including the mangrove warbler, golden 

fronted woodpecker, osprey, common black hawk, egrets, and herons (see bird list). The central pond of on this 

caye is strongly influenced by diurnal tides, fluctuating from a mud flat at low tide to about 30cm of water at high 

tide and would make a good independent variable for natural experiments. 

Belize from Sea to Stars (50 pts): Each student will prepare a presentation before arrival on some aspect of 

Belize. Topics could include the following: Art, Astronomy, Culture, Economics, Ecology, Geology, History, 

Languages, Music, Politics and others. After dinner each night, one or more students will give oral presentations 

on their topic. This is NOT a Power Point presentation! Ideally, there should be some interactive nature such 

as stargazing, quiz bowl, role playing, or crossword puzzle. These should be approximately 20-40 minutes long, 

informative and interesting to a general audience. The island staff will be invited to join us when this is feasible. 

Once you have selected your topic, you must register it with Dr. C to prevent replication of topics by students. 

For some interesting issues in Belize search the following topics in association with Belize: 

Lethal Yellowing Disease, Coral Bleaching 

Business Ventures: Chalillo Dam, BEL, Fortis; Cruise 

Ship Industry explosion; sugar and banana industries 

Glow Worms and Bioluminescence (Odontosyllis 

luminosa, Dr. Gary Gaston); Pica Pica and Thimble 

Jellies 

Parliamentary Government: UDP vs. PUP 

Meteor Showers, the Southern Cross and other 

Astronomical Views 

Culture: Maya, Garifuna, Kriole/Creole, Mestizo, 

Mennonites 

Geography: 5 Oceanic Ridges and the Atolls 

Local NGOS: BACONGO, TIDE, TASTE, Friends of 

Nature, Belize Audubon, Wildtracks, Sharon Matola and 

the Belize Zoo 

Some Famous People from Belize: Baymen of Belize and 

the 1798 Battle of St. George’s Caye, Baron Bliss, Andy 

Palacio, George C. Price, Marion Jones, Jamal Shyne 

Barrow, Evan X Hyde, Zee Edgell, Milt Palacio, Said 

Musa, Dean Barrow 

Conservation in Belize: Protected Areas, Hicatee Turtles, 

Coral Reefs, Harpy Eagle, etc. 

Xaté (sha-tay): leaves from three Chamaedorea palm 

species (C. elegans, C. oblongata and C. ernesti-augustii) 

used in the floral industry 

Belize-Guatemala Border Dispute 

Music: Stonetree Records 

Destinations: Caye Caulker, San Pedro, Placencia, 

Orange Walk, Punta Gorda, Dangriga, Belmopan, 

Corozal, Bermudian Landing, San Ignacio, Benque Viejo, 

Hopkins, Crooked Tree, Sarteneja 

Maya Archeological Sites: Xunantunich, Cahal Pech, 

Lamani, Altun Ha, Caracol, El Pilar, Lubaantun, Nim Li 

Punit, Actun Tunichil Muknal, Cerros, Tikal (Guatemala) 

Food: Sere, Hudut, Escabeche, Rice and Beans, Beans 

and Rice, Cowfoot Soup, Johnny Cakes, Creole Bread, 

Powder Buns, Black Cake, Dukunu, Meat Pies, Relleno, 

Stew Chicken, Garnaches, Salbutes, Panades, Tambrand 

Candies, Gibnut, Bamboo Chicken, Marie Sharp’s, Boilup, 

etc. 

Invasives: Lionfish Pterois volitans, ?P. miles 


Ecology, Behavior & Conservation of Manatees and Dolphins 

A Unique Field Course in the Drowned Cayes, Belize 

Session III: August 4-17 2012 

Step 1: PRINT & COMPLETE THIS FORM - ALL PRICES ARE IN $US 

Step 2: Mail, Fax, or Scan & Email the SIGNED registration, syllabus, transcripts & policy forms 

Step 3: I will send you and invoice, which you can pay online or by mail 

Mailing Address, Email Address, and Fax: 

Caryn Self-Sullivan, 200 Stonewall Drive, Fredericksburg, VA 22401-2110 

Phone: 540.287.8207 | Fax: 888.371.4998 (Country Code 001) 

Email: Caryn Self-Sullivan (cselfsullivan@sirenian.org) 

Name: 

Mailing Address: 

City, State, Postal Code, Country: 

Email Address(es): 

Cell & Home Phone #s: 

(cell) (home) 

Why do you want to participate in this course? You do NOT need to be currently enrolled in school, however describe your academic status & highest 

degree. Don't forget to send unofficial copies of your transcripts and answer questions on page 2: 

Openings available only in Session III Fee 

Session I: 26 May - 8 June 2012 $2,995 

Session II: 16 June - 29 June 2012 $2,995 

Session III: August 4-17 2012 $2,995 

Note: If you register for more than one session, you will be responsible for expenses b/t sessions! 

Total Cost (excludes airfare, credit hours & tips) 

DEPOSIT (Minimum $500) Due now; I will invoice you upon receipt of registration! 

Low-income Country Scholarship* $500 

Early Registration & Recruiting Discounts* (Max $100) 

Late Payment / Late Registration Fee $100 

Balance due at least 60 days prior to fielding 

* Attach a 1500 word essay describing how this opportunity will enhance both your personal career goals AND 

sirenian research, educational outreach, and conservation in your home country 

** $100 discount if you register and submit $500 deposit by February 1st; $25 discount each for you and a friend, for 

each friend you recruit, provided you and your friend(s) register and submit $500 deposit by March 1st; $25 discount if 

you register and pay in full by March 1st ; Mix and Match discounts for up to a maximum total discount of $100. 

By signing below, I hereby promise to pay the price indicated above subject to qualified discounts 

and the refund policy as stated in the Syllabus. I understand that I will be invoiced for the deposit 

immediately, and balance is due at least 60 days prior to fielding. Invoices will be sent via PayPal 

from "MIB: Research & Educational Expeditions." A $100 fee will be assessed for returned checks 

or chargebacks. 

Signature ____________________________________________________________________ 

Comments or Questions:

Please provide the following information about yourself. Use additional pages if necessary! 

* Gender: 

* Date of Birth: 

* Citizenship: 

male female (circle or highligh) 

** Passport Country and Number: 

** DAN Preferred Membership Number: 

*REQUIRED at time of application **REQUIRED at least 60 days prior to fielding 

Are you currently enrolled in school? Please give details about your status and program of study. Attach additional 

pages if necessary! 

Do you want/need credit for this course? How many hours? 

If yes, please provide contact information for your academic advisor: 

Name: 

Department: 

University: 

Phone: 

Email: 

Are you SCUBA Certified? YES NO 

If yes, provide a copy of your Certification Card and DAN Card. 

Tell us about other field courses or field work you have done: 

What should we know about your history (allergies, dietary restrictions, psychological conditions, physical or chronic 

conditions, etc.) that might affect your ability to participate in this course? 

Why did you chose this course? What are you expectations? Do you have any specific background, skills, or talents? 

Attach additional pages if necessary! 

Tell us about your experiences working with teams, with different cultures, or other situations that demonstrate your 

adaptability. Use additional pages if necessary! 

Circle or highlight your current swimming ability: 

non-swimmer recreational swimmer strong swimmer life-saving certificate 

Circle or highlight your comfort level in the ocean: 

not at all comfortable in calm seas comfortable in choppy seas 

Describe any life saving training you have done, include dates (Red Cross, First Aid, CPR, EMT, etc.)? 

What kind of snorkel, SCUBA, and/or boating experience (power, sail, kayak, etc.) do you have?

2012 Field Course Policy & Liability Release Form 

Ecology, Behavior & Conservation of Manatees & Dolphins in Belize 

August 4-17, 2012 

Field Class Policy & Liability Release 

COMPLETE, SIGN, INITIAL, AND RETURN BY REGISTRATION DEADLINE 

As your instructors, it is our responsibility to ensure that students, staff, colleagues, and associates are familiar 

with and understand field course policies. As a student participant, you are required to read, fill out, and sign 

this document where indicated. Please feel free to contact me if you have any questions about our Field Class 

Policy & Liability Release Form. 

Return this signed document via mail, FAX, or Email at the same time you submit your Registration and Signed 

Syllabus (page 4 only). Also, be sure to send copies of your Passport, Dive Card, DAN Card, and Flight 

Itinerary ASAP, but not later than 60 days prior to fielding, to: Caryn Self-Sullivan, 200 Stonewall Drive, 

Fredericksburg, VA 22401-2110; Email: cselfsullivan@sirenian.org; Phone: 540.287.8207; FAX: 888.371.4998 

As Principal Investigator and Lead Instructor, I am responsible for: 

• ensuring policies are followed; 

• ensuring that risks are minimized to the best of my ability; 

• ensuring that students or staff are removed from the course if they, in my sole judgment, are in violation of these 

policies and/or present a danger to the safety and/or success of the course. 

Should a student become seriously injured or leave the course early for any reason, I will inform the student's emergency 

contact that they have left the course and why. Your signature below authorizes me to do so! Please complete your 

emergency contact information: 

In case of emergency or my removal from this course, please contact the following person(s): 

Name(s): __________________________________________________________________________________ 

Address: __________________________________________________________________________________ 

Phone(s): __________________________________________________________________________________ 

Email(s): __________________________________________________________________________________ 

Relationship to Student: ______________________________________________________________________ 

Student Signature: ___________________________________________________________________________ 

CONSENT TO INHERENT RISKS 

Some of the characteristics that make a field course attractive to students may also put the student or their property at risk. 

To reduce this risk, all services from arrival to and departure from Philip S. W. Goldson International Airport (PGIA, 

airport code BZE) are provided by Hugh Parkey's Belize Dive Connection (BDC), which has over 20 years of experience in 

Belize and also has liability insurance in place. 

Each student agrees to purchase international medical travel insurance in the form of a DAN Preferred Membership 

(Divers Alert Network) to cover his/her expenses in case of an emergency. This policy can be purchased online at 

http://www.diversalertnetwork.org/ under the MEMBERSHIP tab. Sign up as an Individual (not a student) and select the 

BEST: Preferred Membership Plan ($110). Note: you do not have to be a certified diver to purchase DAN Preferred 

Membership. Some of the potential risks inherent to this course are listed below. Initial Here: Yes ____ No ____ 

Climate: Students must be prepared to spend long days in hot, humid, and wet conditions. The tropical sun is very strong. 

Risks include dehydration, sunburn, and other heat related illnesses. Students agree to take precautions as advised by 

instructor and staff to prevent illness. Students agree to notify instructor immediately if they are feeling ill. 

Insects: Sand flies and mosquitoes can be problematic on the caye. Sand flies are believed to be a vector for leishmaniasis 

in some regions of Belize, but this has not been reported for the cayes. Mosquitoes may transmit a number of diseases (see 

Diseases below). Botflies (Dermatobia hominis) are also reported in Belize, and mosquitoes may transmit their larvae to 

human hosts where the larvae will grow and develop. This is not life threatening, but can be painful and unpleasant. 

Students agree to keep instructor informed of insect bites. 

Page 1 of 4 Updated by CSS on 4/4/2012


Marine life: Fire corals, several species of stinging jellyfish, sharks, sea urchins, lionfish, and other potentially dangerous 

marine organisms can be found in the study area. These can inflict painful and occasionally severe stings or bites, which 

may become infected if untreated. Those with a serious allergy to bee or wasp stings may have a similarly dangerous 

reaction to corals and jellyfish. The best prevention is to avoid touching unfamiliar plants & animals. Students agree to 

notify instructor immediately if they are injured as a result of an interaction with marine life. Students with known allergies 

must notify instructor on this form and bring their own medications and an 'epipen' as prescribed by their physician. 

Snorkeling: All the inherent risks of snorkeling are obviously present, including the effects of environmental conditions, 

marine life and other risks specific to your own physical/medical history. Snorkeling is optional. Students who chose to 

snorkel should bring their own gear (mask, snorkel, fins, wet suit or skin) and know how to snorkel safely without 

hyperventilating. A snorkel "check-out" by the instructor will be conducted on day 2 of the course. 

Boats: We will be aboard a small fiberglass boat for all fieldwork. All boats should have ladders and a bimini cover for 

sun protection; however, in some instances we may use a boat that lacks a ladder or shade. Deck surfaces of boats will 

become slippery and may place you at risk of slips, falls, and injuries that result from these accidents. All boats are operated 

by a licensed captain, employed by BDC. Students are not allowed to operate boats during the expedition. 

Disease: Diseases found in tropical regions include malaria, dengue fever, filariasis, leishmaniasis, onchocerciasis, 

trypanosomiasis (Chaga’s disease), schistosomiasis, leptospirosis, rabies, brucellosis, hepatitis, and typhoid. Most diseases 

are preventable with basic safety cautions. Students certify that they have sought professional advice from a physician, 

local health department, or international travel clinic regarding immunizations against diseases. 

Driving: Driving conditions in Belize are considered poor by US standards and pose inherent risks. All land transfers will 

be done by licensed drivers, employed by Hugh Parkey's Belize Adventures. Students will not be permitted to drive during 

the expedition. 

INTELLECTUAL PROPERTY RIGHTS 

Students may share photos, videos, and stories of the expedition with family, friends, local media, and in public forum for 

educational outreach purposes. 

However, all information (data and images) shared or gathered during the expedition remains the intellectual property of PI 

Caryn Self-Sullivan (CSS) and Co-PI Katherine S. LaCommare (KSL). Students are strictly forbidden from co-opting or 

plagiarism of data, images or information gathered during an expedition for use in a scientific thesis, masters or PhD work, 

for profit, or for the academic or business use of a third party without the express written permission of CSS & KSL. 

Students are aware that data gathered during the interviewing of local people becomes the intellectual property of CSS & 

KSL. 

Students are sometimes required to submit a written report reflecting what they have learned on a project, sometimes as a 

step toward receiving credit at their home institutions. Permission is hereby granted to students to use data and images for 

this purpose. 

LIFESTYLE CHOICES 

Our course does not discriminate on the basis of race, religion, ethnicity, or sexual orientation; and we respect students' 

rights to privacy. However, students should be warned that their lifestyle decisions may offend or clash with the 

sensibilities of local residents in our area of operations, or potentially violate local laws. Further, certain lifestyle decisions 

and behavior that impacts fellow students or the instructor may result in an uncomfortable, hostile and/or unproductive 

work environment. 

To ensure enjoyable and productive work conditions and smooth relations with local peoples, we have established the 

following code of conduct. Beyond practicing cultural sensitivity and showing common courtesy, please be mindful of the 

following limitations, and please remind and encourage all participants to practice sensitivity, courtesy, and compliance 

with these policies. 

Fraternization: Instructors, staff, colleagues, and associates are prohibited from becoming intimately involved with 

students during the duration of the field course. Romantic relationships between students that may otherwise seem 

permissible often create an unpleasant and/or unproductive work environment and are therefore strongly discouraged for 

the duration of the field course. 

Sexual Harassment: The inter-personal dynamics that exist between field course instructors, staff, and students are 

considered student-teacher relationships. Therefore, please be aware of the following policies. 

• Sexual harassment of students by the instructor or staff is prohibited. 

• Likewise, sexual harassment of the instructor, staff, other students, or local people by students is also prohibited. 



Sexual harassment infringes on an individual’s right to an environment free from unsolicited and unwelcome sexual 

overtones of conduct either verbal or physical. Sexual harassment does not mean occasional compliments of a socially 

acceptable nature. Sexual harassment refers to conduct which is offensive, which harms morale, or which interferes with 

the effectiveness of field courses and research expeditions. Such conduct is prohibited. Lewd or vulgar remarks, 

suggestive comments, displaying derogatory posters, cartoons or drawings, pressure for dates or sexual favors and 

unacceptable physical contact or exposure are examples of what can constitute harassment. It is important to realize that 

what may not be offensive to you, may be offensive to other students, the local population, staff members, or an instructor. 

Any individual who feels subjected to sexual harassment or has any knowledge of such behavior should report it at once to 

his or her instructor or staff members. All reports of sexual harassment will be handled with discretion and will be 

promptly and thoroughly investigated. Any student who is found to have engaged in conduct constituting sexual 

harassment will be removed from the course immediately. Any expenses involved in an early departure from the course are 

the responsibility of the student. 

Drugs: The manufacture, possession, use, purchase and/or sale of illegal drugs as defined by the United States Code and/or 

Belize Law is strictly forbidden while participating in this field course. Prescription drugs may only be purchased and used 

by the individual indicated on the prescription, in keeping with the intended use guidelines. 

Alcohol: Instructors and staff members are in a position of leadership and must therefore always be prepared to make 

responsible, timely decisions in any situation that may arise. If you decide to consume alcohol after course work and 

research has concluded for the day, please exercise your best judgment. Please respect local laws and customs. 

Intoxication can jeopardize your own safety, in addition to that of other students and staff. 

Students who are US Citizens must be a minimum of twenty-one (21) years old to consume alcohol. Be prepared to show 

your identification to the HP staff prior to the purchase of alcoholic drinks. Per day limits on alcohol consumption are in 

place during the course. In addition, restrictions on the use, possession, sale, or purchase of alcohol are solely at the 

discretion of the instructors. Local statutes, customs, practices, ordinances, and regulations with regard to the use, 

possession, sale, or purchase of alcohol are applicable to all students, instructors, and staff participating in this course. 

The instructor has the discretion to remove individuals from the course who consume alcohol in a time and manner that 

endangers the safety and/or productivity of other students, staff, the course, or any expedition. 

RECREATIONAL DAYS 

As an instructor and part-time resident of Belize since 1998, we (CSS & KSL) are familiar with local conditions and 

activities that may place the student at risk. Depending on the size of the student body, students may be given options for 

recreational day activities, but all activities must be conducted through BDC or their authorized agents. Potentially 

dangerous recreational day activities will not be allowed, as they may jeopardize your safety, the safety and well being of 

students, and ultimately, the success of this long-term research project. 

Students will occasionally have unsupervised free time before and after classes & discussions/field trips/research sessions. 

Activities undertaken during unsupervised time will be at your own risk. 

IN THE EVENT OF AN EMERGENCY: GOOD SAMARITAN ACTIONS 

In the event of emergencies, instructors, staff, and students must make certain judgments. While we have made an effort to 

ensure that qualified people make the most informed decisions possible, occasionally First Aid must be administered and 

other immediate steps taken by expedition participants who are not officially certified to make these decisions. We have 

safety protocols and emergency procedures in place. However, in rare, unforeseeable emergency situations, you are not 

restricted from exercising your best judgment with regard to your own safety. We do not restrict “good Samaritan” 

actions, or actions taken to assist fellow participants during emergency situations in the field. In the event of an unforeseen 

contingency that has not been provided for in BDC's emergency plan, we will take all reasonable steps to assist students 

and each other, with the understanding that we do not expect you to take steps that unreasonably jeopardize your own 

safety or that of others. 

STUDENTS AND DRIVING 

Students are not allowed to drive project vehicles or boats during the field course. Students may not transport themselves, 

other students, staff, or equipment in a vehicle of any kind, including their own. Students may only drive a project vehicle 

or boat, transport other students or perform errands in the field in case of an emergency and when no authorized drivers are 

available. 


SCUBA, DIET, ALLERGIES 


I (AM) or (AM NOT) (circle one) certified to dive using SCUBA equipment by _________________________ 

_________________ (certifying organization). If certified, my certification level is ______________________; 

my certification number is ____________________; and I have attached a copy of my Dive Card to this form. 

Dietary Preferences (circle one): Vegan Vegetarian Carnivore Omnivore 

Allergies (circle one): NONE FOOD (list below) DRUGS (list below) OTHER (list below) 

REFUND POLICY 

I hereby acknowledge that if I cancel my registration before May 1 st , I will receive 100% of my deposit less a 

$50 service fee to cover bank and processing costs. If I cancel between May 1 st and June 1 st , I will forfeit my 

$500 deposit, but will receive a full refund of any balance paid above the deposit, less a $50 service fee. No 

refunds will be given after June 1 st . However, if the course is canceled by the instructor for any reason, I 

understand that I will receive a full refund of all payments made. I agree that I will NOT purchase my airfare 

until the instructor has confirmed that the course has made minimum enrollment. Initial Here: Yes ____ No ____ 

PERMISSION TO RELEASE YOUR IMAGE AND INFORMATION 

I hereby consent to Caryn Self-Sullivan, the Hugh Parkey Foundation, and Belize Dive Connections releasing or 

using photographs of me taken during my field course & research expedition. Initial Here: Yes ____ No ____ 

I hereby consent to Caryn Self-Sullivan releasing or using information gathered about me in the course of my 

field course & research expedition, except for contact and medical information and/or information that is 

otherwise agreed to be kept confidential. Initial Here: Yes ____ No ____ 

ASSENT TO POLICIES 

I have read and understand the policies, rights, and responsibilities expressed in this document. I accept the 

policies above as a condition of participating on this field course and I accept the consequences described above 

for gross negligence or serious violations of course policies. 

RELEASE OF LIABILITY 

Student Signature: _____________________________________Date: ____/____/____ 

I understand the potential hazards and risks attendant to the field course that is described in the syllabus, course 

briefing, and this policy document. By signing below I agree to participate in the field course at my own risk. I 

declare that I am in good health. I declare that I, and my heirs, in consideration of my participation in the 

Ecology, Behavior & Conservation of Manatees, Dolphins, Turtles field course from 18 th to 31 st May 2011 in 

Belize, hereby release Caryn Self-Sullivan, course instructors, and visiting scientists from any and all liability 

for damage to or loss of personal property, sickness or injury from whatever source, legal entanglements, 

imprisonment, death, or loss of money, which might occur while participating in this course. I am aware of the 

risks of participation, which include, but are not limited to, the possibility of injury or death. I hereby state that I 

am in sufficient physical condition to accept a normal level of physical activity during long-term exposure to the 

sun and heat. I understand that participation in this program is strictly voluntary and I freely chose to participate. 

I understand that the course does not provide medical coverage for me. I verify that I have purchased travel 

insurance equivalent to DAN Preferred Membership and that I will be responsible for any medical costs I incur 

as a result of my participation. 

However, I do not release Caryn Self-Sullivan, course instructors, and visiting scientists from liability on 

account of any injury, loss, or damage to me directly caused by the gross negligence or wanton or reckless 

misconduct of Caryn Self-Sullivan, course instructors, and visiting scientists. 

Student Signature: _____________________________________Date: ____/____/____ 


FIELD JOURNALS 

You are required to keep a permanently bound field journal or notebook (no loose leaf binders) in 

addition to having a notebook for your course notes. We encourage you to make daily entries following 

guidelines presented here and to include a “101 Species List” in the back of the journal. Your goal is to 

identify at least 101 organisms to the species level during the course including the 3 most prominent sea 

grass species, 4 mangrove species, common birds, fish, corals, reptiles, and insects. Your list should 

include common name, Genus and Specific Epithet, Phylum, identification keys, and a sketch. You will 

use information from your journal to complete your final exam, which will be in the form of a scavenger 

hunt! 

Memories are ephemeral and perceptions change with time, thus you should have your field journal with 

you at all times during to document your field experience, journal readings, and research efforts. Some 

researchers tend to write rough field notes in their journal while in the field, and then write a more 

complete description and expand on their observations each night after the fieldwork--in the same journal. 

This method has the advantage of allowing you to recognize what type of information you are omitting 

from your field notes and make sure you collect those data in the future. 

Your journals must be neat, legible and have appropriate spelling, etc. We recommend using a pencil or 

permanent ink pen (i.e., Pigma pens, Rite-in-the-Rain, etc.) since we may be in situations in which the 

pages of your journal will get wet. Most local stores that carry office supplies also have journals that are 

waterproof. While that type of journal is not required, it is encouraged. 

Drawings and sketches are an invaluable addition to your journal. Even the lousiest artist (like me :-) can 

make a decent field drawing in about 2 minutes. Start with the sea grasses and mangroves, then move on 

to the animals! A portion of your final grade will be based on the completeness, legibility, and accuracy 

of your journal. Also, do not erase incorrect entries but strike through them with a single line and write 

any correction above or below the original entry. 

A good field journal includes time, date, place, conditions, guests, professors, and other information at the 

heading of each entry. Entries should include information about each site and details about field 

techniques as well as information about your activities and data collection during your research project. 

In addition, entries should contain reflective thought about how you feel about the experience. 

Finally, you should always include contact information for anyone you meet in the class or the field as it 

may assist you in future endeavors. We are happy to review your journal at any time and it will be 

collected briefly and graded on the last day of class. 

Things that must be included in your journals: 

1. Your name, phone number, email and permanent address 

2. The names and contact information for your research partner 

3. Dates, times, weather conditions, and location of all field activities that are of sufficient detail to 

be replicated 

4. Name and contact information for every researcher or staff member that provides you information 

(including Belizeans!) 

5. Descriptions of field trips with detail on methodologies learned that would allow replication 

directly from your notebook 

6. Brief summaries of your daily activities 

7. All data and summaries of your thoughts regarding your individual research projects 

8. Your thoughts and reflections about each of the field experience 

9. Complete citations and notes from any sources (readings, etc.) so you can reference them in the 

future 

By J. Young (2010), Revised by C. Self-Sullivan (2011)

Red Mangrove Root Crab 

Goniopsis cruentata 

Hana Bucholz and Meagan Wise 

Edited by Caryn Self-Sullivan, Ph.D. 

Ecology & Behavior of Manatees & Dolphins in 

Belize, Class of 2009 (contact: caryns@sirenian.org) 

Taxonomy 

Kingdom Animalia 

Phylum Arthropoda 

Class Crustacea 

Order Decapoda 

Family Grapsidae 

Genus Goniopsis 

Species Goniopsis cruentata 

Ecology 

One of the more elusive crab species on Spanish 

Lookout Caye is the mangrove root crab 

(Goniopsis cruentata). Also known simply as 

the root crab, this brightly colored crab (purple, 

red and orange with white spots) lives among 

the red mangrove roots and branches. During 

low tide, you can find it beneath the red 

mangrove roots (Rhizophora mangle) and 

pimento stakes along the island’s central 

causeway. According to Feller (1996), these 

crabs have been observed feeding on mangrove 

propagules, insects, and organic material. In 

fact, mangrove root crabs may affect the 

distribution red mangroves. Little is known 

about the mangrove root crabs on Spanish 

Lookout Caye. 

Physical Description 

According to Kaplan (1984), the root crab is 

about 2.5 inches long and has stalked eyes, a 

brown carapace with white spots, and hairy red 

legs with white or yellow spots. Female crabs 

have a wide abdomen for egg storage, and males 

have a thin abdomen (Coulombe 1984). At 

sexual maturity, females and males are roughly 

the same size (Oliveira 2004). 

Conservation 

Any impact that significantly alters the red 

mangrove ecosystem may affect the red 

mangrove root crab because of its dependence 

on mangroves shelter and food. Worldwide, 

Figure 1. G. cruentata under red mangrove root on SLC 

mangroves are threatened by sea level rise, 

development, pollution, dredging, and disease. 

In Belize, the greatest threat is probably 

unsustainable development. 

Behavior 

When crabs mate, the female stores the male’s 

sperm until she releases her eggs. The eggs are 

kept in a mass (sponge) on the abdomen of the 

female and released simultaneously with the 

stored sperm, which flows over and fertilizes the 

eggs. Zygotes develop through four phases: 

fertilized egg, zoea larvae, megalops larvae, and 

adult (Coulombe 1984). Through personal 

observations we discovered that when mangrove 

root crabs are disturbed these crabs remain 

motionless for a short period of time before 

moving quickly sideways into a nearby burrow. 

If the crab does not automatically move away, it 

will bring its front claws forward in a defensive 

position. 

Figure 2. G. cruentata in Dominican Republic (photo by 

Pedro Genaro Rodriguez) 

Hugh Parkey Foundation for Marine Awareness & Education (belizeadventurelodge.com) 

Sirenian International (sirenian.org)

OUR INVESTIGATION 

Figure 2. G. crutentata on mud flat at SLC, 6 June 2009 

Introduction 

Red mangrove root crabs provide food for other 

species and reduce the insect population within 

the red mangrove ecosystem. By eating the leaf 

litter and organic material around the mangrove 

roots, they contribute to the recycling of 

nutrients. During our island orientation walk, we 

noticed these beautiful crabs and decided to 

investigate them further. 

Methods 

We conducted surveys each morning at 0600hrs 

for ten days during June 2009. For 

approximately one hour each morning, we 

walked the SLC central causeway, scanning the 

area on either side of the causeway, to observe 

the location and behavior of red mangrove root 

crabs. 

Results 

During low tides, G. crutentata were both near 

the mangrove roots and on the mud flat some 

distance away from the mangrove roots. At high 

tide, when there was no mud flat and the 

mangrove roots are partially submerged, crabs 

were observed only on structures above the 

water line, including roots, cement blocks, 

wooden planks, pimento stakes, and piles of 

emergent mud. They were predictably observed 

at certain locations and generally found alone or 

at least 30 cm away from any other crab. 

To better understand the distribution and 

behavior of G. crutentata on SLC, we propose 

the following sampling design for future 

students. 

Effect of Tidal Variation on Distribution and 

abundances of the Red Mangrove Root Crab 

on Spanish Lookout Caye, Belize 

Hypothesis: Tidal variations influence the 

abundance of the Red Mangrove Root Crab 

(Goniopsis cruentata) in the Spanish 

Lookout Cayes, Belize. 

Methods: Collect data during two complete 

lunar cycles, one during the dry season 

(February-April) and the other during the wet 

season (May-November). Conduct walking 

surveys three times a day at high tide, low tide, 

and intermediate tide. Each survey should 

include one transect along the central causeway 

in a single direction, one person on either side of 

the board walk scanning for crabs. Each person 

will observe both the area around the roots and 

in the water. The number and location of crabs 

will be recorded on a map of the area. At the 

beginning and end of each bridge along the 

causeway, water depth, salinity, temperature, 

and wind speed will be recorded. General 

observations, such as precipitation and debris 

will also be noted. 

If our hypothesis is true, then we expect more 

sightings of red mangrove root crabs at low tide 

than at high or intermediate tides. 

Literature Cited 

Coulombe, D. A. 1984. The Seaside Naturalist. 

Simon and Schuster. New York, New York. 139. 

Feller, I. C. 1996. Effects of nutrient enrichment 

on leaf anatomy of dwarf Rhizophora mangle 

L.(red mangrove). Biotropica 28: 13-22. 

Feller, I. C., Sitnik, M. 1996. Mangrove Ecology 

Workshop Manual. 

Kaplan, E. H. 1988. Southeastern and Caribbean 

Seashores. Houghton Mifflin Company. Boston, 

New York. Plate 22. 

Oliveira, N. F., Coelho, P. A. 2004. Maturidade 

sexual fisiológica em Goniopsis cruentata 

(Latreille) Crustacea, Brachyura, Grapsidae) no 

Estuário do Paripe, Pernambuco, Brasil. Revista 

Brasileira de Zoologia 21 (4): 1011–1015. 




Oreaster reticulates 

Jessica Barth and Aarin C. Allen 

Edited by Caryn Self-Sullivan, Ph.D. 



Taxonomy 


Phylum Echinodermata 

Class Asteroidea 

Order Valvatida 

Family Oreasteridae 

Genus Oreaster 

Species Oreaster reticulatus 

Ecology 

Cushion sea stars are found in the Atlantic 

waters from the Carolinas to Brazil (Puglisi, 

2008). Juveniles are green in color and can 

reach up 15cm in diameter (Kaplan 1982). 

Adults are tan, orange or rust in color and can 

grow to 50cm (Figure 1). 

O. reticulates is an omnivore, feeding on 

copepods, crab larvae and sponges (Puglisi 

2008). They are found in the calm shallow 

sandy flats around turtle grass, usually in 

shallow waters (Kaplan 1982). However, they 

have been found at depths of 37 meters (Puglisi 

2008). 

In Belize, they are ubiquitous in the seagrass 

beds where they are considered detritus feeders 

(C. Self-Sullivan, pers. comm.) 

Figure 1. Juvenile, adult, not to scale (Belize 2009). 

Behavior 

While feeding, cushion sea stars use their 

suction cup-like tube feet to wrap around their 

prey. In times when food availability is low the 

Figure 2. Six-armed specimen (Belize 2009). 

cushion sea star will prevent starvation by 

reabsorbing its own body tissue, which 

ultimately leads to a decrease in the sea stars 

overall size (Puglisi 2008). 

The species reproduces annually in the summer 

but can be found spawning continuously in the 

warm waters of the tropics (Puglisi 2008). The 

larvae can travel far distances in the ocean 

current before settling into a sea grass bed 

(Puglisi 2008). 

If a sea star is injured, it has the ability to 

regenerate its arms, as long as some portion of 

the central disk remains viable (Kaplan 1982), 

occasionally resulting in the production of an 

extra arm (Figure 2). 

Conservation 

O. reticulates was once the most common sea 

star in the Caribbean but is currently found most 

often in areas where the human population is 

relatively low. The species is considered to be 

rare in areas of high human populations due to 

being over harvested for souvenirs and 

aquariums (Puglisi 2008, Kaplan 1982). 




Introduction 

The Hugh Parkey Foundation for Marine 

Awareness and Education hosted our 2-week 

field course in June of 2009. At our base station 

on Spanish Lookout Caye (SLC, a 186 acre 

mangrove island just east of Belize City), we 

immediately noticed many bright orange sea 

stars in the seagrass beds just off the western 

shore of the caye. However, we didn’t see any 

off the eastern shore. This led us to ask why 

more sea stars were observed on the western 

than the eastern side of this pristine mangrove 

island. 

Methods 

The eastern shore of SLC faces windward, 

overlooking the Belize Barrier Reef and 

Caribbean Sea. This side of the caye is subject 

to more wind and wave action than the western 

shore, which overlooks the Belize mainland, 

about 10 miles west of SLC. To confirm our 

initial observation, we snorkeled along both 

sides of the caye once a day for ten days, 

counting cushion sea stars. Our snorkel 

transects were approximately 100m long and 

approximately 5m offshore. 

During our snorkels, we also noted the color, 

size, and behavioral state of each individual sea 

star, along with the depth and substrate at which 

they were found. We simulated turbulent 

conditions by placing individuals on their backs, 

and observing their behavior. 

Results 

During the surveys, we found no sea stars off the 

eastern side of the island, but many sea stars off 

the western side. On average, we observed 11 

sea stars per day off the western shore (Figure 

3). Smaller sea stars, presumably juveniles, 

were green in color. Medium, presumably subadults, 

were green with brown and orange 

patches. Large, presumably adults, were tan, 

orange, or rust in color. Sea stars were most 

often found on the sandy flats outside of the 

turtle grass (Thalassia testudinum) beds, in 

water depths of 1-3 meters. When turned over, 

most were holding onto some sort of shell or 

rock with their tube-feet. 

Number of Sea Stars 

Observed 

Sea Star Observations 

Figure 3. Counts off the western shore of SLC. 

The sea star’s body was somewhat pliable when 

picked up underwater; however the body 

became rigid if removed from the water. When 

picked up and held for a few minutes, they 

would attached to our 

hand using feet-like 

suction tubes. 

However, if we swam 

with one in our hand, 

it would become 

limp. When we 

inverted an individual 

to simulate conditions 

that may affect a sea star in a rough 

environment, it took approximately three 

minutes for the sea star to turn back over. 

Discussion 

With only ten days in the field, we were unable 

to follow-up on the results of our inductive, 

hypothesis generating survey. If given a chance 

to deductively test our hypothesis that “sea stars 

select the western shore to avoid more turbulent 

waters”, we would set up an experiment under 

laboratory conditions. Perhaps we could set up a 

large tank to simulate the 2 environments found 

around the caye. If a sea star placed in the more 

turbulent environment moved towards the 

calmer environment, then our hypothesis would 

be supported. 


Kaplan, Eugene H., 1982. A Field Guide to Coral 

Reefs Caribbean and Florida. New York: Houghton 

Mifflin. 176 pp. 

Puglisi, Melany P. 2008. Oreaster reticulatus 

http://www.sms.si.edu/IRLSpec/Oreaster_reticulatus. 

htm. Downloaded 06/01/2009. 


Sirenian International (sirenian.org) 

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Day of Observation

Fiddler Crab 

Uca minax 

Whitney Montgomery & Daniel Hill 



Taxonomy 



Subphylum Crustacea 

Class Malacostraca 


Family Ocypodidae 

Species Uca minax 

Ecology 

Fiddler crabs inhabit a wide range of tropical 

regions. In Belize, their habitats are mangroves 

and salt marshes. Fiddler crabs are extremely 

populous species. The semi-terrestrial species is 

diverse in color and habitat, with the most 

distinguishing characteristic being the males’ 

asymmetrical claws (Fig. 1). They use the large 

claw to signal to other crabs within their 

vicinity, to attract a mate, and as a weapon used 

in combat between other males (Magnhagen, 

1991). These behaviors could draw attention to 

them from predators. The claw can be up to 

50% of an adult male’s body weight. If a claw is 

lost, the smaller claw of some species will grow 

larger and the crab will regenerate the lost claw 

with a new, smaller one. 

Figure 1. Fiddler crabs during experiment. (Belize, 2010) 

fiddler crab (Belize 2010) 

Figure 

2. Adult 

male 

Behavior 

Fiddler crabs tend to feed near their burrows, so 

that if they feel threatened, they will retreat into 

it to seek shelter. The crabs use their small 

claws to pick up pieces of sand, filtering out 

microscopic bits of algae, microbes, or fungus 

with their mouthparts. Crabs live about two 

years and molt their shells indeterminately (one 

to two times per year) as they continue to grow 

throughout their lives. Males wave their larger 

claw to attract female attention when ready to 

reproduce. Fiddler crab eggs are fertilized 

externally and the female fiddler crabs carry 

their eggs on their underside in a large mass. 

She keeps them safe in her burrow for a two 

week period and then journeys down to the edge 

of the sea to release the eggs into the receding 

tide. The larvae remain in a planktonic state for 

a further two weeks before venturing onto land 

and setting up a territory of their own. 

Conservation 

While fiddler crabs are not seriously threatened, 

their habitats are under pressure. As human 

populations continue to expand, they are 

destroying the mangroves and salt marshes 

where the crabs live. Fiddler crabs may serve as 

an important indicator species for these places. 

Fiddler crabs are important to the conservation 

of their ecosystems. Some experts believe that 

by continually sifting through the sand for food, 

their feeding habits aerate the substrate and 

prevent anaerobic conditions (Montague, D. L. 

1980).


Introduction 

On a 13-day Field Biology class, the Hugh Parkey 

Foundation for Marine Awareness and Education 

was our host for the May 26 –June 8, 2010 

educational trip. Staying and studying on the 

Drowned Cayes (a mangrove island east of the 

Belize mainland), fiddler crabs are one of the easiest 

species to first recognize. After several days of 

observation of their behaviors and movements, the 

question of “Does the handedness of a fiddler crab 

affect its movement when threatened?” was 

developed. In other words, do crabs with a larger 

left claw tend to move towards the left side when 

threatened? 

Method 

After a tour of the island, we determined two prime 

spots for observation and collection of data. On the 

west side of the island, the mangroves and other 

vegetation provide protection for burrowing crabs 

with still access to sediments in which they eat. We 

studied the red-jointed fiddler crab (Uca minax) for a 

period of 2-h over the course of 2-d, with special 

emphasis on movement and behavior when 

threatened. We then collected a total of 20 fiddler 

crabs over another 2-d period (nleft claw=10 and nright 

claw=9). We used a ruler to determine the claw 

length of each crab (Fig. 2) and noted whether the 

larger claw was on the right or left (handedness). 

The crab was placed into a plastic container and 

allowed time for to calm down from the stress of 

human handling. We then “threatened” the crab by 

using the ruler to come at the crab facing its front 

(head) side. Using the same ruler, we measured the 

distance it traveled and noted the direction in which 

it moved. Ten of the fiddler crabs were collected 

from the West side of the island within an area and 

the other 10 were collected from a similar site on the 

East side of the island. They were taken from two 

sites to ensure we had a wide variety of crabs. The 

crabs were returned to their original sites upon 

completion of the experiment. 

Results 

Of the 20 crabs tested, 11 moved in the direction 

opposite their large claw (55%) and 9 moved in the 

direction of their large claw (45%). We found that 

the direction moved in relation to the larger claw 

was not significant. Using a chi-square test (df=1), 

we found crabs did not move significantly in the 

direction of their larger claw (Fig. 3, =0.2, p > 

0.05). 

 

 

 

Figure 3. The number of crabs and direction of crab movement s in 

relation to their larger claw. 

Discussion 

Our hypothesis that fiddler crabs would be more 

likely to move in the direction of their larger claw 

was not supported. The sample size was reasonable 

given the time constraint and if given the 

opportunity to redo the experiment, a larger sample 

size would allow for a stronger test of the 

hypothesis. While our findings showed no size 

sided preference in movement, a few observations 

suggested that fiddler crabs might move away from 

their large claw when threatened. Some research 

suggests that the large claw increases vulnerability 

to predation (Martin & Lopez, 1999), while other 

research suggests the claw might actually be used to 

ward off potential avian predators (Bildstein et all, 

1989). More research on the effect of fiddler crab 

movement while threatened could test this 

hypothesis. 

References 

Bildstein, K. L., McDowell, S. G. & Brisbin, I.L. 1989. 

Consequences of sexual dimorphism in sand fiddler 

crabs, Uca pugilator: differential vulnerability to 

avian predation. Animal Behavior, 37, 133-139. 

Magnhagen, C. 1991. Predation risk as a cost of 

reproduction. Trends in Ecology and Evolution, 6, 

183-186. 

Martin, J. & Lopez, P. 1999. When to come out from a 

refuge: risk-sensitive and state-dependent decisions 

in an alpine lizard. Behavioral Ecology, 10, 487- 

492. 

Montague, D. L. 1980. A natural history of temperate 

western Atlantic fiddler crabs (genus Uca) with 

reference to their impact on the salt marsh. 

Contributions in Marine Science, 23, 25-55.

Patch Reef Habitats 

Kelly Haun and Emy Rodriguez 

Edited by Caryn Self-Sullivan 



Ecology 

Corals are defined as small animals that attach 

themselves on hard surfaces to the sea floor. 

They colonize in the thousands and build 

skeletal structures of calcium carbonate, which 

produces the limestone foundation of coral 

reefs (Humann & Deloach, 2002). Hard 

corals are reef building corals that provide 

shelter and food for juvenile fish. 

Several types of coral reefs exist, which are 

defined by their general structure. Patch reefs 

represent one type of coral zone found near 

shore and are commonly surrounded by 

seagrass, sand, or algae (Mumby, 1999). 

These reefs are composed of hard and soft 

corals and rock or rubble, which form the 

concrete foundation on the sea floor. 

Patch reefs provide protective niches 

and food sources for many species of 

vertebrates and invertebrates (Kaplan, 1982). 

Conservation 

Coral reefs are in a state of decline around the 

world due to anthropogenic impacts that 

include overfishing, increased runoff and 

pollution from land, rising concentrations of 

carbon dioxide and invasive species (Turnball 

& Harborne, 2000). Overgrowth of algae, 

sponges and tunicates appears to have 

increased at many locations in the Caribbean. 

The growing problem can be partially 

contributed to the excess of nitrogen and other 

nutrients carried into the sea by runoff which 

stimulates the growth of plankton. The 

increase of plankton provides food to such 

organisms, which compete for space on corals 

and may eventually cause corals to die 

(Humann & Deloach, 2002). No previous 

studies have been made to analyze the reef 

system around the Drowned Cayes or 

document how these impacts may be affecting 

the reef ecosystem. 

View of reef patch from the surface. 

Introduction 

Our Investigation 

The Belize Barrier Reef System fringes along 

the eastern side of the Spanish Lookout Caye, 

which is a mangrove island surrounded by 

seagrass beds. Patch reefs are intermingled 

throughout and contribute to this complex and 

intricate environment. 

With the help of our guide, Denroy Usher, we 

surveyed the coastline around the caye and 

found several patch reefs varying in depth 

from 4 ft to 18 ft. These reefs have not been 

previously studied and an understanding of 

their structure and role can help contribute to 

conservation efforts in the area. 

Our objectives are to draw up preliminary data 

on the percentage of substrate types found in a 

coral patch and determine the relative 

abundance of fish in relation to the distance 

from a coral patch. We predict that the 

number of fish will decrease the further we 

move from the patch. 



Method 

We selected a patch reef located on the south 

west point of the caye approximately 150 ft 

from the coastline. The depth of the coral 

patch was 4.7 ft with 100% water clarity 

which enabled ease of data collection. We 

randomly selected a patch head and set up a 

10 ft x 10ft study site. We randomly sampled 

four quadrants within the site to determine the 

percentage of substrates within the patch. A 

line transect was positioned from the center of 

the site east and west along the contour of the 

coastline each 40 feet from the center, totaling 

80 feet across. Fish counts were conducted 

every 10ft radiating from the center of the 

study site. 

Results 

Our findings show that substrate cover varied 

between quadrants 1 and 2. After calculating 

the total percent cover of both quadrants we 

determined the reef patch substrate to be 

composed of 40% rock/rubble, 22.5% hard 

coral and 16.25% algae/sponge (See Table 1 

in appendix).Figure 1 shows the data obtained 

during the fish line transect, showing a general 

trend whereby the total number of fish 

decreased as the distance from the coral patch 

increased. However, the east transect shows a 

decreased number of fish at 10 ft from the 

patch reef. 

Figure 1. Number of fish located at 10 ft increments from 

the center of the research site. 

Discussion 

This study attempted to draw up preliminary 

data on the percentage of substrate types 

found in a coral patches. However, due to 

limited time constraints we were unable to set 

up a control site with which to provide a 

comparative analysis. 

Our fish counts confirm our initial hypothesis 

that the relative abundance of fish decreased 

in relation to distance from the coral patch. 

This demonstrates the importance of patch 

reefs as a shelter and as a food source for fish, 

and suggests fish do not migrate far from these 

rocky/rubble and hard coral substrates. 

We believe that the slight discrepancy in data 

on the east transect line (10 ft distance) is a 

result of disturbance caused while performing 

the fish counts, as snorkeling became more 

challenging at shallower depths. 

We observed algal growth on many hard 

corals as well as a small amount of disease 

which may be indicative of increased nitrogen 

levels, as well as other anthropogenic stresses, 

and should be further investigated. 


Humann, P., & Deloach, N. (2002). Reef Coral 

Identification. Jacksonville: New World Publications. 

Kaplan, E. H. (1982). Ecology of the Coral Reef. In 

E. H. Kaplan, A Field Guide to Coral Reefs, 

Carribean and Florida (pp. 101-120). New York: 

Houghton Mifflin Company. 

Mumby, P. J. (1999). Classification Scheme for 

Manatee Habitats of Belize. London: Centre for 

Tropical Coastal Management Studies. 

Turnball, C., & Harborne, A. (2000). Summary of 

Coral Cay Conservation's Atlantic and Gulf Rapid 

Reef Assessment Data From Turneff Atoll, Belize. 

London: Coral Cay Conservation LTD. 



Method 

We selected a patch reef located on the south 

west point of the caye approximately 150 ft 

from the coastline. The depth of the coral 

patch was 4.7 ft with 100% water clarity 

which enabled ease of data collection. We 

randomly selected a patch head and set up a 

10 ft x 10ft study site. We randomly sampled 

four quadrants within the site to determine the 

percentage of substrates within the patch. A 

line transect was positioned from the center of 

the site east and west along the contour of the 

coastline each 40 feet from the center, totaling 

80 feet across. Fish counts were conducted 

every 10ft radiating from the center of the 

study site. 

Results 

Our findings show that substrate cover varied 

between quadrants 1 and 2. After calculating 

the total percent cover of both quadrants we 

determined the reef patch substrate to be 

composed of 40% rock/rubble, 22.5% hard 

coral and 16.25% algae/sponge (See Table 1 

in appendix).Figure 1 shows the data obtained 

during the fish line transect, showing a general 

trend whereby the total number of fish 

decreased as the distance from the coral patch 

increased. However, the east transect shows a 

decreased number of fish at 10 ft from the 

patch reef. 

Figure 1. Number of fish located at 10 ft increments from 

the center of the research site. 

Discussion 

This study attempted to draw up preliminary 

data on the percentage of substrate types 

found in a coral patches. However, due to 

limited time constraints we were unable to set 

up a control site with which to provide a 

comparative analysis. 

Our fish counts confirm our initial hypothesis 

that the relative abundance of fish decreased 

in relation to distance from the coral patch. 

This demonstrates the importance of patch 

reefs as a shelter and as a food source for fish, 

and suggests fish do not migrate far from these 

rocky/rubble and hard coral substrates. 

We believe that the slight discrepancy in data 

on the east transect line (10 ft distance) is a 

result of disturbance caused while performing 

the fish counts, as snorkeling became more 

challenging at shallower depths. 

We observed algal growth on many hard 

corals as well as a small amount of disease 

which may be indicative of increased nitrogen 

levels, as well as other anthropogenic stresses, 

and should be further investigated. 


Humann, P., & Deloach, N. (2002). Reef Coral 

Identification. Jacksonville: New World Publications. 

Kaplan, E. H. (1982). Ecology of the Coral Reef. In 

E. H. Kaplan, A Field Guide to Coral Reefs, 

Carribean and Florida (pp. 101-120). New York: 

Houghton Mifflin Company. 

Mumby, P. J. (1999). Classification Scheme for 

Manatee Habitats of Belize. London: Centre for 

Tropical Coastal Management Studies. 


Coral Cay Conservation's Atlantic and Gulf Rapid 

Reef Assessment Data From Turneff Atoll, Belize. 

London: Coral Cay Conservation LTD. 



139 

140 

141 

142 

143 

144 

145 

146 

147 

148 

149 

Average BML Average AML


Lytechinus variegatus 

Rachelle Boucher, Elizabeth Ferrell, and 

Samantha Egelhoff 

Edited by Caryn Self-Sullivan, Ph.D 

& Dr. Bruce Schulte, Ph. D 


Belize, Class of 2010 (contact: 

caryns@sirenian.org) 

Taxonomy 

Kingdom: Animalia 

Phylum: Echinodermata 

Class: Echinoidea 

Order: Temnopleuroida 

Family: Toxopneustidae 

Genus: Lytechinus 

Species: Lytechinus variegatus 

Ecology 

Commonly known as the green sea urchin, 

Lytechinus variegatus is found in waters from 

Bermuda to Brazil, including the Caribbean Sea 

(Norris 2003). In their adult form, they are 

mainly white to green in color, although some 

have a pinkish-purple hue. They are covered in 

short spines that can regenerate. While their size 

usually varies from 1-12 cm, some can grow as 

large as 36 cm (Barnes 1982). 

Purple Variation of L. variegatus 

L. variegatus is normally found in calm, shallow 

waters, although they can be found in waters up 

to 50m deep (Norris 2003). It feeds on seagrass, 

mainly Thalassia sp., by using its tube feet and 

Aristotle’s Lantern (Norris 2003). The tube feet 

act as an anchor and hold the green sea urchin in 

White variation of L. variegatus 

place, while the mouth of the sea urchin, known 

as Aristotle’s Lantern, which is composed of 

strong joints and teeth, can scrape its food off of 

rocks or other hard surfaces (Barnes 1982). 

Behavior 

The green sea urchin reproduces by releasing 

unfertilized eggs and sperm into its water column, 

where the eggs are fertilized and develop into 

larvae (Norris 2003). The larvae undergo a 

complex metamorphosis to reach the adult form. 

L. variegatus use their spines and tube feet to 

cover their exterior with surrounding debris, 

serving as protection from predators and the sun’s 

rays. 

Conservation 

In Caribbean reef ecosystems, sea urchins have 

the capability of population explosion if one of 

their key predators is taken out of the system. 

Since their main food source is turtle grass 

(Thalassia sp.), a large urchin population can 

easily clear out whole patches of seagrass on 

which other animals, such as manatees and sea 

turtles, depend. However if sea urchins are taken 

out of a reef ecosystem, the seagrass patches that 

they normally keep under control can grow 

exponentially in some reef regions and kill off 

fragile corals. Jackson, however, mentions that 

Diadema urchins have always been abundant in 

their environment since pre-colonization, and 

predator control might not even be a factor 

(1997).


Introduction 

We found L. variegatus to be quite common 

along the sea wall on the west side of Spanish 

Lookout Caye off the coast of Belize City, 

Belize. While observing them, we noticed that 

they were always hidden underneath rocks or 

covered with seagrass or shells, perhaps done in 

order to provide protection against predators or 

to protect them from the sun or other physical 

factors (Verling, 2004). The objective of this 

research was to see if the size of the sea urchin 

determined how fast the urchin recovered itself 

with debris, or if the size was related to how far 

they traveled away from their initial spot once 

uncovered. Smaller sea urchins are in need of 

more protection because they are more 

susceptible to threats. Therefore, we expected 

them to travel further or in less time in order to 

find protection. 

Methods 

Over a four-day period, we noted abiotic 

conditions and searched for different sized sea 

urchins along the shallow sandy and rocky 

bottoms. We removed all debris on 10 urchins 

using tweezers and tested 3 additional control 

urchins (n=13). Two controls were untouched, 

and one was touched but no debris was removed. 

Every two minutes for twenty minutes we 

measured the distance each traveled from its 

initial position. After observing for 20 minutes, 

we measured the diameter of each urchin, not 

including spines, and noted its coloration. Two 

graphs were plotted to see if the size of the 

urchins had an effect on the time of movement 

or distance traveled in order to recover 

themselves with debris. 

Results 

We found that there was no significant 

relationship between size and total distance 

(F(1,8)=1.32, P=0.28) (Fig 1) or size and time of 

movement (F(1,8)=0.38, P=0.55) (Fig 2). We 

tested a variety of juvenile-sized urchins, but 

each urchin had its own individual response. The 

control urchins suggested that there was no 

relationship between human interaction and 

individual urchin movement, only that they 

sought protection. All urchins either recovered 

themselves with debris or moved under rocks in 

place of coverings within the 20-minute time 

frame after we removed their initial debris. 

Figure 1. Total Distance Moved vs. Size 

Figure 2. Total Time of Movement vs. Size 

Discussion 

Time and distance traveled by each individual 

urchin appeared to be to dependent on how 

quickly they were able to recover themselves, 

whether with debris or under a rock; not their size. 

Further research should be done using a larger 

sample size including adult urchins in varying 

habitats. Since most of the urchins were juveniles 

and found in shallow water, this might have 

skewed our data and conclusions. 

Literature 

Barnes, Robert D. (1982). Invertebrate Zoology. 

Philadelphia, PA: Holt-Saunders International. 

Pp 961-981. ISBN 0-03-056747-5. 

Jackson, J.B.C. (1997). Reefs since Columbus. Coral 

Reefs: S23-S32. 

Norris, Amy. (2003). Green Sea Urchin Lytechinus 

variegatus. Marine Invertebrates of Bermuda: 

1-7. 

Verling, E. D.K.A. (2004). The dynamics of covering 

behavior in dominant Echinoid populations 

from American and European West coasts. 

Marine Biology: 191-206.

Red Fin Needlefish 

Strongylura natata 

Jamie Hennis and Carol Lacey 

Edited by Bruce A. Schulte, Ph.D. and 


Ecology & Behavior of Manatees & 

Dolphins in Belize, Class of 2010. 

(contact: caryns@sirenian.org) 

Taxonomy 


Phylum Chordata 

Super Class Osteichthyes 

Class Actinopterygii 

Order Beloniformes 

Family Belonidae 

Genus Strongylura 

Species Strongylura natata 

Ecology 

The redfin needlefish is a marine fish 

located in warm, clear, coastal waters 

(Humann 2002). They can be seen 

solitary or in small groups in mangroves 

and sea grass ecosystems (Sweat 2009). 

Redfin needlefish are about 9 times their 

length than their width with an elongated 

needle-like bill. All species of needlefish 

are blue-green in color dorsally with 

silver sides. The redfin needlefish gets 

its name because the caudal and anal fins 

appear red in color. They are similar to 

other species in this family because their 

upper jaw is slightly shorter then the 

lower jaw, they have a short tail and the 

lower lobe is slightly longer than the 

upper lobe. We could find no 

information regarding conservation 

issues of needlefish. 

Figure 1. Needlefish at rest (photo by Carol 

Lacey). 

Behavior 

Needlefish are considered surface feeders. 

They are generally found just below the 

water surface where feeding is convenient for 

them due to their lateral line being located 

ventrally on their body (Lovejoy 2000). They 

are known as ram feeders. They capture their 

prey by striking them with their beak and 

pinning them in their jaws. The organism is 

then released and positioned properly for 

consumption in a head first position. Redfin 

needlefish have low predation risk because of 

their blue-green counter shading with the 

water, camouflaging them from overhead 

birds. Their nicknamed the skipper because 

when frightened, they tend to leap out of the 

water and skip across the surface. 

Figure 2. Needlefish foraging (photo by Carol 

Lacey).

OUR RESEARCH FINDINGS 

Introduction 

The Hugh Parkey Foundation for Marine 

Awareness and Education hosted our 13day 

field course (May 26-June 8, 2010). 

Our base station was located at Spanish 

Lookout Caye in the Drowned Cayes 

east of Belize City. This is a mangrove 

island made up of 186 acres. We found a 

population of redfin needlefish near the 

boat dock. We observed these fish for 

two days prior to collecting data and 

noticed several types of behavior. These 

observations suggested that activity 

levels depend on the time of day. Our 

objective was to determine if the 

occurrence of redfin needlefish 

behaviors varied with time of day. 

Method 

The sample area was 152.7 sq ft between 

the restaurant and the manatee museum. 

This area is full of marine life offering 

food and calm water (except waves from 

boats docking). During our observations 

we identified three behaviors as follows: 

1) Resting - needlefish oriented to the 

current in a head first position (Fig. 1). 

2) Foraging - needlefish swim in a 

random, non-organized manner looking 

for food (Fig. 2). 3) Socialization - 

needlefish appear to be aware of others 

in the population and interactions or 

non-aggressive swim takes place. 

We observed needlefish three times each 

day: morning 6:30-8 am, afternoon 12-4 

pm, and evening 6-9 pm. We scanned 

fish behavior once per minute for fifteen 

minutes, only including calculations in 

our results when fish were present. The 

abiotic factors of tidal depth, current 

speed, and weather conditions also were 

recorded. 

Results 

Needlefish were found to be most socially 

active in the morning and afternoon, with the 

three behaviors occurring equally at night 

(Fig. 3). The only abiotic factor appearing to 

have an effect on needlefish behavior was 

weather; needlefish were absent during rains. 

Figure 3. Number of fish resting, foraging, and 

socializing three times during the day. 

Discussion 

We found that fish numbers did not differ 

with time of day, but there was a difference 

in behaviors. Behaviors were equal in 

occurrence at night with mornings showing 

the highest socializing. With further research 

we could develop a better understanding of 

the effect time of day and other abiotic 

factors have on needlefish behavior and 

activity. 


Humann, Paul. 2002, Reef Fish Identification 

Florida Caribbean Bahamas, pg. 58. 

Lovejoy, Nathan R., 2000. Systematics of 

Needlefishes and their Allies (Teleostei: 

Beloniformes). Volume 54:pg 1349-1362. 

Sweat, L.H. 2009, Redfin Needlefishes. 

Smithsonian Marine Station at Fort Pierce. 

Downloaded May 20, 2010. 

www.sms.si.edu/irlspec/strong_hotata.htm.

Fiddler Crabs and Hermit Crabs 

Uca minax and Pagurus annulipes 

Rachel Calhoun and Molly Martin 

Ecology & Behavior of Manatees & Dolphins in Belize, 

Class of 2010 (contact:cselfsullivan@sirenian.org) 

Taxonomy 

Kingodom Animalia 


Subphylum Crustacea 

Class Malacostraca 


Family Ocypodidae 

Species Uca minax 

Superfamily Paguroidea 

Species Pagurus annulipes 

Ecology 

Fiddler crabs are found in mangroves, salt marshes, 

and on sandy or muddy beaches in the Southeastern 

U.S., the Gulf of Mexico, and the Carribean (Kaplan 

1988). Their distinctively asymmetric claws easily 

identify them. U. minax is a detritivore, consuming 

algae, microbes, fungus, and other decaying materials. 

They appear to be a common resident along the 

brackish intertidal mud flats, lagoons, and swamps of 

Belize. 

Similarly, terrestrial hermit crabs are found in tropical 

areas within the intertidal zone. They also are 

detritivores, feed primarily on algae and decaying 

materials. They lack a carapace, or shell, so they 

“borrow” one from snails, such as periwinkles or 

oyster drills. As hermit crabs grow in size, they have 

to locate a larger shell, abandoning the previous one. 

Aside from this, their soft-coiled abdomens, two pairs 

of walking legs, and their asymmetric claws, are also 

used to identify them. 

Behavior 

Fiddler crabs create small burrows in the sediment 

that are used for mating, sleeping, refuge from 

predators, and ‘hibernating’ during the winter. They 

are very active during the day, foraging for food and 

digging burrows; they will return to their burrows at 

night and during high tide, plugging the entrance with 

mud or sand. Shells are an important resource for 

hermit crabs, but empty shells are generally low 

supply in nature (Kellogg 1976) and may be a limited 

resource for hermit crabs (Turra and Denadai 2004). 

As a result, hermit crabs will often compete with one 

another for shells. Competition may occur in two 

Figure 1. Hermit crab on the beach. 

ways: 1) hermit crabs may use chemical cues to locate 

newly available shells (Mesce 1982),or 2) they may 

display ritualized agonistic shell fighting behaviors 

and subordinate other individuals of the same species 

(Hazlett 1966). This is known as interference. 

However, many hermit crab species coexist in coastal 

areas and may cause various degrees of niche overlap 

(Turra and Denadai 2001). 

Introduction 

Our research took place during our 13-day research 

trip as part of a field marine biology class. We stayed 

on a mangrove island in the Drowned Cayes east of 

the Belize mainland with the Hugh Parkey Foundation 

for Marine Awareness and Education. Both hermit 

crabs and fiddler crabs are abundant on the island and 

are easily found. After much observation around the 

island of both crab species we asked the question of 

“How do fiddler and hermit crabs abundances change 

with the tides?” 

Figure 2. Fiddler crab near a burrow. 

Methods 

We chose two different areas to use for our research 

according to where we found the most of each crab 

species. Both areas were counted twice a day for three 

days. The area for the fiddler crabs was in a marshy 

Hugh Parkey Foundation for Marine Awareness & Education (belizeadventruelodge.com) 


area on the north part of the island near the lagoon. 

The area for the hermit crabs was on the east part of 

the island only a few meters from the edge of the 

beach. Presence or absence of a breeze, temperature 

estimation, precipitation, the substrate moisture, and 

tide were taken before each data collection. We noted 

the presence and activity levels of each species in and 

around the study area before and after collecting data. 

We counted the number of fiddler crab burrows within 

a 10x10 ft area within the marshy area. This area had 

a small mangrove tree that marked one corner. 

Vegetation coverage in the area was estimated by 

looking at what percentage of the soil was covered by 

vegetation. The study area was divided in half and 

each person counted the number of burrows on each 

side to make counting easier and switched which side 

they counted in the afternoon. 

In the second area where hermit crabs were counted 

we demarcated a 15x15 ft study area with a palm tree 

in the eastern corner of the box and the number of 

hermit crabs on the beach was recorded. Next, the 

number of hermit crabs either climbing the tree or 

hidden in the braches of the tree were counted. Hermit 

crabs in the tree often crowded in crevices and would 

move when we got near making them more difficult to 

count. Therefore, each person counted and then 

shared numbers and an average number between 

counts was agreed upon. Also observations of hermit 

crabs in the area especially those near the water of the 

beach were recorded. 

Results 

The density of both crab species did not vary much 

with tide level (Fig. 3). The high tide for the fiddlers 

had the lowest density but it was also the only data 

taken during high tide whereas three data sets were 

taken during low tide and two taken during an ebb 

tide. 

The average density of fiddler crabs per square foot 

was 13 times greater than the average density of 

hermit crabs per square foot although the fiddler crab 

area was smaller. Most of the hermit crabs found were 

located in the crevices of the palm tree in the area and 

only a total of eight hermit crabs were found on the 

beach over all three days. The fiddler crab burrows in 

the designated area averaged 128.7 for each data 

collection and hermits found in the palm tree averaged 

21 for each data collection. 

Discussion 

We did not observe any major differences in the 

abundance of either crab species during different 

times of the tide. We did see six times more fiddler 

crabs than hermit crabs in a smaller area but neither 

species fluctuated too much with the tides. It is hard to 

draw any absolute conclusions from our data because 

we only took six data sets over three days and did not 

cover all the tides fairly. If we had more time to take 

more sets we would have more reliable data. 

Additionally, we did not have enough data to do any 

statistical analyses, so no certain conclusions can be 

made. However, this study seems to suggest that tides 

do not seem to directly affect either species’ numbers 

or their activity. Interestingly, the high tide did not 

reach the study site of the hermit crabs, which means 

that their decrease in density or relocation to the tree 

does not appear to be directly correlated with tides. 

There appears to be another reason as to why hermit 

crabs hide in trees, which could be predator 

avoidance. 

References 

Hazlett, B.A., 1966. Social behavior of the Paguridae and 

Diogenidae of Curacao. Stud. Fauna Curacao Other 

Caribb. Isl. Vol. 23, 1 –143. 

Kaplan, E.H. 1988. “Fiddler Crabs of the Southeastern 

U.S., Gulf of Mexico, and Carribean.” Southeastern 

and Caribbean Seashores. p 334-338 

Kellogg, C.W., 1976. Gastropod shells: a potentially 

limiting resource for hermit crabs. J. Exp. Mar. Biol. 

Ecol.Vol. 22, 101–111. 

Mesce, K.A., 1982. Calcium-bearing objects elicit shell 

selection behavior in a hermit crab. Science. Vol. 215, 

993–995. 

Turra, A., Denadai, M.R., 2001. Desiccation tolerance of 

four sympatric tropical intertidal hermit crabs 

(Decapoda Anomura). Mar. Freshw. Behav. Physiol. 

Vol. 34, 227– 238. 

Turra, A., Denadai, M.R., 2004. Interference and 

exploitation components in interespecific competition 

between sympatric intertidal hermit crabs. Journal of 

Experimental Marine Biology and Ecology Vol. 310, 

183– 193. 

 

Hugh Parkey Foundation for Marine Awareness & Education (belizeadventruelodge.com) 



Oreaster reticulates 

Whitney Allen and Rory McGonigle 

Edited by: Dr. Caryn Self-Sullivan, Ph.D. 

& Dr. Bruce Schulte, Ph.D. 


Belize, Class of 2010 (contact: cselfsullivan@sirenian.org) 

Taxonomy 

Kingdom: Animalia 


Class: Asteroidea 

Order: Valvatida 

Family: Oreasteridae 

Genus: Oreaster 

Species: Oreaster reticulates 

Ecology 

Cushion sea stars are found to be fairly common 

in Belize and other parts of the Caribbean. They 

are usually located in shallow waters inhabited 

with sea grasses and/or sand (Hummann and 

Deloach, 2002). Sea stars are normally fivearmed 

creatures varying in colors from green 

and brown to dark red and orange (Fig. 1). 

Juveniles tend to be green with spots of brown 

developing on them as they get older. Full adults 

may be yellow, orange, or red, normally mixing 

at least two of those together. 

Figure 1. Mid-range Adult Sea Star (Belize 2010) 

Some sea stars have six legs, which is almost 

always a cause of one previously being torn off. 

 

When growing back, it grows back mutated and 

forms two arms in the place of one (D. Usher, 

field assistant, pers. comm.). 

Behavior 

Sea stars have suction-like tube feet that allow 

them to stay on the sea floor (Fig. 2). Their 

connective tissue allows them “to change in 

response to passive mechanical properties” that 

can be caused by numerous environmental 

factors (Motokawa, 1984). When picked up or 

otherwise displaced, the tube feet close and are 

not opened until after the initial threat subsides. 

The center of their body is the central location of 

the digestive system, where all food is brought 

up into the body. The tube feet also may pick up 

food particles; those particles are then 

transferred down the arm to the mouth at the 

body’s center. Sea stars are not rapidly moving 

organisms. Our evidence suggests that they 

experience site fidelity, meaning they can be 

found in the same or near the same location on a 

day-to-day basis. However, their location can be 

affected by the water’s turbulence and weather 

conditions. 

Figure 2. Six-Armed Sea Star (Belize 2010) 

Conservation 

Sea stars, with their normally shallow location 

and non-movement along the sea floor, are 

typically taken for granted. With no visible 

breathing, many people forget they are even a 

living creature. Therefore, many sea stars lose 

their life when brought above water for too long, 

and from there, some are even kept for souvenirs 

and decorations.

Introduction 

Our Investigation 

Before our arrival to Hugh Parkey’s Adventure 

Lodge, we were asked to do pre-experimental 

research of information relating to a topic shared 

with a fellow student. After actual research 

began, we started by observing certain locations 

of sea stars along the western shore of the island. 

However, there did not appear to be a preference 

of their dwelling, so we eliminated that aspect 

out of our research. We noted that each time we 

picked up a sea star off the sea floor, it closed up 

its tube feet. It appeared that the time it took to 

completely close up the tube feet varied from 

one individual to another. This observation lead 

us to the main question of our project: Does the 

size of a sea star affect the amount of time it 

takes for it to close up its tube feet? 

Methods 

All of the data collected was done via snorkeling 

along the western shore (See appendix). Once a 

sea star was spotted, it was removed from the 

sea floor, and at the point of first contact the 

stopwatch was started. The star was flipped over 

in one’s hand and the time was recorded after 

complete closure. The sea star was measured 

from the end of one arm to the very center of the 

body. It was then measured again from the 

center of the body to a different leg to obtain a 

general diameter (two radii) for the organism. 

The following were also noted: location (sea 

grass or sand), color, number of legs and eating 

behavior at the time. After the data was 

collected, the sea star was gently placed back in 

its original position on the sea floor. 

Results 

No juveniles could be found on the western side 

of the island, but there was still a 16cm-27.5cm 

range of diameters in the sample pool (Figure 3). 

The average diameter was 24.0 cm (± 3.07). 

Four seconds was the most common closing 

time, consisting of 25% of our data. The fastest 

closing time was two seconds, which was a star 

measuring 25.5 cm in diameter. A 28.5 cm star 

closed the slowest, taking a total of nine 

 

seconds. Our evidence shows a weak but 

significant relationship between the size of a sea 

star and the time it takes to close (r 2 =0.20, df= 1, 

23, F=5.63, P=0.026; raw data located in 

appendix). 

Figure 3. Size of sea star and the time to completely close its tube 

feet when picked up and inverted underwater. 

Discussion 

Our hypothesis (“The bigger the sea star is the 

quicker it will close up its tube feet.”) was not 

supported by our data. We expected a negative 

correlation, while our results produced one that 

is positive. However, our acquired R square 

value shows that that the time it takes a sea star 

to close is somewhat size dependent, with larger 

stars taking longer. The rate at which it protects 

itself could also be caused by either the 

experience of turbulent waters or even predation. 

A follow-up analysis could be done to continue 

to further test our hypothesis. If each sea star in 

our sample pool had been in the exact same 

location or raised under the exact same 

conditions, the role of size in its closure speed 

would be easier to isolate. 

References 

Humann, P. and N. Deloach. (2002). Reef 

Creature Identification, Sea Stars, p. 

366. New World Publications. 

Motokawa, T. (1984). Connective tissue catch in 

echinoderms. Biol. Rev. 59, 255-270.


Oreaster reticulatus 

Blakely Rice 

Edited by: Caryn Self-Sullivan, Ph.D. 

Ecology and Behavior of Manatees and 

Dolphins in Belize, Class of 2011 

(contact: cselfsullivan@sirenian.org) 

Taxonomy 


Phylum Echinodermata 

Class Asteroidea 

Order Valvatidas 

Family Oreasteridae 

Genus Oreaster 

Species Oreaster reticulatus 

Ecology 

The Cushion Sea Star (Oreaster 

reticulatus) is located throughout the 

Caribbean and are commonly found in 

shallow water seagrass and sand 

habitats (Scheibling, 1980). Adult sizes 

can range from 5 inches to 20 inches 

and juveniles from about 2 inches to 6 

inches (Kaplan, 1982; Rice, personal 

measurements). Coloration in adults is 

generally orange, yellow and red or any 

variation of the above. Juvenile 

coloration is a broad spectrum of greens 

(Figure 1). 

Oreaster is predominately a omnivorous 

grazer eating a variety of organisms 

including sponges and algae 

(Scheibling, 1982). 

Behavior 

Oreaster reticulates feeds by inserting 

its stomach into or onto its prey and 

secrets enzymes that digest the good, 

which is then absorbed (Kaplan, 1982). 

Their tube feet help them hold onto their 

prey. Oreasters many tube feet enable 

them to move quite quickly and cover 

significant distances in a short amount 

of time. 

Because sea stars reproduce asexually 

in a marine environment gametes meet 

mostly by chance (Kaplan, 1982). To 

increase chances of fertilization sea 

stars will release their gametes if other 

gametes are detected in the area 

(Kaplan, 1982). 

Conservation 

Even though Oreaster reticulatus is one 

of the most common sea stars in the 

Caribbean populations have become 

rare in some areas mainly due to over 

harvesting for the souvenir trade 

(Kaplan, 1982).

Introduction 

Sea stars have long been a favorite 

sight for snorkelers and divers, mainly 

because they are one of the only 

animals that does not bite or sting when 

handled. There only defensive behavior 

when being picked up is to become 

rigid, however after some time they will 

relax. This behavior inspired the 

question for my independent research 

project, how long does it take for a sea 

star to relax after becoming rigid and is 

there a difference between adults and 

juveniles. I hypothesized that juveniles 

will take more time to relax and the 

adults do. 

Methods 

I chose the western side of Spanish 

Lookout Caye (SLC) as my study 

location because of the persistence of 

sea stars in that area. To investigate my 

hypothesis I snorkeled along the sea 

wall and sea grass beds until I found a 

sea star. When a sea star was found it 

was picked up and turned over until all 

the tube feet had retracted and the 

animal was rigid. This was done to 

insure that the timing was accurate as it 

was found that some animals took 

longer to become rigid than others. 

Once fully rigid the animal was placed in 

my right, once it was on my hand timing 

began. Timing stopped when the first 

tube feet were present. The time was 

recorded on a slate and the animal was 

replaced in its original location, habitat 

location and size of the animal were also 

recorded. 

Results 

At the end of the study a total of 20 

adults and 6 juveniles were surveyed. A 

two-sample t-test for independent data 

was conducted to compare the latency 

(time) in adults and juveniles. There was 

a significant difference in the latency of 

adults and juveniles (t=2.34, df= 24, 

p=0.014). A one-way ANOVA was also 

conducted for post-HOC analysis 

regarding the latency with habitat type 

and latency with size. In regards to 

latency and habitat there was no 

significant difference in adults (f=0.45, 

df=18, p=0.6455) or juveniles (f=1.19, 

df= 5, p=0.3366). When looking at 

latency in regards to size there was a 

significant difference in adults (f=11.86, 

df=19, p=0.000596) but not a significant 

difference in juveniles (f=0.47, 

df=5,p=0.6644). 

Discussion 

My hypothesis that latency in juveniles 

would be longer than in adults was 

disproved. I found that latency in adults 

was actually longer than in juveniles. 

Continued studies need to be conducted 

to determine the reason for this 

behavior. 

Resources 

Kaplan, Eugene H., 1982. A field guide 

to Coral Reef. New York: Houghton 

Mifflin. P.171-176. 

Scheibling, R.E., 1982. Feeding habits 

of Oreaster reticulatus 

(Echinodermata: Asteroidea). Bulletin 

of Marine Sciences, 32, 504-510. 

Scheibling, R.E., 1980. Abundance, 

Spatial distribution and size structure 

of populations of Oreaster reticulatus 

(Echinodermata: Asterodiea) on Sand 

Bottoms. Marine Biology, 107-119.

Magnificent Feather-Duster 

Sabellastarte magnifica 

Sean Herbert 

Ecology, Behavior and Conservation of 

Manatees & Dolphins in Belize, Class of 2011 


Taxonomy 


Phylum Annelida 

Class Polychaeta 

Order Sabellida 

Family Sabellidae 

Genus Sabellastarte 

Species S. magnifica 

Ecology 

Feather duster worms inhabit reefs, mangroves, 

rocks, wrecks, and sand or gravel bottoms. They 

often grow from coral heads (Humann & DeLoach 

2002), and in Belize, the magnificent variety is often 

found attached to mangrove roots. Whatever the 

substrate, they are usually found sharing the space 

with various sessile animals such as sponges, 

mollusks and tunicates. S. magnifica are among the 

largest and most common feather dusters found in 

Belize. Those who may cringe at the word ‘worm’ 

need not fear; their bodies remain hidden, encased in 

a parchment-like tube attached to the substrate. The 

worms construct their tubes using fine sand and 

mucus secreted from glands just below their head. 

The only visible portion of the worm is the crown of 

feather-like appendages, which can be used to easily 

identify magnifica because of its exclusive doublecrown 

arrangement. The ‘feathers’ are usually 

banded and come in a variety of colors, including 

brown, tan, gold, reddish purple and white (Humann 

& DeLoach 2002). 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Behavior 

Feather duster worms use their ‘feathers’, known 

as radioles, as both gills and filters to capture 

plankton – their cuisine of choice. Trapped 

microscopic food is brought to its mouth at the 

center of its crown of ‘feathers’ (Fitzsimons 

1965). As largely sessile animals, they rely on 

currents to provide them with their edible treats. 

Their soft bodies remain out of sight throughout 

their lives, slowly adding length to their tubes as 

they mature. Their most notable behavior is the 

near instantaneous retraction of their radioles back 

into the tube when disturbed. The worms can 

detect changes in water movement, light intensity 

white (Humann & DeLoach 2002), and of course, 

tactile stimulation. As such, predators are often 

sucker-feeding fish . They have evolved rows of 

upper-facing hooks along each segment of their 

body, which allow anchoring in the event a fish 

attempts to suck them out (Woodin 1987). 

Conservation 

Although feather dusters themselves are not 

seriously threatened, many populations are subject 

to ongoing anthropogenic impacts on the coral 

reef and mangrove ecosystems, including, but not 

limited to, pollution, increased ‘fin’ traffic as 

Belizean tourism expands (reef), ocean 

acidification (reef), development (mangrove), and 

invasive species (Turnball & Harborne 2000).

INVESTIGATION 

Introduction 

Retraction of radioles is its primary form of 

defense, yet they are necessary for both respiration 

and ingestion. Given that they are sessile, I would 

assume that the animal would achieve the most 

benefit from having its radioles extended as long 

and often as possible. Therefore, a predator 

physically touching the radioles should cause a 

full retraction, with a longer latency, versus a 

distant water disturbance causing a shorter 

retraction and latency. Two tests were devised 

for this hypothesis: is there a correlation between 

latency and disturbance type; and, do worms 

respond differently to tactile and distant 

disturbance? 

Methods 

S. magnifica were identified in two locations 

along western shore of Spanish Lookout Caye: 

randomly distributed along a concrete seawall and 

clustered against square concrete pillars once used 

for a pier. Fourteen individuals were found 

attached to the seawall, and sixteen were found 

attached to different pillars, often in groups of 

two. Traditional snorkel gear was used for data 

collection, including a floatation device so as to 

keep unwanted disturbance at a minimum. 

Individuals are disturbed physically by a light 

index finger touch. For water movement 

disturbance, a ruler was used to gauge a distance 

of about 5-6cm from the radioles, and then I 

waved my hand laterally until the worm retracted. 

Some individuals would not respond to the wave, 

in which case I would flick my four fingers from 

behind my thumb towards the animal. A static 

distance of 5cm was originally intended, though 

the sensitive nature of the animal prevented this. 

A full or partial retraction was noted. After 

retraction, a stopwatch is used to measure the 

latency until reemergence. Reemergence from full 

retraction is defined as radiole tips protruding 

from the rim of its tube, or visible anterior 

movement if it is partially retracted. 

Results 

Using a correlated one-tailed t-test for latency of 

each disturbance type, a significant difference was 

observed between tactile and distant disturbances in 

S. magnifica (t = +2.58, df=29, P < 0.01, n=30), 

supporting this portion of the hypothesis. However, 

using a 2x2 categorical analysis chi-square test, no 

significant difference was found between full and 

partial retraction ( 2 = 3.27, df=3, P = 0.3518). 

 

 

 

 

 

 

 

Discussion 

The data collected only partially supports my 

hypothesis: tactile disturbance definitely results in 

a longer latency than distant water disturbance (P 

= 0.007), although full or partial retraction among 

individuals appears to be random. An alternate 

hypothesis could be that perhaps radioles grow 

more rapidly relative to tube construction, and 

may protrude even when the animal has retracted 

as far as it can. Another possibility is that 

individuals can detect the strength of the 

disturbance, either tactile or distant, and react 

accordingly. Further investigation using measured 

static force could be conducted to test this 

hypothesis. 

References 

Humann, P. and N. Deloach. (2002). Reef Creature 

Identification, Sea Stars, p. 140 & 148. New 

World Publications. 


Coral Cay Conservation's Atlantic and Gulf 

Rapid Reef Assessment Data From Turneff 

Atoll, Belize. London: Coral Cay 

Conservation LTD. 

Fitzimons, G. (1965). Feeding and Tube-Building in 

Sabellastarte magnifica (Shaw). Bulletin of 

Marine Science, 15 (3) : 642-670

Marine Hermit Crab 

Clibanarius vittatus 

Michelle Cassidy 

Ecology and Behavior of Manatees and Dolphins in 

Belize, Class of 2011 


Taxonomy 


Phylum Arthopoda 

Class Crustacea 


Family p 

Genus Clibinarius 

Species Clibinarius vittatus 

Ecology 

Common to most marine, estuarine, and 

shoreline environments, hermit crabs can 

be easily found worldwide. On Spanish 

Lookout Caye in Belize, Central America, 

both terrestrial and aquatic varieties of this 

crab can be easily spotted; the former found 

wandering the sandy shore, and the latter in 

the muddy shallows of the mangrove 

swamp. The mangrove species, C. vittatus, 

feeds on plant and animal detritus that sinks 

to the bottom. 


Hermit crabs utilize shells (generally from 

gastropods) for protection. This results from 

their development of a non-calcified 

abdomen that would make them vulnerable 

to predation (Schejter & Mantelatto 2009). 

Crabs have large foreclaws and smaller 

hindclaws. Shell sizes and coloration vary 

significantly between individuals. 

Conservation 

Though the hermit crab itself is not 

endangered, human expansion threatens its 

habitat. These crabs play a key role in the 

Mangrove ecosystem via scavenging and 

consuming detritus. In order to protect these 

animals and the web of life they exist within, 

it is important to conserve Mangrove 

swamps, such as the ones on Spanish 

Lookout Caye. Plenty of Mangrove Cayes in 

Belize have been dredged and filled to 

provide land for resorts, the process of 

which destroys valuable Mangrove 

resources and hermit crab habitats. 

Promoting awareness of the numerous 

species that depend on Mangroves for 

survival is key to conserving these animals. 

Behavior 

Crabs retreat quickly into their shells at any 

sign of potential danger. They will warily 

emerge from their shells if not touched or 

approached for approximately one minute. 

Competition for particularly nutirient-rich 

patches can become aggressive, with larger 

crabs often strong-arming smaller 

individuals into leaving the area, so they can 

enjoy the food source (Ramsay et al. 1997). 

Hermit crabs reproduce seasonally, with 

intensive mating activity occurring in the 

warmer months. Studies show that the 

recruitment area for young crabs differs 

from the adult habitat, and individuals are 

already an intermediate size once they 

appear. (SantÁnna et al. 2008, Turra & 

Leite 2000) 

Crabs can detect chemical signals of a dead 

or dying gastropod or conspecific, alerting 

them to the presence of a potential home 

(Rittschof 1980, Rittschof et al. 1992). They 

can also use chemical stimuli to identify 

predators (Rosen et al. 2009).

Introduction 

Shells serve as a limiting factor for hermit 

crabs in most environments (Tricarico & 

Gherardi 2006). As a result, crabs must 

develop strategic behaviors to procure 

viable shells as they grow. Synchronous 

vacancy chains (SVC) are adaptive 

behaviors that address this limitation by 

providing SVCs have been observed in 

terrestrial hermit crabs in the Drowned 

Cayes of Belize (Rotjan et al. 2010), but it is 

unknown if the marine species C. vittatus 

also implements SVCs. This study aims to 

answer the question of whether marine 

hermit crabs also utilize SVCs for shell 

acquisition. 

Closely related species of terrestrial Hermit Crabs 

(Coenobita clypeatus) in a SVC on SLC. 

Materials and Methods 

I gathered medium and large empty 

gastropod shells from the seagrass beds 

near the mangrove pond, then placed them 

within four 30 cm x 30 cm quadrats placed 

within the hermit crab habitat. I observed for 

two hour and a half sessions, making note 

of behavior in each quadrat every 10 

minutes. The number of hermit crabs 

present and the presence or absence of 

characteristic SVC behaviors were noted 

(piggybacking, waiting, tug of war). A SVC 

was present if the largest crab moves into 

an empty shell, while smaller crabs lined up 

behind move successively into the shell of 

the crab before it. 

Results 

Data collected couldnt be statistically 

analyzed, but some patterns emerged from 

observation. Crabs investigated empty 

shells, and one individual waited for 

approximately 30 minutes by a shell that 

was too large for it. On several occasions, 

crabs would “piggyback”, grasping to the 

shell of a larger individual while it moved 

around the area. The was one incident of 

“tug of war” in which two crabs pulled an 

empty shell back and forth between them 

for approximately ten minutes. Eventually 

the smaller crab walked away, and the 

larger crab switched into the empty shell. 

No other crabs came to take the shell left 

behind by that switch. 

Discussion 

While no SVCs were observed for C. 

vittatus, there was evidence of behaviors 

such as piggybacking and waiting that 

suggest that this species of hermit crab also 

utilizes this method of shell acquisition. It is 

possible that for this population, shells are 

not as vital as food—many individuals in the 

study area ignored the shells completely 

and spent their time feeding. The one shell 

switch I witnessed suggests that both 

synchronous and asynchronous vacany 

chains are useful methods of gaining new 

protective shells. It would require further 

investigation to evidence which method 

occurs more frequently for the marine hermit 

crabs of Spanish Lookout Caye. 


Rotjan D, Chabot J, and Lewis S. Social 

context of shell acquisition in Coenobita 

clypeatus hermit crabs. Behavioral Ecology. 

(2010) 21: 639-45. 

Tricarico E and Gherardi F. Shell acquisition 

by hermit crabs: which tactic is more 

efficient? Behavioral Ecology Sociobiology. 

(2006) 60: 492-500.


Lytechinus variegatus 

Kalie Bishop 

Ecology and Behavior of Manatees and 

Dolphins in 

Belize, Class of 2011 (contact: 

cselfsullivan@sirenian.org) 

Taxonomy 

Kingdom: Anamalia 


Class: Echinoidea 

Order: Temnopleuroida 

Family: Toxopneustida 

Genus: Lytechinus 

Species: Lytechinus variegates 

Ecology 

L. variegatus is commonly found in shallow, 

calm waters, such as seagrass beds. They 

have adapted to survive in many marine 

environments but primarily subsist within 

seagrass and kelp beds. L. variegatus 

inhabits the waters from North Carolina and 

Bermuda southward to the Caribbean and 

Brazil (Hendler et al. 1995). Although they 

cannot live in freshwater, they inhabit all 

depths and climates of the oceans. 


L. variegatus vary in color, but the most 

frequently seen are green, purple and light 

pink. L. variegatus have radially symmetrical 

bodies divided into five equal parts. The 

skeletal structure of the sea urchin is a rigid 

test or theca that is made up of plates 

encircling the mouth in the center of the oral 

side, encompassing the urchins inner 

organs (Nichols 1962). Spines, which can 

regenerate, cover the entire surface of the 

sea urchin test and play a role in protection 

as well as movement. Among the spines are 

five paired rows of tiny tube feet with 

suckers that help with locomotion, capturing 

food, and holding onto the seafloor. 

White variation of L. variegatus 

Behavior 

L. variegatus feed on decaying matter, kelp, 

sea grass, algae and occasionally even sea 

urchin skeletons. Sea urchins reproduce by 

releasing the unfertilized eggs and sperm 

into the water column, where the eggs are 

fertilized and develop into free-swimming 

larvae known as plutei (Pechenik 2000; 

Harvey 1956). The larval form 

of L. variegatus, as with most echinoderms, 

is very different from the adult form and 

must undergo a complex metamorphosis to 

reach adult form. 

Conservation 

Being primary grazers of kelp, and algae, L. 

variegatus play an important role within the 

marine communities that they inhabit. The 

population of L. variegatus in an area is vital 

to the health of the coral reef, as they 

eliminate the seaweed and algae that can 

consume coral if a balance is not 

maintained within the environment. The 

opposite can also occur with an increase in 

L. variegatus causing erosion on coral reef. 

It is crucial to have balance within the 

environment to maintain healthy 

populations, such as the population on 

Spanish lookout Caye.

Introduction 

Lunar reproductive rhythms have been part 

of fishermans folklore since ancient times. 

As described in much detail by H. Monroe 

Fox in 1923, “Sizes of certain marine 

invertebrates, chiefly mollusks and 

echinoderms varies with the phases of the 

moon.” On a field biology course studying 

the Drowned Cayes, I noticed that L. 

variegatus was in abundance along the 

seawall on the North facing aspect of 

Spanish lookout Caye off the coast of Belize 

City, Belize. The objective of my research 

is to determine if L. variegatus mass 

increases in relation to the lunar cycle. 

Methods 

I selected the North facing concrete seawall 

on the West side of Spanish Lookout Caye. 

On 08/07/2011, 80/09,2011, and 

08/10/2011, I removed 14 individuals from 

the area by placing them in a bucket filled 

with seawater. All debris was removed from 

each individual by hand, then removed from 

the bucket for 15 seconds then placed on a 

scale to record each individuals body mass. 

Individual photos were taken and were 

reviewed later for photo identification in 

chronological order. Due to technical 

difficulties, I was unable to analyze 

individuals with photo I.D. from 08/10/2011. 

Results 

Although there was a trend there was no 

significant increase in body mass between 

day one and day two. (t=1.67), (df=4), 

(p=0.08). Despite failure to meet statistical 

criteria, each individual increased slightly 

from day one to day two. This suggests that 

it is plausible that increase in body mass of 

L. variegatus correlates to the lunar cycle. 

Green variation of L. variegatus 

Discussion 

Further investigation should been 

conducted using a larger sample size. 

Photo identification methods should be 

performed with the same high pixel lens 

throughout the study to ensure photo 

identification methods are correct, as this 

skewed my data and conclusions. Further 

research should be conducted throughout 

the entire duration of the lunar cycle, from 

new moon until full moon. 


Hendler, G., Kier, P.M., Miller, J.E., 

Pawson, D.L. 1995. Sea Stars, Sea 

Urchins, and Allies: Echinoderms of 

Florida and the Caribbean. Washington: 

Smithsonian Institution Press; 390p 

Nichols, D. 1962. Echinoderms. London: 

Hutchinson & CO LTD; 192p. 

Pechenik, J.A. 2000. Biology of the 

Invertebrates, Fourth Edition. U.S.A.: 

McGraw-Hill Companies, Inc.; 578p.

Our Data Sheets 

We have designed our data sheets for long-term project use and built in redundancy to 

ensure we don’t miss data. They have been field tested over the past decade with high 

success. 

We organize the data sheets in field bins. Each bin should have sharpened pencils, a 

white eraser, and datasheets as described below. Please take the time to review these 

datasheets before fielding! 

We will use 5 bins total. Each volunteer/student will be responsible for one bin per day. 

After they master their data sheet, they will rotate jobs and teach each other, with 

oversight from the PI, Visiting Scientists, TAs, and Interns. The PI will personally teach 

and monitor for the first few days. If all goes as expected, interns and TAs will have 

mastered the forms with a few days in the field. 

One bin will have the Trip Summary (2-page data sheet). We should have 2 page-one 

of the Trip Summary per day (~20 per team) and 10 page-two per day (~100 per team). 

The team member who is responsible for this form is writing pretty much all day. 

The 2nd bin will have the Record of Effort (1-page data sheet) in it. We should have 4 

(front and back for a total 8) Record of Effort Sheets per day (~40/team). The team 

member who is responsible for this form is writing pretty much all day. 

The 3rd bin will have the Manatee Sighting and Scan (4-page data sheet). We should 

have 10 sets/day (~100/team). The team member who is responsible for this form is only 

writing during a scan or an opportunistic manatee sighting. 

The 4th bin will have the Habitat Sampling (4-page data sheet). We should have 10 

sets/day (~100/team). The team member who is responsible for this form is only writing 

during the habitat sample, which follows every scan. 

The 5th bin will have the Dolphin Survey (2-page data sheet). We should have 5 

sets/day (~50/team). The team member who is responsible for this form is documenting 

when we depart and return, but only writing down data when we encounter dolphins. 

Copies of our study site (map), marine life and bird field cards should also be kept in the 

bins.

TRIP SUMMARY SHEET (page 1) Day of the Week: 

Trip ID: Date: Julian Day: 

(yy-julianday-onedigittrip#) (dd-mon-yy) (001-365) 

EW Team #: # EW Vols: Total Obs: 

(yy-one digit team#) 

EW Team Members (first and last name): 

Researcher(s): Intern(s): Field Asst.: 

(first name) (firstname and initials) (firstname and initials) 

Effort Data Taken by: 

Sighting/Scan Data Taken by: 

Trip Summary Data Taken by: 

Behavioral Data Taken by: 

Seagrass Data Taken by: 

Locations (scan locations): ________________________________________________________ 

_________________________________________________________________________ 

Total # of Scans: Total # of Sightings (opp/scan): Total # Manatees:_______ 

GENERAL WEATHER CONDITIONS 

DEPART DOCK: WEATHER CHECK I : WEATHER CHECK II: 

RETURN DOCK: Time: Time: 

*TIDES IN ORDER: Wind Speed: mph Wind Speed: mph 

High: Wind Direction: Wind Direction: 

Low: Sea State: Sea State: 

High: Swell Height: ft Swell Height: ft 

Low: Cloud Cover: Cloud Cover: 

High: Water Temp: °C Water Temp: °C 

Low: Air Temp: °C Air Temp: °C 

Rainfall Overnight: Salinity: PPT Salinity: PPT 

Rainfall Today: Barometer: HPa Barometer: HPa 

Cruise Ships (#): 

Comments: 

* If a high or low falls pre/post today’s date, put in parentheses in order of occurrence. 

Please Complete Trip Log on reverse side and additional pages! 

CSS/KSL ____________ Trip Summary Sheet Page_______Of_______ 

(c) 2001-2004 Manatees in Belize - Earthwatch Project PIs: Katherine S. Lacommare & Caryn Self Sullivan -Updated 4/7/11

TRIP SUMMARY - LOG SHEET Date Page _____ of _____ 

Record All Events during the Day 

TIME WPoint EVENT LOCATION LATITUDE LONGITUDE COMMENTS 

17. 88. 














2001-2004 Manatees in Belize – Earthwatch Project PIs: Katherine S. LaCommare and Caryn Self Sullivan 4/7/2011

RECORD OF EFFORT DATA SHEET 

Event (include num.) Location or Route from/to: ____________________________ 

Enter one of the following: Travel (trav)– Survey (surv)– Pt. Scan (pscn) – Sighting (sght)– Sampling (samp)- Other Work (othw) – Lunch (lunc)– Other Free (othf) 

Start time _________Stop time _______Average Speed (km/hr) Trip (km)______________ 

Start WP (Garmin) _________ Stop WP (Garmin) ________EPE = _ # Manatees__________ 

Comments: 



Start time _________Stop time _______Average Speed (km/hr) Trip (km)_____________ 

Start WP (Garmin) _________ Stop WP (Garmin) ________EPE = __ # Manatees_________ 

Comments: 




Start WP (Garmin) _________ Stop WP (Garmin) ________EPE =__ # Manatees_________ 

Comments: 




Start WP (Garmin) _________ Stop WP (Garmin) ________EPE = __ # Manatees_________ 

Comments: 

DATE: ______________________ Effort Data Taken By? _____________________ 

(dd-mon-yy) 

Trip ID: _____________________ RECORD OF EFFORT Page _______of________ 

(yy-julianday-one digit trip#) 

(c) 2001-2007 Manatees in Belize - Earthwatch Project PIs: Caryn Self Sullivan & Katie LaCommare -Updated 4/7/11

MANATEE SIGHTINGS AND SCANS Page 1 of ____ ID # _______________________________ 

(yy-julianday-sight#scan#) 

Sighting Number Sight Start (24 hr) Sight Stop 

Point Scan Number Scan Start (24 hr) Scan Stop 

Sighting Type (circle one): Opportunistic or Scan 

Wayppoint (Garmin): EPE: 

Location: Loc. Code (see list for proper code): 

MUST Enter for both sightings and scans ONLY Enter code if this is a scan (whether there is a sighting or not). 

# Of Other Boats in area during scan: Distance (closest point) (1) (2) ___(3) 

Comments (size, type, speed) (1) (2) (3) 

Manatee Sighted By__________________ Confirmed By________________________ 

Enter one of the following: Researcher, Field Assistant, Intern, Volunteer, Team, Not confirmed 

*Total # Of Manatees No. Calves Calf Size NEW, YOY, OTHER 

1 ST 20 minutes of SCAN: Minimum: Maximum: Best Estimate: *TOTAL # DURING SIGHTING 

Total 30 minutes of SCAN: Minimum: Maximum: Best Estimate: 

__________________________________________________________________________________________ 

Initial Distance to 1st Manatee at 1 st Sighting (m): Time: Initial Movement of 1st Manatee: 

Aw from boat Towards boat Milling No change Undetermined 

(CIRCLE Distance Detection Method: DIRECT INDIRECT ESTIMATE) (CIRCLE initial movement in relationship to observation boat) 

Habitat Type: (Circle habitat where the manatee is, NOT the scan pt. ) UNDETERMINED Resting hole-yes or no or unk 

InBogue/OutBogue/Reef | Chann/ChannEdge/DeadEndBogue/Lagoon/Grassflat/UNK | Mud/Grass/Sand/Coral/UNK | Turtle/Shoal/Manatee/None/UNK 

DISTURBED? YES OR NO OR UNK Predominate Behavioral State (circle one): 

Feeding Resting Socializing Traveling Milling Undetermined Other (describe): 

__________________________________________________________________________________________ 

Initial Distance to 2 nd Manatee at 1 st Sighting (m): Time: Initial Movement of 2 nd Manatee: 







__________________________________________________________________________________________ 

Initial Distance to Center of Manatee Group at 1 st Sighting (m):____________________________________ 

U/W Video Attempt : yes no; if yes, was it successful? _____ Seagrass Sample/Habitat Sample/No Sample 

SIGHTING/SCAN CONDITIONS 

Glare 

Yes 

No 

Glare 

Direction 

Cloud cover 

clear 

scattered 

partly 

mostly 

overcast 

Precipitation 

Dry 

Light rain 

Heavy rain 

Sea State 

Swell Height Tide State* 

High (+/- 60m) 

Low (+/- 60m) 

Flood Ebb 

* If Scan Start Time falls within 60 min of High or Low Tide, then circle High or Low; if not and Scan Start Time falls b/t High and Low, circle Ebb; if not and Scan 

Start Time falls b/t Low and High, circle Flood. 

DATE: ______________________ Sighting/Scan Data Taken By? ______________ 

(dd-mon-yy) 

Trip ID: _____________________ SIGHTINGS AND SCANS Data Set _______of________ 

(yy-julianday-one digit trip#) 




Site Map: On this page you will sketch the characteristics of the scan point in relationship to the 

Boat. Map Perspective: illustrator is standing on the driver’s seat and facing north when 

looking towards the top of this page. Sketch the above water characteristics and draw a vector 

(distance & direction) to each landmark and to each manatee sighted. Label each manatee vector 

with time, distance, & direction. 

N 

W E 

S 




Comments:_________________________________________________________________________________ 

___________________________________________________________________________________________ 

CatalogID # _______________________ Marked / Un-Marked / Undetermined Sex: M / F / U Prop Scars? Yes / No 

RESIGHT? _______________________ Tape Start _______Stop______ Animal _____ of _____ captured on tape 

Enter Feature Codes* 2 (see below) 

for each unique marking seen on animal 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

__ __ __ __ __ __ __ __ __ __ 

Barnacles: Yes / No / Undetermined 

Number? ______ Size? ____________ 

Remoras: Yes / No / Undetermined 

Number? ________________________ 

Algae: Yes / No / Undetermined 

Color/Coverage? __________________ 

Medial Notch: Yes / No / Undetermined 

Comments? ______________________ 

Behavioral State: Rest / Feed / Travel / Social / Mill 

Play / Other / Undetermined 

Initial Reaction to diver: Approach / Retreat / No Change / Touch / Other 

Secondary Reaction to diver: Approach / Retreat / No Change / Touch / Other 

* 2 Identifying Feature Codes to use in blanks above, use one line for each unique marking: 

Type Region Position Number Size Color Shape 

S – scar D – dorsal F – flipper 1 – single L – large G – gray B – blotch 

M – mutilation L – left H – head 2 – 2 or 3 M – medium W – white L – line(s) 

D – deformity R – right A – ant. trunk 4 – 4 or more S – small 

F – freeze brand V – ventral B – mid. trunk 

N – medial notch C – post. trunk 

K – trunk plain D – peduncle 

L – tail plain X – ant. tail 

P – skin pigmentation Y – post. tail 




__________________________________________________________________________________________ 

Initial Distance to 3 rd Manatee at 1 st Sighting ((m): Time: Initial Movement of 3 rd Manatee: 







__________________________________________________________________________________________ 

Initial Distance to 4th Manatee at 1 st Sighting ((m): Time: Initial Movement of 4th Manatee: 







__________________________________________________________________________________________ 

Sighting Comments (con’t): 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 

____________________________________________________________________ 


Date: Page 1 of ____ Sight/Scan Record ID: 

(dd-mon-yy) (yy-julianday-sighting#scan#) 

HABITAT SAMPLING 

Sample ID: Data Recorded By: 

(yy-julianday-location code) 

LOCATION DATA 

LOC. CODE: WAYPOINT: LOCATION NAME: 

PHYSICAL DATA 

SECCHI READINGS (vertical secchi – take from center of boat; horizontal secchi – take from bow (0.5 meter) 

below the surface; secchi disk should face the sun.) 

Name (volunteer who took the data) Horiz. Vertical Depth Comments 

Air Temp 

°C 

H20 Temp 

Surface °C 

H20 Temp 

Bottom °C 

Salinity 

Surface ‰ 

Salinity 

Bottom ‰ 

Sea State 

Beaufort 

Swell 

Height (ft) 

Habitat Type: Circle the habitat characteristics of the scan point (where the boat is, NOT where the manatee 

was observed). This may be different from where the manatee was sighted or where the plot was set. 

InBogue/OutBogue/Reef | Chann/ChannEdge/DeadEndBogue/Lagoon/Cove/Grassflat 

Mud/Sandy Mud/Muddy Sand/ Sand/Coral | Turtle/Shoal/Manatee/None 

Comments and other description:___________________________________________________________________ 

______________________________________________________________________________________________ 

______________________________________________________________________________________________ 

PLOT DATA 

VECTOR (Distance in yards & Direction N, NE, E...) TO SAMPLE PLOT: 

Habitat Type: Circle the habitat characteristics of the plot NOT where the boat is but where the plot is. This 

may be different from where the boat is. 

InBogue/OutBogue/Reef | Chann/ChannEdge/DeadEndBogue/Lagoon/Cove/Grassflat | Mud/Sand/Coral | Turtle/Shoal/Manatee/None 

PLOT DEPTH at poles -- Center: North: South: East: West: 

Sediment Type (circle sediment type based on biomass cores): mud -- sand/coral – mud/sand -- -- other 

2001 Manatees in Belize – Earthwatch Project PIs: Katherine S. LaCommare and Caryn Self Sullivan 4/7/2011



BIOLOGICAL DATA 

BIOMASS CORES: (Enter zero if core would be empty; enter yes if core was taken; enter N/A if not taken. Take 

cores from the “a” corner of the small (density) quadrats. If you enter zero, a biomass datasheet must be filled out!!! This 

does not need to be entered into the database) 

N:__________S:__________E:__________W:__________ 

DENSITY COUNTS 

4 samples: 

See plot design for sample layout. 

At least 2 Replicas: If possible, each replica should be taken by the same person. Please make comments about person 

who took data i.e., intern, volunteer etc.) 

Replica 1: Name (volunteer who took the data): 

A quarter B quarter C quarter D quarter Total 

N: T/ S/ M T/ S/ M T/ S/ M T/ S/ M T/ S/ M 

S: T/ S/ M T/ S/ M T/ S/ M T/ S/ M T/ S/ M 

E: T/ S/ M T/ S/ M T/ S/ M T/ S/ M T/ S/ M 

W: T/ S/ M T/ S/ M T/ S/ M T/ S/ M T/ S/ M 
















PERCENT COVER (1 x 1 m QUADRAT) 

4 samples N,S,E,W: See plot design for sample layout. Each quadrat will be rolled 5 times. 


Sample N (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample S (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample E (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample W (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 





Sample N (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample S (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample E (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


Sample W (grand total is entered into database) (rows 1-10) 

1 

2 

3 

4 

5 

Total 

Grand Total 


DOLPHIN ENCOUNTER: Boat-Based Data Sheet Location: Drowned Cayes, Belize, Central America 

Survey # Encounter # Date: 20____ Boat: Captain: Photographer: # of images: 

(day month) 

Survey Start Time: End Time: Effort: Hours with Dolphins: Sunrise: Sunset: Moonrise: Moonset: 

Tide 1stHigh: 1stLow: High: Low: High: Total Survey Effort to Date: Total Hours with Dolphins to Date: Total Images to Date: 

Start Initial GPS Reading Sea Water Water Sighting Description Identified IDs: 

Time Tide State Swell Depth Temp Area Habitat Other Objects 

N W (m) (m) (C) General Comments: 

End Final GPS Reading Sea Water Water 

Sighting Description 

Time Tide State Swell Depth Temp Area Habitat Other Objects 

N W (m) (m) (C) 

Time Group Estimate ID Ratio 

Group Membership Marked: 

Calves Juveniles Adults Unmarked: 

< 1 month 1 - 3 mos 3 - 6 mos 6 - 10 mos Total < 1 yr 1 - 2 yr Total: 

Best Estimate ID-Ratio: 

SIGHTING LOG 

Way GPS Reading Area / Habitat Water Group Behavior Response to 

Time Pnt. N W Boats / Birds / Other depth Size State Research Vessel Notes and Comments 

Contact Details: Dr. Caryn Self-Sullivan, Ph.D., Sirenian International, 200 Stonewall Drive, Fredericksburg, VA 22401 Email: caryns@sirenian.org; Phone: 540.287.8207

Sighting Log Continued from Page 1 

Way GPS Reading Area / Habitat Water Group Behavior Response to 

Time Pnt. N W Boats / Birds / Other depth Size State Research Vessel Notes and Comments 

Contact Details: Dr. Caryn Self-Sullivan, Ph.D., Sirenian International, 200 Stonewall Drive, Fredericksburg, VA 22401 Email: caryns@sirenian.org; Phone: 540.287.8207


200 Stonewall Drive, Fredericksburg, VA 22401-2110 

cselfsullivan@gmail.com | 540.287.8207 

Education 

Ph. D. 2008 Texas A&M University, College Station, TX, Department of Wildlife and Fisheries Sciences 

B. S. 1997 Coastal Carolina University, Conway, Department of Marine Science, minors in Biology and 

Mathematics 

2000 Pennsylvania State University, Graduate Program in Acoustics, non-degree seeking student (June) 

1996 Deakin University, Geelong, Victoria, Australia, exchange student (July-December) 

Professional Positions 

2011-Present Distance-Education Faculty (Adjunct), Fischler School of Education and the Oceanographic Center, 

Nova Southeastern University 

2010-2011 Assistant Professor (visiting, full-time faculty) Department of Fisheries & Wildlife, Virginia Tech 

2008-2010 Assistant Professor (temporary, full-time faculty) Department of Biology, Georgia Southern University 

2008 Substitute Teacher (Secondary Level) for Spotsylvania, Stafford, Fredericksburg, VA 

2010-Present Technical Expert to Friends of Swallow Caye, Swallow Caye Wildlife Sanctuary, Belize 

2010-Present Technical Expert to the Sarteneja Allicance for Conservation & Development, Corozol Bay Wildlife 

Sanctuary, Belize 

2007-Present Marine Science Advisor, Hugh Parkey Foundation for Marine Awareness & Education, Belize 

2005-Present Principal Advisor, NCRC Community Conservation of West African Manatees in Volta Lake, Ghana 

2005-Present Member, IUCN Species Survival Commission Sirenia Specialist Group 

2004-Present Member, Belize National Manatee Working Group 

2004-Present Member, Belize Marine Mammal Stranding Network 

2000-Present President & Co-founder, Sirenian International, Inc. 

1998-Present Principal Investigator, Ecology and Behavior of Antillean Manatees and Bottlenose Dolphins in the 

Drowned Cayes Area of Belize 

2004-2007 Director of Research & Education, Spanish Bay Conservation & Research Center and the Hugh Parkey 

Foundation for Marine Awareness and Education, Belize 

Professional Memberships: National Science Teachers Association (NSTA), North American Association for 

Environmental Education (NAAEE), Society for Marine Mammalogy (SMM), Society for 

Conservation Biology (SCB), Animal Behavior Society (ABS), American Pet Dog Trainers 

Association (APDT), Karen Pryor Academy Certified Training Partner (KPA CTP), Sirenian 

International (SI) 

Teaching Experience 

2011-Present OCEE 540 Interpreting our Environment, Nova Southeastern University, Florida 

2011-Present OCEE 520 Teaching Environmental Concepts, Nova Southeastern University, Florida 

2010-2010 FIW 4314 Conservation Biology, Department of Fisheries & Wildlife Sciences, Virginia Tech 

2008-2010 BIOL 1130 General Biology, Department of Biology, Georgia Southern University 

2009-2010 BIOL 2108L Biology of Organisms Lab, Department of Biology, Georgia Southern University 

2009-2010 BIOL 2108SI Biology of Organisms Supplemental Instruction, Georgia Southern University 

2006-2011 Behavior, Ecology, and Conservation of Manatees & Dolphins in Belize, Independent Course with 

approved credit hours accepted by ~ a dozen accredited U.S. universities. 

2007-2009 EW/NCRC West African Fellows Manatee Conservation Workshop, Ghana, West Africa 

2008 Substitute for high school science classes in Spotsylvania, Stafford, & Fredericksburg, VA 

2004-2008 Marine Biology for Primary & Secondary Teachers Workshop, Belize Ministry of Education 

2004-2008 Biology of Mangroves, Sea Grass & Coral Reefs Field Course, Belize Ministry of Education 

1993-1997 Marine Biology, Chemistry, Mathematics, and Scientific Writing tutor, Coastal Carolina University 

1986-1993 Principals of Real Estate, Real Estate Brokerage, Real Estate Finance, Fair Housing, and Continuing 

Education Courses, Fredericksburg Area Association of Realtors, Virginia Real Estate Commission 

Additional Training in Education 

2011 KPA: Karen Pryor Academy Certified Training Partner 

2011 TTI: TAGteach International Certification 

2011 CCPDT: Real Solutions for Canine Behavior Problems by Pat Miller (June 11-12, 2011) 

2011 NSU: Blackboard Learn Distance-Education Training 

Caryn Self-Sullivan CV Page 1 of 1 Updated 

12/10/2011

2010 VT: Scholar, BANNER, Safe Zone Training 

2010 GSU: Teaching Large Classes, Teaching What You Don’t Know, Thinking Like Leonardo, Safe Space 

Training, Creating a Safe Learning Environment; Service-Learning "All for One and One for All 

Integrating Service with Teaching and Scholarship for Maximum Impact"; Successful Grant Writing 

Workshop; Inertia vs. Critical Mass Engaging Students in Active Discussions, Team-Based Learning-A 

Transformational Use of Small Groups in College Teaching; Scholarship of Teaching and Learning 

Commons; Teaching Large Classes FLC; Lab Safety Training, VISTA/WebCT/Blackboard/GeorgiaView; 

Service-Learning; CPS Classroom System; WINGS, BANNER, The Art of Changing the Brain; Teaching 

Large Classes FLC; POGIL Workshop; Active Learning in Large Classes; Active Learning for Students 

Graduate Students 

2011-Present Kristin Montour-Grubbs, Nova Southeastern University, M.S. Student, Committee Chair 

2011-Present Allen Conrad Allen, Nova Southeastern University, M.S. Student, Mentor 

2006-Present Haydee Dominguez, Duke University, Ph.D. Student, Mentor, Field Advisor, External Advisor. 2011 

Proposal: Manatees in the Dominican Republic. 

2006-2008 Marie-Lys Bacchus, Loma Linda University. M.S., Mentor, Field Advisor, Committee Member. 2007 

Thesis: Characterization of Resting Holes and Use by the Antillean Manatee (Trichechus manatus 

manatus). 

2009-2011 Kamla Aristide, University of Dschang, Cameroon, M.S. Student. Mentor, Co-advisor. 2011 Thesis: 

Activity Center, Habitat Use and Conservation of the West African Manatee (Trichechus senegalensis 

Link, 1795) in the Douala-Edea Wildlife Reserve and Lake Ossa Wildlife Researve. 

2008-2009 Andrea Tanny, Georgia Southern University, M.S. Student, Mentor, Field Advisor, Committee Member. 

MS Proposal: 2008 Foraging Behavior in West Indian Manatees. 

Publications 

Appletons, W. et al. (in review). Magnitude of global marine biodiversity: one third of sea creatures discovered. 

Submitted to Science on 15 October 2010. 

Bacchus, M-L, S. G. Dunbar, C. Self-Sullivan. 2009. Characterization of resting holes and their use by the Antillean 

manatee (Trichechus manatus manatus) in the Drowned Cayes of Belize. Aquatic Mammals 35(1)62-71. 

Deutsch, C. J., C. Self-Sullivan, and A. A. Mignucci-Giannoni. 2007. Trichechus manatus. In 2007 IUCN Red List of 

Threatened Species (www.iucnredlist.org). 

Hoffman, M., et al. 2010. The impact and shortfall of conservation on the status of the world’s vertebrates. Published 

in Science Express online 10/26/2010; pending print publication date. 

LaCommare, K. S., C. Self-Sullivan, and S. Brault. 2008. Distribution and Habitat Use of Antillean Manatees 

(Trichechus manatus manatus) in the Drowned Cays Area of Belize, Central America. Aquatic Mammals 

34(1)34-43. 

LaCommare, K.S., S. Brault, C. Self-Sullivan, E.M. Hines. (in review). A Boat-based Method for Monitoring 

Sirenians: Antillean Manatee Case Study. 

Schipper, J., et al. 2008. The status of the world's land and marine mammals: diversity, threat, and knowledge. 

Science 322225-230, 10 October 2008. DOI 10.1126/science.1165115. 

Self-Sullivan, C. 2004-2010. Manatee and mangrove special topics in the 6th, 7th, & 8th editions of Moon 

Handbooks Belize by Joshua Berman and Chicki Mallan, Avalon Travel Publishing, Emeryville, CA. 

Self-Sullivan, C. 2008. Conservation of Antillean Manatees in the Drowned Cayes Areas of Belize. Ph.D. 

Dissertation, Department of Wildlife and Fisheries Sciences, Texas A&M University. 

Self-Sullivan, C. (in press). West Indian Manatees (Trichechus manatus) in the Wider Caribbean Region. Book 

Chapter in Sirenian Conservation Issues and Strategies in Developing Countries. Edited by Ellen Hines, John 

Reynolds, Lemnuel Aragones, Antonio A. Mignucci-Giannoni, Miriam Marmontel. University of Florida 

Press. 

Self-Sullivan, C. and A. A. Mignucci-Giannoni. 2007. Trichechus manatus manatus. In 2007 IUCN Red List of 

Threatened Species (www.iucnredlist.org). 

Self-Sullivan, C., and L. Bird. 2007. Marine Science for Students Workbook. BRC Publishers, Benque, Belize. 

Self-Sullivan, C., Smith, G. W., Packard, J. M., and LaCommare, K. S. 2003. Seasonal occurrence of male Antillean 

manatees (Trichechus manatus manatus) on the Belize Barrier Reef. Aquatic Mammals 29(3)342-354. 

Williams, Jr., E. H., Mignucci-Giannoni, A. A., Bunkley-Williams, L., Bonde, R. K., Self-Sullivan, C., Preen, A., and 

Cockcroft, V. G. 2003. Echeneid-sirenian associations, with information on sharksucker diet. Journal of Fish 

Biology 631176-1183. 


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Unpublished Reports 

Ofori-Danson, Patrick, Caryn Self-Sullivan, Victor M. Mombu, and Martin A. Yelibora. 2008. Enhancing 

Conservation of the West African Manatee in Ghana 2007 Annual Report. Prepared by Nature Conservation 

Research Centre (NCRC), P. O. Box KN925, Accra. June 2008. 

Self-Sullivan, C. 2006. Report to NCRC on an Insular Population of West African Manatees (Trichechus 

senegalensis) in the Upper Afram Arm of Volta Lake. 

Self-Sullivan, C., and K. S. LaCommare. 1998-2010. Annual Progress Reports to Belize Forestry Department, Belize 

Fisheries Department, Belize Coastal Zone Management Authority & Institute, Friends of Swallow Caye, 

Earthwatch Institute. 

Self-Sullivan, C., M. Fogel, and M. J. Wooller. 2005. Carbon and nitrogen stable isotope analyses of Antillean 

manatees from three distinct ecosystems in Belize inference about relative differences in diets and habitats. 

Preliminary Report to Wildlife Trust Belize, 30 October 2005. 

Conference Presentations & Posters 

Bonde, R. K., P. Lewis, D. A. Samuelson, C. Self-Sullivan, N. E. Auil, and J. A. Powell. 2006. Belize manatee 

(Trichechus manatus manatus) epibionts SEM viewing techniques. Poster Presentation at SMM 16 th Biennial 

Conference on the Biology of Marine Mammals, San Diego, 12-16 December 2005. 

LaCommare, K. S., C. Self-Sullivan, and S. Brault. 2005. Distribution, habitat use and seasonal occurrence of 

Antillean manatees in the Drowned Cayes area of Belize, Central America. Oral Presentation at the SMM 

16th Biennial Conference on the Biology of Marine Mammals, San Diego, 12-16 December 2005. 

LaCommare, K. S., Sullivan, C. S., Brault, S. 2001. Distribution and Foraging Ecology of Antillean Manatees 

(Trichechus manatus) in the Drowned Cays Area of Belize, Central America. Poster Presentation at the SMM 

14 th Biennial Conference on the Biology of Marine Mammals, Vancouver, British Columbia, 28 November - 3 

December 2001. 

Mignucci-Giannoni, A. A., and C. Self-Sullivan. 2005. Conservation Status of the Antillean Manatee (Trichechus 

manatus manatus) in the Wider Caribbean Region. Oral Presentation at the International Sirenian Workshop, 

SMM 16 th Biennial Conference on the Biology of Marine Mammals, San Diego, 12-16 December 2005. 

Self-Sullivan, C. 2009. Conservation of Antillean manatees in Belize 1998-2008. Oral presentation at the 2009 

International Sirenian Conservation Conference, 23-24 March 2009. 

Self-Sullivan, C. 2009. Triumph on the commons in Belize the importance of traditional knowledge and stakeholder 

input to successful MPAs. Oral Presentation at the Sirenian Workshop, Improving the Contribution of Marine 

Protected Areas to the Conservation of Sirenians. Society for Conservation Biology Marine Section, 

International Marine Conservation Congress, May 21-24, 2009, Johnson Center, George Mason University, 

Fairfax, Virginia, USA. 

Self-Sullivan, C. 2008. Conservation of Antillean manatees in Belize. Seminar (3 hours) at Coastal Zone 

Management Authority and Institute, Belize City, Belize. 

Self-Sullivan, C. 2006. Non-lethal boat scars on manatees in Belize as a tool for evaluation of a Marine Protected 

Area. Oral Presentation at the 59th Annual Gulf and Caribbean Fisheries Institute Conference, Belize City, 6- 

11 November 2006 (Science and Management of Marine Protected Areas Session). 

Self-Sullivan, C. 2007. Community Conservation of West African Manatees in the Upper Afram Arm of Volta Lake, 

Ghana. Oral Presentation, Marine Mammals & Indigenous Communities Workshop, SMM 17th Biennial 

Conference on the Biology of Marine Mammals, Cape Town, November 2007. 

Self-Sullivan, C. 2007. Conservation and Status of West African Manatees in Ghana, Senegal, Nigeria, Cameroon, 

and Sierra Leone. Oral Presentation, Marine Mammals in Africa Workshop, SMM 17th Biennial Conference 

on the Biology of Marine Mammals, Cape Town, November 2007. 

Self-Sullivan, C. LaCommare, K.S. 2003. One Issue Related to Research and Conservation: Cruise Ship Tourism in 

Belize. Oral Presentation at the International Sirenian Workshop, SMM 15 th Biennial Conference on the 

Biology of Marine Mammals, Greensboro, North Carolina, 14 December 2003. 

Self-Sullivan, C., and A. A. Mignucci-Giannoni. 2006. Conservation Status of the Antillean Manatee (Trichechus 

manatus manatus) in the Wider Caribbean Region. Oral Presentation at IMC9, Sapporo, Japan, 31 July 2005. 

Self-Sullivan, Caryn. 1996. A Survey of Macroalgae in Discovery Bay, Jamaica Species Diversity and Zonation 

Differences in the Lagoon. Senior Thesis, Coastal Carolina University, SC Oral presentation to Discovery 

Bay Lab, Jamaica. 

Self-Sullivan, Caryn. 1996. The Effects of Benthos on Acartia tonsa Population Dynamics. National Conference on 

Undergraduate Research, Ashville, NC POSTER - Results of NSF-REU Fellowship research. Oral 


12/10/2011

presentation to Horn Point Environmental Lab and Coastal Carolina University. 

Sullivan, C. S., LaCommare, K. S., Packard, J. M., and Evans, W. E. 2001. Seasonal Occurrence of Male Antillean 

Manatees (Trichechus manatus manatus) on the Belize Barrier Reef and the Effect of Scale on Seasonal 

Distribution Studies. Poster Presentation at the SMM 14 th Biennial Conference on the Biology of Marine 

Mammals, Vancouver, British Columbia, 28 November - 3 December 2001. 

Sullivan, C. S., Packard, J. M., and Evans, W. E. 1999. Spring distribution and behavior of Antillean manatees in the 

Drowned Cayes, Belize. Poster Presentation at the SMM 13th Biennial Conference on the Biology of Marine 

Mammals, Maui, Hawaii, November 28 - December 3, 1999. 

Achievements, Awards, Honors 

• 2011 B.F. Skinner Scholarship, KPA 

• 2009 CCU COS Alumnus of the Year 

• 2003 Earthwatch Young Scientist Award 

• 1998-2001 NSF Graduate Fellowship 

• 1997 Outstanding Marine Science Senior 

• 1997 President's Excellence Nominee 

• 1996 Exchange student to Deakin 

University 

• 1995 NSF-REU Fellowship 

• 1994-1997 Nelson Scholarship 

• 1993 Freshman Essay Contest 

• 1993-1997 President's Honor List 

• 1993-1997 Dean's Honor List 

• Sigma Zeta Beta Mu Honor Society 

• Omicron Delta Kappa Society 

• Pi Mu Epsilon Honor Society 

Grants and Fellowships 

• Marine Mammal Commission 2009. Sirenian/MPA Workshop. Amount funded $12,105. 

• Earthwatch Institute, Center for Research 2001-2007. Field Research. Amount funded ~ $56,000/year 

• UNDP/GEF/COMPACT, 2006. HPF Educational Outreach Programme. Amount funded $40,000USD 

• Project AWARE Small Grant Program 2004. Field Research. Amount Funded $1,000 

• Earthwatch Institute, Center for Research 2003 Young Scientist Award. Amount funded $2,500 

• Conservation Action Fund, New England Aquarium 2001. Capacity Building Grant. Amount funded $5,000 

• American Museum of Natural History Lerner-Grey Fund for Marine Research 2000. Field Research. Amount 

funded $2,000. 

• Oceanic Society 1998-1999. Field Research. Amount funded undisclosed (9 months of field research in Belize) 

• National Science Foundation Graduate Fellowship 1998-2001. Tuition & Stipend. Amount funded $75,000 

Other Service Projects 

• Workshop Organizer Society for Conservation Biology, 2009 IMCC Conference, Sirenians and MPAs 

• Peer reviewer for academic journals: Aquatic Mammals, Behaviour, Journal of Wildlife Management, USGS 

Sirenia Project, Journal of Environmental Studies and Sciences, Estuaries & Coasts 

• Scientific Advisor to field scientists from Guatemala, Ghana, and Dominican Republic regarding techniques for 

evaluating manatee populations in remote areas, with an emphasis on the incorporation of manatee behavior 

• Mentor young people (especially women) entering the sciences (M.S., Ph.D. students and interns) 

• Science Judge National Oceans Science Bowl Regional Competition, Texas A&M, 2006 

• Coordinator National Marine Science Symposium, Belize City, Belize 2006 

• Coordinator National Marine Science Quiz Bowl, Belize City, Belize 2006-2007. 

• Committee Member Society for Marine Mammalogy Conference Committee, 2003 

Educational Outreach Publications and Presentation: >100 public presentations on animal behavior, marine mammals, 

marine and environmental science through NGO and academic organizations including: public schools & dive clubs, the 

Sierra Club, Green Drinks, New England Aquarium, Coastal Carolina University, Mary Washington University, Texas 

A&M University, Universidad Autonoma de Santo Domingo, Rutgers University, Georgian Court University, Brookdale 

Community College, The Wetlands Institute, and at community festivals, etc. 

References 

Jane Dougan, Distance-Ed Coordinator, Nova Southeastern University, douganj@nova.edu, 866.229.2557 

Stephen P. Vives, Ph.D., Georgia Southern University, Statesboro, GA, svives@georgiasouthern.edu, 912.478.5487 

Bruce A. Schulte, Ph.D., Western Kentucky University, Bowling Green, KY, bruce.schulte@wku.edu, 270.745.5999 

Jessica R. Young, Ph.D., Western State College of Colorado, jyoung@western.edu, 970.943.3045 

Michelle Kopfer, Teaching Assistant, Virginia Tech, Blacksburg, VA, midavis1@vt.edu, 540.577.1081 

Paul J. Camp, Ph.D., Professor, Spelman College, pjcamp@gmail.com, 404.270.5864 

Jane M. Packard, Ph.D., Professor, Texas A&M University, College Station, TX, j-packard@tamu.edu, 979.845.1465 

Wyndylyn von Zharen, Ed.D., J.D., Professor, Texas A&M University, dr_vonzharen@msn.com, 409.740.4485 


12/10/2011

145 S. Tompkins Street 

Howell, MI 48843 

K ATHERINE S PENCER L A C OMMARE 

EDUCATION 

PhD. June 2011. Environmental Biology, University of Massachusetts, Boston, MA 

MSc. 1994. Forestry and Natural Resources, Purdue University, West Lafayette, IN 

B.Sc. 1989. Anthropology/Zoology, University of Michigan, Ann Arbor, MI 

Kslacommare@gmail.com 

(248) 756-3985 

TEACHING EXPERIENCE 

Instructor: Introduction to Environmental Science (2004, 2008-2011). Face-to-face; Hybrid, 

Online. Lansing Community College, Lansing, MI, 

Instructor: Organismal Biology (2010-2011). Face-to-face. Lansing Community College, Lansing, 

MI, 

Instructor: Behavior and Conservation of Marine Mammals Field Course. (2008-2010) Spanish 

Bay Research and Education Center, Belize, C.A. 

Field Instructor: Coastal Ecology and Marine Mammal Ecology (1998-2007) Oceanic Society, 

Earthwatch 

Teaching Assistant: Cell Biology (2001). University of Massachusetts, Boston 

Teaching Assistant: General Biology (2001). University of Massachusetts, Boston 

Writing Instructor: Introduction to Environmental Science (1999-2000), University of 

Massachusetts, Boston, 

PROFESSIONAL DEVELOPMENT AND CERTIFICATIONS 

University of Michigan Community College Biology Active Learning Workshop: August 

2011, Ann Arbor, MI 

Teaching Ecology to Undergraduates: Spring 2011. Pierce Creek Institute, Hastings MI. 

What should college biology look like? the first two years: Spring 2001. Michigan State 

University 

Leading Effective Discussions: Spring 2010. Lilly Seminar Series – Michigan State University 

Transforming Learning Through Teaching: Spring 2009. 14-week professional development 

course through Lansing Community College’s Center for Teaching Excellence. 

Michigan Virtual University Certification: Fall 2008 

PROFESSIONAL EXPERIENCE 

Principal Investigator: January 2001 – December 2003, Co-PI: January 2004 – Dec. 2007, Manatees in 

Belize, Earthwatch Project (part-time, contract) 

• Managed all project logistics: developed and managed the budget, hired and supervised staff, 

recruited and hired student interns, trained interns and volunteers, completed endangered species 

permit applications, wrote agency reports, wrote and received grants, hired vendors, conducted 

government relations and managed volunteer activities and developed and managed education 

activities.

• Developed and managed educational activities including: determining priorities, developing 

curriculum and leading expedition activities for students and volunteers. 

• Designed research protocol. Collected, analyzed, presented and published project data. Utilized 

Excel, SPSS, MatLab. 

• Managed data collection, training, education and field trips for 1-5 two-week teams per year of 8-24 

volunteers per team. 

• Managed project logistics: budgets ($43,000 per year), permits, agency reports, and vendors. 

• Managed 2-3 field assistants and student interns per team. 

• Networked with local agencies and NGO’s to develop an appropriate manatee research program. 

• Conducted 1-3 public/professional speaking events per year. 

• Authored or co-authored 4 scientific papers. 

• Designed and maintained an Access database to archive, organize and house individual manatee, 

manatee population, habitat and seagrass data. 

Aerial observer, (Part-time - contract) April - May 2001, National Marine Fisheries Service, Northeast 

Fisheries Science Center, Woods Hole, MA. Supervisor: Pat Gerrior. 

• Participated in line transect surveys from a twin engine Otter for right and other large whales off 

the Massachusetts coast. 

Fisheries Research Biologist, May 1999 – August 2000, National Marine Fisheries Service, Northeast 

Fisheries Science Center. CMER Assistantship program, Woods Hole, MA. Supervisor: Tim Smith 

• Analyzed distribution and habitat ecology of Brydes whales in the North Pacific with ArcView GIS 

and SPlus statistical package. 

Field Naturalist and Biologist: (Contract Position) October 1998 – March 2000, Oceanic Society 

Expeditions, Belize Dolphin/Manatee Project, Drowned Cayes, Belize, Central America 

• Designed research methods, collected and analyzed data on the habitat and foraging ecology of 

manatees. 

• Coordinated volunteer data collection. 

• Coordinated daily educational and natural history activities for volunteers. 

Land Protection Specialist: March 1995 – October 1998, The Nature Conservancy, Michigan Field 

Office, East Lansing, MI, Supervisor: Bill McCort 

• Developed and managed a landowner education program to promote conservation stewardship of 

private lands. Program activities included educating landowners about endangered habitats and 

assisting them in maintaining these habitats on their property. 

Natural Areas Preservation Assistant: October 1994 – March 1995, Ann Arbor Parks and Recreation 

Department, Ann Arbor, MI, Supervisor: David Borneman 

• Assisted Natural Areas Preservation Coordinator with general duties. 

• Managed plant inventory database. 

• Coordinated volunteer workdays in city parks. 

PUBLICATIONS 

LaCommare, Katherine et al. (in review). A Boat-based Method for monitoring Sirenians: Antillean 

Manatee Case Study. Biological Conservation 

Aragones, Lemenuel; Katherine S. LaCommare, Sarita Kendall, Delma Nataly Castelblanco- 

Martinez, Daniel Gonzalez-Socoloske. In press. Boat and Land-based Surveys for Sirenians in 

Developing Nations. In Hines et al. International Strategies for Manatee and Dugong 

Conservation. Florida University Press 

LaCommare, Katherine et al. 2008. Distribution and Habitat Use of Antillean Manatees in the Drowned 

Cayes Area of Belize, Central America. Aquatic Mammals Journal. 34(1): 35-42

Self Sullivan, Caryn, Gregory W. Smith, Jane M. Packard, Katherine S. LaCommare. 2003. 

Seasonal Occurrence of Male Antillean Manatees (Trichechus manatus manatus) on the Belize Barrier Reef. 

Aquatic Mammals. 29(3): 342-354. 

Weiler, Katherine S. and Joseph T. O’Leary. May 1994. Demographic Change and Forest Resources: 

Implications for the Lake States. Lake States Forest Resource Assessment. 

PUBLICATIONS IN PREPARATION 

LaCommare, Katherine et al. (in prep). Coastal Development in Belize: Impact on Manatees and 

Seagrass.. Aquatic Botany. 

LaCommare, Katherine et al. (in prep). Conservation Planning for Antillean Manatees in Belize. 

Conservation Biology. 

POPULAR PUBLICATIONS 

LaCommare, Katherine S. Fall 2000. Sirenian Song. Fall newsletter for the Evergreen Group’s Manatee 

ambassador program 

LaCommare, Katherine S. Spring 2000. Sirenian Song. Spring newsletter for the Evergreen Group’s 

Manatee ambassador program 

LaCommare, Katherine S. Fall 1999. Sirenian Song. Fall newsletter for the Evergreen Group’s Manatee 

ambassador program 

Adimey, Nicole M. and Katherine S. Weiler. October 1994. Orcas of Johnstone Strait. Waterway Times 

Weiler, Katherine. December 1994. The Bald Eagle Soars, But What About the Fuzzy Sandoze? The Bard 

PRESENTATIONS AT NATIONAL CONFERENCES 

LaCommare, Katherine et al May 2011. Oral Presentation. A Boat-based method for monitoring 

Sirenians: Antillean Manatee Case Study. Oral Presentation. International Marine Conservation 

Congress. Victoria, BC Canada. May 2011. 

LaCommare, Katherine et al. May 2009. Mangrove Clearing and Bottom Dredging: How is Antillean 

Manatee (Trichechus manatus manatus) Habitat Use Affected by Coastal Development in Belize?. Oral 

Presentation. International Marine Conservation Congress. Washington, DC. May 2009. 

LaCommare, Katherine et al. December 2005. Distribution, Seasonal Occurrence and Habitat Use of 

Antillean Manatees in the Drowned Cayes Area of Belize, Central America. Oral Presentation. 16th Biennial Conference on the biology of Marine Mammals. San Diego, California. November 

2005. 

LaCommare, Katherine et al. December 2003. Habitat Use of Seagrass in the Drowned Cayes Area of 

Belize, Central America. Poster Presentation. 15th Biennial Conference on the biology of Marine 

Mammals. Greensborough, SC. 

LaCommare, Katherine et al. December 2001. Habitat Use of Antillean Manatees in the Drowned Cayes 

Area of Belize, Central America. Poster Presentation. 14th Biennial Conference on the biology of 

Marine Mammals. Vancouver, BC 

INVITED PRESENTATIONS 

LaCommare, Katherine S. April 2002. Habitat Ecology of Antillean Manatees in the Drowned Cayes Area 

of Belize. Earthwatch Chicago, Spring Event, Kent Culinary Institute, Chicago, IL 

LaCommare, Katherine S. March 2002. Habitat Ecology of Antillean Manatees in the Drowned Cayes 

Area of Belize. Science in Action Lecture Series, Maritime Aquarium, Norwalk, CT

LaCommare, Katherine S. November 2001. Habitat Ecology of Antillean Manatees in the Drowned Cayes 

Area of Belize. Lowell Lecture Series, New England Aquarium, Boston, MA 

FUNDING AND AWARDS 

June 2007 Dissertation Improvement Grant, University of Massachusetts, Office of Sponsored 

Programs. Project Title: Ecology and Behavior of Antillean Manatees in the Drowned Cays, Belize, Central 

America. Funding: $1,200 

January 2003 – December 2006. Co-Principal Investigator. Earthwatch Institute. Project Title: Ecology 

and Behavior of Antillean Manatees in the Drowned Cays, Belize, Central America. Funding: $43,000/year 

October 2002. Young Scientist Award. Earthwatch Institute. Project Title: Ecology and Behavior of 

Antillean Manatees in the Drowned Cays, Belize, Central America. Funding: $5,000 

January 2001 – December 2003. Principal Investigator. Project Title: Ecology and Behavior of Antillean 

Manatees in the Drowned Cays, Belize, Central America. Funding: $43,000/year 

December 2000. Conservation Action Fund. Project Title: Ecology and Behavior of Antillean Manatees in the 

Drowned Cays, Belize, Central America. Award: $5,120 

ADVISORY BOARDS/PROFESSIONAL SOCIETIES 

Livingston Land Conservancy, Board of Directors, Fundraising and Membership Chair, (2010present) 

Livingston Land Conservancy, Fundraising Committee (2004, 2010) 

Sirenian International, Inc., Co-founder 

Sirenian International, Inc.,Board of Directors, Secretary, (2000-2005) 

Michigan Science Teachers Association, Member 

National Science Teachers Association, Member 

Michigan Association of Community College Biology Teachers, Member 

Science Department Curriculum Committee, Adjunct Faculty Representative 

REFERENCES 

Meg Clark Elias, Professor, Science Department, Lansing Community College, Lansing, MI 48933. (517) 

483-1557, Clarkm1@lcc.edu 

Solange Brault, Associate Professor, University of Massachusetts, Boston, Department of Biology, 100 

Morrissey Blvd., Boston, MA 02125. (617) 287-6683, Solange.brault@umb.edu 

Robert Stevenson, Associate Professor, University of Massachusetts, Boston, Department of Biology, 100 

Morrissey Blvd., Boston, MA 02125. (617) 287-6579, Robert.stevenson@umb.edu 

Caryn Self Sullivan, Adjunct Faculty, Nova Southeastern University, President, Sirenian International. (540) 

287-8207, cselfsullivan@sirenian.org 

William D. McCort, Ph.D., Director and Manager of Canine Professor LLC, Chair, Natural Areas Technical 

Advisory Committee, Natural Areas Preservation Program, Washtenaw County Parks & Recreation 

Department, Volunteer, Land Protection Committee, Washtenaw Land Trust, 18819 Bush Road, 

Chelsea, MI 48118-9749. 734-475-6908, billmccort@comcast.net

CURRICULUM VITAE 

HEATHER J. KALB 

Department of Natural Sciences and Mathematics, West Liberty University, 

West Liberty University, West Liberty, WV 26074 

(812) 461-8965 (C); heather.kalb@westliberty.edu 

Education 

Ph.D. in Zoology, 1999. Dept. Biology, Texas A&M University, College Station, TX. “Behavior and 

Physiology of Solitary and Arribada Nesting Olive Ridley Sea Turtles during the Internesting 

Period.” General areas of specialization: chelonians, conservation, reproductive physiology and 

behavior. Academic Advisor: Dr. David W. Owens 

B.A., 1989. Major Biology, Minor Chemistry, Wittenberg University, Springfield, OH. 

Positions Held 

Assistant Professor, Dept. of Natural Sciences and Mathematics, West Liberty University, Wheeling, 

WV 26074. Aug. 2010 - current 

Assistant Professor (temp.), Dept. of Biology, Georgia Southern University, Statesboro, GA 30460. 

Aug. 2008 - 2010 

Assistant Professor, Dept. of Biology, University of Evansville, Evansville, IN 47722. 

Aug. 2003 - May 2008 

Assistant Professor (temp.), Dept. of Biology, Arkansas State Univ., State University, AR 72467. 

Aug. 2002 - May 2003 

Lecturer, Dept. of Biology, West Chester University, West Chester, PA 19383. 

Aug. 2000-May 2002 

Teaching Assistant, Dept. of Biology, Texas A&M University, College Station, TX 77845. 

1989-92, 1994-99. Responsibilities: teach labs, write/grade quizzes & exams, hold office hours. 

Course Director / Assistant Lecturer for “Advanced Sea Turtle Biology” course. Jan. 1998. 

Méxican Sea Turtle Center in Mazunte, Oaxaca, México. 

Primary instructors: D. Owens (Dept. of Biology, Texas A. & M. Univ.), J. Flanagan 

(Veterinarian, Houston Zoo), R. Marquez (National Coordinator, Sea Turtle Research, Méxican 

National Fisheries Institute) 

Students: 15 Méxican/Cuban government researchers, veterinarians, and students. 

Range of topics: reproductive physiology & behavior, disease, and life history and hands-on 

training with laparoscopy, ultrasonography, blood sampling, and radio-telemetry. 

Assistant Lecturer/Organizer for “Reproductive Physiology of Sea Turtles” course. 

2-week course at Rancho Nuevo, México. May 1996. 

Courses Taught (locations where the course was taught are in parenthesis) 

Intro level courses, Majors 

• Animal Diversity/Introductory Zoology, lecture and lab (UE, ASU, WCU) 

• Biology 1 lab (GSU, UE, TAMU) 

• Biology 2 lab (GSU, TAMU) 

• Scientific Communications (UE) 

Upper level courses, Majors 

• Comparative Animal Physiology lecture and lab (GSU, UE, WLU) 

1

• Comparative Vertebrate Anatomy, lecture and lab (WCU, TAMU) 

• Animal Behavior, lecture (UE, WLU) 

• Vertebrate Zoology, lecture and lab (UE, WLU) 

• Conservation Biology, lecture (WCU) 

• Vertebrate Ecology, lecture and lab (WCU) 

• Undergraduate research (individual student) (GSU, UE) 

Biology courses for (usually) non-majors 

• Human Anatomy and Physiology 1, lecture and lab (GSU, WCU) 

• Human Anatomy & Physiology II, lecture and lab (WCU) 

• Microbiology lecture (summer 2010) (GSU) 

• Microbiology lab (scheduled for fall 2010) (GSU) 

• General Biology, lecture and lab (GSU, UE, ASU, WLU) 

• Environmental Science, lecture (UE) 

Honors, Fellowships, Other Recognitions 

Affiliate status for the Graduate Faculty at Georgia Southern University. 2010. 

Clare Booth Luce Fellowship in Science and Engineering ($25,000/yr). 1992-1994. 

Outstanding Teaching Performance, Dept. of Biology, Texas A&M University. 1992. 

Alpha Lambda Delta, Honor Society. 1985. 

Wittenberg University Scholar (top 5% of incoming freshman). 1985-1989. 

Reviewed Book Chapter, Peer Reviewed Publications, and Professional Reports 

S. Morreale, P. Plotkin, D. Shaver, and H. Kalb. 2007. Adult Migration and Habitat Utilization. In 

Biology and Conservation of Ridley Turtles. P. Plotkin and S. Morreale, Editors. John Hopkins 

University Press. 

G. Zug, H. Kalb, S. Lazar. 1997. Age and growth in wild Kemp’s ridley sea turtles (Lepidochelys 

kempii) from skeletochronological data. Biological Conservation 80: 261-268. 

H. Kalb and G. Zug. 1990. Age estimates for a population of American toads, Bufo americanus 

(Salientia: Bufonidae), in northern Virginia. Brimleyana 16:79-86. 

H. Kalb. 1992. Reproductive Physiology of the Spotted Turtle, Clemmys guttata at the Prairie Road 

Fen, in Springfield Ohio. Final Report to the Ohio Dept. of Natural Resources. 

H. Kalb and L. Laux. 1990. A Population Study of Clemmys guttata at the Prairie Road Fen, in 

Springfield Ohio. Final Report to the Ohio Dept. of Natural Resources. 

Editor 

H. Kalb, A. Rohde*, K. Gayheart, and K. Shanker. 2008. Proceedings of the 25th Annual 

Symposium on Sea Turtle Biology and Conservation. NOAA Tech. Memo. 

H. Kalb and T. Wibbels. 2000. Proceedings of the 19th Annual Symposium on Sea Turtle Biology 

and Conservation. NOAA Tech. Memo. NMFS-SEFSC-443. pp. 291. 

H. Kalb. Turtle and Tortoise Newsletter. 2000-2005. Official newsletter of the IUCN/SSC 

Freshwater Turtle and Tortoise Specialist Group. Published by Chelonian Research Foundation. 

1 st Edition, Feb. 2000. Editorial Board: Anders Rhodin, Peter C.H. Pritchard, John Behler, and 

Russell Mittermeier. 

H. Kalb. 1994-1999. Box Turtle Research and Conservation Newsletter. Initial funding: Savannah 

River Ecology Lab, later: Chelonian Research Foundation. 

*Names in bold are undergraduate students who were working directly with me. 

2

Grants and Internships 

Faculty Development Grant for travel to the Society for Integrative and Comparative Biology’s 

Annual Symposium in Seattle, WA. $1024. January 2010. 

The Effects of Incubation Temperatures on Embryonic Development and Post-hatching Morphology 

and Behavior in Malayan Box Turtles (Cuora amboinensis). Summer 2006. Funding by 

University of Evansville Undergraduate Research Program and Honor’s Program. Students: 

Alison Rohde, Katie Aldred, and Natalie Byars. 

Management of the Cuora amboinensis Taxon Management Group through Genetic Identification 

of Captive Stock. Spring 2006. $1,735. University of Evansville’s Undergraduate Research 

Program. Student: Sasha Rohde. 

Continued Support for the University of Evansville Captive Breeding Colonies of Asian Turtles. 

Spring 2005. $1,359. Univ. of Evansville Alumni Research and Scholarly Activity Fellowship. 

Subspecies Identification of Individuals in a Captive Colony of Malayan Box Turtles, Cuora 

amboinensis. Summer 2005. Funding Univ. of Evansville Honor’s Program. Student: Andrea 

Eyler. 

Treatment of Parasites in Malayan Box Turtles, Cuora amboinensis. Summer 2005. $9,810. 

Funding Univ. of Evansville Undergraduate Research Program. Student: Bozorgmehr Ouranos. 

Ultrasound Technology in the Research Lab and Classroom. 2004. $2,500. U.E. Arts, Research and 

Teaching Projects Grant. 

Maintenance and Reproduction in Two Asian Turtle Assurance Colonies. Fall 2003, Spring 2004. 

Total $5,330. University of Evansville’s Alumni Research and Scholarly Activity Fellowship. 

Behavior of the Olive Ridley in the Reproductive Patch. 1993. National Geographic Society. David 

Owens grantee. 

Reproductive Physiology of Clemmys guttata (Spotted Turtle). Grantee and Primary Investigator. 

1991-1992. Ohio Dept. of Natural Resources, Division of Parks and Recreation. 

Life History Study of Clemmys guttata. Primary Investigator. 1989. 

Ohio Dept. of Natural Resources, Division of Parks and Recreation. 

Vertebrate Zoology Internship, Smithsonian Institution, Washington, D.C. 1988. Project: 

Skeletochronological Age Estimates on the American Toad and the Kemp’s Ridley Sea Turtle. 

Travel Grants (2 @ $500) from Dept. of Biology, Texas A&M Univ. 1995 and 1997. To attend the 

77th Annual Meeting of Herpetologists’ League/SSAR and 15 th Annual Sea Turtle Symposium. 

Travel Grant ($500) to 2 nd International Congress on Chelonian Conservation. From Congress 

organizers. 1995. 

Research Presentations 

T. Hayes and H. Kalb. 2010. Visual Stages of Egg Development in the Malayan box turtle (Cuora 

amboinensis) as Observed with Ultrasound Technology. Annual Conference of the Society for 

Integrative and Comparative Biology, Seattle WA. (Poster presentation) 

N. Byars, A. Rohde, K. Aldred, and H. Kalb. 2007. Effects of Incubation Temperature on 

Incubation Duration and Hatchling Fitness in Malayan Box Turtles (Cuora amboinensis). 21 st 

National Conference on Undergraduate Research, California. Apr. 12-14. (Poster presentation) 

H. Kalb, N. Byars, and K. Aldred. 2006. Observations on Reproduction in a Captive Colony of 

Malayan Box Turtles, Cuora amboinensis. 4 th Annual Symposium on Conservation and Biology 

of Freshwater Turtles and Tortoises. St. Louis, Mo. Aug 10-13. (Poster presentation) 

A. Rohde, B. Ouranos, S. Patton and H. Kalb. 2006. Parasites Present in a Stable Breeding 

Population of Malayan Box Turtles (Cuora amboinensis). 4 th Annual Symposium on 

Conservation and Biology of Freshwater Turtles and Tortoises. St. Louis, Mo. Aug 10-13. 

(Poster presentation) 

3

B. Ouranos, C. Bursey, and H. Kalb. 2005. Preliminary Parasite Results in a Captive Colony of 

Malayan Box Turtles (Cuora amboinensis). Univ. of Evansville Fall Research Symposium. 

(Poster presentation) 

A. Eyler, A. Rohde, Y. Hsiang-Jui, and H. Kalb. 2005. Obtaining Blood Samples and Sequence 

from Cuora amboinensis: Preliminary Studies for Identifying Subspecies of a Local Collection. 

University of Evansville Fall Research Symposium. (Poster presentation) 

B. Hart, J. Legout, H. Kalb and M. Davis. 2005. Identification and Antibiotic Sensitivity Testing of 

Bacteria Infecting Threatened Asian Freshwater Turtles. 19 th National Conference on 

Undergraduate Research, Lexington, VA. Apr. 21-23. (Poster presentation) 

H. Kalb. 2005. Preliminary Data on Reproduction in Malayan Box Turtles (Cuora amboinensis). 25 th 

Annual Sea Turtle Symposium, Savannah GA. (Oral presentation) 

H. Kalb. 2004. Female Reproductive Physiology: a Review, Techniques, and Applications. Turtle 

Survival Alliance Symposium, Orlando FL. (Oral presentation) 

H. Kalb and D. Owens. 1997. The Olive Ridley Aggregation at Playa Nancite, Costa Rica. 77 th 

Annual Meeting of Herpetologists’ League/Society for the Study of Amphibian and Reptiles. 

Seattle, WA. (Oral presentation) 

H. Kalb and D. Owens. 1995. Internesting Movements and Conservation Concerns of the Olive 

Ridley Sea Turtle during the Reproductive Season at Nancite, Costa Rica. International Congress 

of Chelonian Conservation, Gonfaron, France. (Oral presentation) 

H. Kalb and D. Owens. 1995. Nancite to Ostional: Post-mating Movements of Female Olive Ridley 

Sea Turtles. 15th Annual Sea Turtle Symposium, Hilton Head, SC. (Oral presentation) 

H. Kalb, J. Kureen, P. Mayor, J. Peskin, and R. Phyliky. 1995. Conservation Concerns for the 

Nancite Olive Ridleys. 15 th Annual Sea Turtle Symposium, Hilton Head, SC. NOAA Tech. 

Memo. NMFS-SEFSC-387:141-142. (Poster presentation) 

H. Kalb. 1994. Reproductive Evaluation of Clemmys guttata, the Spotted Turtle. 74 th Annual 

Meeting of Herpetologists’ League/Society for the Study of Amphibian and Reptiles. Athens, 

GA. (Oral presentation) 

H. Kalb and D. Owens. 1994. Differences between Solitary and Arribada Nesting Olive Ridley 

Females during the Internesting Period. 14 th Annual Sea Turtle Symposium, Hilton Head, SC. 

NOAA Tech. Memo. NMFS-SEFSC-351:68. (Oral presentation) 

H. Kalb and D. Owens.1993. Arribada versus Solitary Nesters: Comparison of Internesting 

Behavior Patterns in Olive Ridley Sea Turtles, Lepidochelys olivacea. 2 nd World Congress of 

Herpetology, Adelaide, Australia. (Oral presentation) 

H. Kalb, R. Valverde, and D. Owens. 1992. What is the Reproductive Patch of the Olive Ridley Sea 

Turtle at Playa Nancite, Costa Rica? 12 th Annual Sea Turtle Symposium, Jekyll Island, GA. 

NOAA Tech. Memo. NMFS-SEFSC-361:57-60. (Oral presentation) 

L. Laux, C. Stanton, and H. Kalb. 1991. Spatial Relationship among a Restricted Spotted Turtle, 

Clemmys guttata, Population in a Small Prairie Fen. Ecological Society of America Annual 

Meeting, San Antonio, TX. (Poster presentation) 

D. Rostal, H. Kalb, J. Grumbles, P. Plotkin, and D. Owens. 1991. Application of Ultrasonography to 

Sea Turtle Reproduction. 11 th Annual Sea Turtle Symposium, Jekyll Island, GA. NOAA Tech. 

Memo. NMFS-SEFSC-302:181. (Poster presentation) 

H. Kalb. 1990. A Population Study of Clemmys guttata at the Prairie Road Fen, in Springfield, 

Ohio. 70 th Annual Meeting of Herpetologists’ League/SSAR, New Orleans, LA. (Poster 

presentation) 

G. Zug and H. Kalb. 1989. Skeletochronological Age Estimates for Juvenile Lepidochelys kempii 

from Atlantic Coast of North America. 9 th Annual Sea Turtle Symposium Jekyll Island, GA. 

NOAA Tech. Memo. NMFS-SEFSC-232:271-273. (Poster presentation) 

4

Invited Speaker 

The Asian Turtle Crisis and the UE Turtle Program. 2005. Hoosier Herpetological Society. 

Indianapolis, IN. 

The Asian Turtle Crisis. 2004. University of Southern Indiana, Dept. Biology Spring Seminar Series. 

Turtles. 2003. Women in Technology and Science Workshop for 6 th grade girls. Jonesboro, AR. 

Olive Ridley Sea Turtles of Playa Nancite, Costa Rica. 2001. Richard Stockton College Biology 

Seminar Series 

Olive Ridley Sea Turtles of Playa Nancite, Costa Rica. 2001. New York Turtle & Tortoise Seminar. 

Box Turtles in the Pet Trade and Sea Turtle Natural History and Conservation. 1997. Dept. of 

Recreational Sports, 1 st Annual Jamboree, T.A.M.U, College Station, TX. 

Box Turtles: Past, Present, and Future. 1997. Rio Brazos Audubon Society. 

Costa Rican Turtle Research & Conservation Implications. 1995. Society for Conservation Biology. 

Sea Turtle Natural History & Conservation. 1991. Texas Environmental Action Coalition 

Conference. 

Scientific American Frontiers TV show. 1991. 10 min. on my chemosensory imprinting research in 

Kemp’s ridleys. 

University Service Work 

University of Evansville, committee work 

Interdisciplinary Studies Committee, Chair 

Admissions and Standards Committee 

Biology library liaison 

Phi Eta Sigma (freshman honor’s society) advisor 

University of Evansville Turtle Program: Tours and Turtle Conservation Talks 

Fall, 2004 & 2005: Scott School. 

Spring, 2005: Memorial High School Environmental Science Classes. Contact Maryann Watson. 

Spring, 2004 & 2005: Luce Elementary School. Contact Pat Keith. 

University of Evansville Turtle Program Open House and Fund Raiser. 

Homecoming Weekend, 2004, 2005, 2006 

Biology representative. United Way Drive, Fall 2004. 

Community Service Work 

Babysat for parents attending English as a second language classes. Statesboro, GA 2009. 

Indiana Master Naturalist Program, Wesselman Woods Nature Preserve. Lecture on Reptile biology 

and conservation. Feb., 2007 & 2008. 

UE Turtle Ambassadors, Maryann Watson’s Environmental Science Class at Memorial High School. 

Six hatchling Malayan box turtles on loan. 2004 - 2008. 

Summer Turtle Classes with E-Academy. 

7 th -12 th graders at U.E. Two weeks, June 2005. 

1 st -3 rd graders at Evansville Day School. Two weeks, June 2004 

Turtle display at Reptile Invasion. Wesselman Woods Nature Preserve. 

June 14-15, 2008. 

June 11-12, 2005 with students Bo and Gollsheed Ouranos. 

June 12-13, 2004 with students Josh Yeager and Amanda Nelson. 

Turtle presentations at public schools. 

2008. Mater Dei summer program. Contact Shelly McFall. 

5

2006. Holy Redeemer Day Camp. Contact Becky Smither. 

2006. Chandler Elementary School. 5 th grade honor’s class. Contact Mrs. Strahle. 

2006. Evansville Day School. Middle School. Contact Mary Ann Kraft 

2004: 1 presentation. 3rd graders. Contact Lisa Oldham. 

2003: 3 presentations. Parkview Jr. High School (Lawrenceville, IL). Contact Joan Brian. 

2003: 3 presentations. Sharon Elementary School. 1st & 6th grade. Contact Carol Stalker. 

2003: 2 presentations. Evansville Day School. 1st graders. Contact Brooke Fuchs. 

Professional Society Memberships 

IUCN/SSC Tortoise and Freshwater Turtle Specialist Group 

Society for Integrative and Comparative Biology 

Turtle Survival Alliance 

Professional Volunteer Work 

Volunteer Coordinator. 25 th Annual Sea Turtle Symposium, Philadelphia, PA. 2005. 

Judge (student competition). 22nd Annual Sea Turtle Symposium, Miami, FL. 2002. 

Volunteer Chairman. 21 th Annual Sea Turtle Symposium, Philadelphia, PA. 2001. 

Program Co-chair. 19 th Annual Sea Turtle Symposium, South Padre Island, TX. 1999. 

Session Chair. 18 th and 19 th Annual Sea Turtle Symposium, 1998, 1999. 

Special Course Work and Skills 

Reading Roundtables, Georgia Southern University, Center for Teaching Excellence. 2009. 

Techniques in Molecular Biology. Biotechnology Institute, Penn. State University. 2002. 

College Teaching (graduate level course), Dept. of Education, Texas A&M University. 1996. 

Teacher Enhancement Workshops for Biology Lab Instructors. Dept. Biol., TAMU. 1989. 

Marine Biology and Oceanography Exchange Program, Duke Marine Lab, Beaufort, NC. 1988. 

6

Molecular Ecology (2007) 16, 

17–18 doi: 10.1111/j.1365-294X.2006.03252.x 

Blackwell Publishing Ltd 

NEWS AND VIEWS 

PERSPECTIVE ARTICLE 

Whose turtles are they, anyway? 

JEANNE A. MORTIMER, *† PETER A. MEYLAN‡ 

and MARYDELE DONNELLY§ 

* Department of Zoology, University of Florida, Gainesville, Florida 32611, USA, † Island Conservation Society, Victoria, Mahe, 

Seychelles, ‡ Natural Sciences, Eckerd College, St. Petersburg, Florida 33711, USA, § Caribbean Conservation Corporation, Gainesville, 

Florida 32609, USA 

Abstract 

The hawksbill turtle ( Eretmochelys imbricata), 

listed since 1996 by the IUCN as Critically 

Endangered and by the Convention on International Trade in Endangered Species (CITES) 

as an Appendix I species, has been the subject of attention and controversy during the past 

10 years due to the efforts of some nations to re-open banned international trade. The most 

recent debate has centred on whether it is appropriate for Cuba to harvest hawksbills from 

shared foraging aggregations within her national waters. In this issue of Molecular Ecology, 

Bowen et al. 

have used molecular genetic data to show that such harvests are likely to have 

deleterious effects on the health of hawksbill populations throughout the Caribbean. 

Hawksbill trade involves ‘tortoiseshell’, the translucent 

scales covering the hawksbill plastron and carapace, which 

has been considered a precious material on par with ivory 

and rhinoceros horn since antiquity (according to legend, 

Cleopatra bathed in a tub made of tortoiseshell). Efforts 

to scientifically manage this resource were, in the past, 

hobbled by ignorance about key aspects of the hawksbill’s 

life cycle, most notably delayed sexual maturity (20– 

30 years in the Caribbean and longer elsewhere) and the 

migratory nature of the species. Flipper tags, used in the 

context of much-reduced hawksbill populations and 

widely dispersed foraging habitats, revealed little about 

hawksbill migrations. Molecular genetics, however, have 

provided the technological breakthrough needed (Bass 

et al. 

1996). The study of Bowen et al. 

(2006) expands on that 

earlier work adding significantly to our understanding of 

the migrations of immature hawksbills. The authors use 

proven molecular techniques to examine the nesting beach 

origins of hawksbills on eight foraging grounds, four from 

previous literature and four newly sampled. The feeding 

grounds studied span the tropical West Atlantic from 

southern Texas to the US Virgin Islands, and include 

Inagua in the Bahamas and a site on the south coast of the 

Dominican Republic. 

The authors report that populations from 8 of 10 Caribbean 

nesting beaches studied are sufficiently distinct that 

their contribution to feeding aggregations can be estimated. 

The feeding aggregations show less genetic differentiation 

than nesting beaches but still exhibit significant differences. 

© 2006 The Authors 

Journal compilation © 2006 Blackwell Publishing Ltd 

Both maximum-likelihood and Bayesian mixed-stock analyses 

are used and yield similar results. Each of the feeding 

grounds (except Texas, which is the only sample consisting 

of pelagic-phase turtles) has significant contributions from 

multiple nesting beaches. Further analysis of the Bayesian 

results reveals strong relationships between feeding grounds 

and nesting beach populations: a direct relationship with 

nesting population size and an inverse relationship with 

distance between nesting and feeding sites. The management 

question that these authors ultimately address is how 

harvest of this species in one nation might affect populations 

elsewhere. Their mixed-stock analysis strongly corroborates 

evidence from tag returns, satellite tracking and 

previous genetic study, that harvests in any part of the 

Caribbean impact the species throughout the region. 

These results have important implications for conservation 

and for CITES. During 1970–92, Japan imported 

∼405 

178 kg of ‘bekko’ (tortoiseshell) from 25 countries in 

Atlantic Latin America and the Caribbean (Milliken & 

Tokunaga 1987; Japanese Trade Statistics). This is equivalent 

to some 302 371 Caribbean hawksbill turtles (1.34 kg/ 

turtle). By the mid-1980s many countries had acceded to 

CITES and stopped exporting shell, but Japan took a CITES 

reservation or exception on hawksbills, and continued to 

import shell until 1992 when international pressure forced 

her to drop the reservation and stop importing bekko. During 

those 22 years, Cuba harvested about 5000 turtles 

annually on their foraging grounds, contributing ∼33% 

of 

the total shell imports from the region (Carrillo et al. 

1999).

18 NEWS AND VIEWS 

By 1995, in response to the Japanese cessation of trade, 

Cuba reduced its annual official harvest to less than 500 

large turtles (Carrillo et al. 

1999), a level that continues to 

the present day. Since 1993, Cuba has stockpiled the shell 

from the harvest in the hope of eventually being able to sell 

it to Japan. 

In 1997 and 2000, Cuba’s interest in re-opening trade for 

‘Cuban hawksbills’ was presented to the biennial meeting 

of CITES. Cuba initially argued that hawksbills found in 

its waters were nonmigratory, part of a closed system and 

sought the rights to harvest 500 animals a year into perpetuity 

for the international trade and to sell off the stockpile 

of raw shell accumulated since 1993. Although these proposals 

were rejected, Cuba maintained an annual harvest 

of 500 or fewer large turtles. In early 2000 the stockpile was 

6900 kg (Cuban CITES proposal, 2000); since that time it 

has been increased by at ∼450 

turtles a year and is now 

estimated at ∼11 

200 kg of shell, representing some 7079 

Cuban-harvested turtles (1.59 kg/turtle). 

Meanwhile, Caribbean hawksbill populations are 

seriously depleted from their historic levels, largely as a 

result of centuries of trade; many populations in the region 

continue to decline (Mortimer & Donnelly, in press). From 

the 1970s onward, increasing numbers of Caribbean countries 

have enacted legislation that protects hawksbills on 

their beaches and in their waters. At some sites protective 

measures appear to have halted the decline of depleted populations 

and nesting numbers have stabilized. Remarkably, 

since the early 1990s, several such nesting populations 

increased significantly. These increases coincide with the 

90% decrease in the Cuban hawksbill fishery since 1994, a 

period during which more than 55 000 large hawksbills 

were spared from slaughter. This is significant given that 

fewer than 5000 female hawksbills are estimated to nest 

annually in the Caribbean region (Meylan & Donnelly 

1999; Mortimer & Donnelly, in press). The implications of 

the paper by Bowen et al. 

are that harvest of hawksbills 

from any nesting beach could impact multiple foreign 

feeding grounds, and that harvest on any feeding grounds 

could impact the nesting beach populations at multiple 

sites. Thus, any nation that opens or promotes harvest 

could be undermining badly needed efforts to conserve the 

species at other sites. 

There is more at stake than turtles. Hawksbills are spongivores 

(Leon & Bjorndal 2002) and spongivory helps to 

maintain healthy coral reefs by releasing corals from competition 

with sponges (Bjorndal & Jackson 2003). Historic 

consumption of sponges by hawksbill turtles is estimated 

to have been 800 times higher than it is now (McClenachan 

et al. 

2006). At a time when coral reefs are among the most 

endangered ecosystems on the planet (Wilkinson 2000), 

successful conservation and management of hawksbills 

may be an essential component for ecosystem restoration. 

References 

Bass AL, Good DA, Bjorndal KA et al. (1996) Testing models of 

female reproductive migratory behavior and population structure 

in the Caribbean hawksbill turtle, Eretmochelys imbricata, 

with mtDNA sequences. Molecular Ecology, 

5, 


Bjorndal KA, Jackson JBC (2003) Role of sea turtles in marine ecosystems 

— reconstructing the past. In: Biology of Sea Turtles (eds 

Lutz PL, Musick JA, Wyneken J), Vol. II, pp. 259–273. CRC Press, 

Boca Raton, Florida. 

Bowen BW, Grant WS, Hillis-Starr Z et al. (2006) Mixed-stock 

analysis reveals the migrations of juvenile hawksbill turtles 

( Eretmochelys imbricata) 

in the Caribbean Sea. Molecular Ecology, 

doi:10.1111/j.1365-294X.2006.03096.x. 

Carrillo CE, Webb GJW, Manolis SC (1999) Hawksbill turtles 

( Eretmochelys imbricata) 

in Cuba: an assessment of the historical 

harvest and its impacts. Chelonian Conservation and Biology, 

3, 


Leon YM, Bjorndal KA (2002) Selective feeding in the hawksbill 

turtle, an important predator in coral reef ecosystems. Marine 

Ecology Progress Series, 

245, 


McClenachan L, Jackson JBC, Newman MJH (2006) Conservation 

implications of historic sea turtle nesting beach loss. Front Ecological 

Environment, 

4, 


Meylan AB, Donnelly M (1999) Status justification for listing the 

hawksbill turtle ( Eretmochelys imbricata) 

as critically endangered 

on the 1996 IUCN Red List of Threatened Animals. Chelonian 

Conservation and Biology, 

3, 

177–184. 

Milliken T, Tokunaga H (1987) The Japanese sea turtle trade 

1970–86. A Special Report Prepared by TRAFFIC (Japan) . Center 

for Environmental Education, Washington D.C. 

Mortimer JA, Donnelly M (in press)). IUCN 2006 Global Assessment 

for the Hawksbill Turtle (Eretmochelys imbricata) . 

Wilkinson CR (2000) Status of Coral Reefs of the World: 2000. 

Global 

Coral Reef Monitoring Network. 

Australian Institute of Marine 

Science. 

© 2006 The Authors 

Journal compilation © 2006 Blackwell Publishing Ltd

Molecular Ecology (2009) 18, 4841–4853 doi: 10.1111/j.1365-294X.2009.04403.x 

Turtle groups or turtle soup: dispersal patterns of 

hawksbill turtles in the Caribbean 

J. M. BLUMENTHAL,*† F. A. ABREU-GROBOIS,‡ T. J. AUSTIN,* A. C. BRODERICK,† 

M. W. BRUFORD,§ M. S. COYNE,†– G. EBANKS-PETRIE,* A. FORMIA,§ P. A. MEYLAN,** 

A. B. MEYLAN†† and B. J. GODLEY† 

*Department of Environment, Box 486, Grand Cayman KY1-1106, Cayman Islands, †Centre for Ecology and Conservation, 

School of Biosciences, University of Exeter Cornwall Campus, Penryn TR10 9EZ, UK, ‡Laboratorio de Genética, Unidad 

Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Mazatlán, Sinaloa 82040, México, §Biodiversity and 

Ecological Processes Research Group, School of Biosciences, Cardiff University, Cardiff CF10 3TL, UK, –SEATURTLE.ORG, 

Durham, NC 27705, USA, **Natural Sciences, Eckerd College, St Petersburg, FL 33711, USA, ††Florida Fish and Wildlife 

Conservation Commission, Fish and Wildlife Research Institute, St Petersburg, FL 33701, USA 

Introduction 

Abstract 

Despite intense interest in conservation of marine turtles, spatial ecology during the 

oceanic juvenile phase remains relatively unknown. Here, we used mixed stock analysis 

and examination of oceanic drift to elucidate movements of hawksbill turtles (Eretmochelys 

imbricata) and address management implications within the Caribbean. Among 

samples collected from 92 neritic juvenile hawksbills in the Cayman Islands we detected 

11 mtDNA control region haplotypes. To estimate contributions to the aggregation, we 

performed ‘many-to-many’ mixed stock analysis, incorporating published hawksbill 

genetic and population data. The Cayman Islands aggregation represents a diverse mixed 

stock: potentially contributing source rookeries spanned the Caribbean basin, delineating 

a scale of recruitment of 200–2500 km. As hawksbills undergo an extended phase of 

oceanic dispersal, ocean currents may drive patterns of genetic diversity observed on 

foraging aggregations. Therefore, using high-resolution Aviso ocean current data, we 

modelled movement of particles representing passively drifting oceanic juvenile 

hawksbills. Putative distribution patterns varied markedly by origin: particles from 

many rookeries were broadly distributed across the region, while others would appear to 

become entrained in local gyres. Overall, we detected a significant correlation between 

genetic profiles of foraging aggregations and patterns of particle distribution produced 

by a hatchling drift model (Mantel test, r = 0.77, P < 0.001; linear regression, r = 0.83, 

P < 0.001). Our results indicate that although there is a high degree of mixing across the 

Caribbean (a ‘turtle soup’), current patterns play a substantial role in determining genetic 

structure of foraging aggregations (forming turtle groups). Thus, for marine turtles and 

other widely distributed marine species, integration of genetic and oceanographic data 

may enhance understanding of population connectivity and management requirements. 

Keywords: conservation genetics, hawksbill, marine turtle, migratory species, mixed stock, 

ocean currents 

Received 29 June 2009; revision received 21 September 2009; accepted 25 September 2009 

Many marine vertebrates have life cycles that span wide 

spatiotemporal scales – complicating research and 

Correspondence: Brendan J. Godley, Fax: 44 (0) 1326 253638; 

E-mail: b.j.godley@exeter.ac.uk 

Ó 2009 Blackwell Publishing Ltd 

management. Recently, molecular techniques have provided 

insights into patterns of migration and stock resolution 

in species ranging from fish (Millar 1987) to 

porpoises (Andersen et al. 2001) and great whales 

(Baker et al. 1999; Witteveen et al. 2004). Such stock resolution 

issues are particularly important when species

4842 J. M. BLUMENTHAL ET AL. 

are commercially valuable, cross geopolitical boundaries 

or have been exploited to the point of endangerment. 

Marine turtles exemplify these concerns: a long history 

of commercial use has resulted in global declines 

(Baillie et al. 2004) and management of marine turtle 

populations is complex, as developmental and reproductive 

migrations may span the territorial waters of 

several nations and the high seas (Bowen et al. 1995; 

Bolten et al. 1998). 

Like many other marine organisms (Mora & Sale 

2002) most marine turtle species experience a phase of 

oceanic dispersal, which in marine turtles is known as 

the ‘lost year’ or ‘lost years’ (Carr 1987). This extended 

period of drifting in concert with initially small size 

and high mortality inhibits tracking movements of neonates 

from the time of entry into marine habitat off 

natal beaches to the time of recruitment into neritic foraging 

grounds (Bolten et al. 1998; Lahanas et al. 1998; 

Engstrom et al. 2002; Bowen et al. 2004; Luke et al. 

2004). Although foraging grounds are typically inhabited 

by individuals originating from multiple nesting 

beaches a behavioural barrier to genetic mixing at nesting 

beaches is maintained: generations of mature 

females return to their natal regions to reproduce (Meylan 

et al. 1990). This ‘natal homing’ leads to genetic differentiation 

at mitochondrial loci of nesting populations 

over time (hawksbills Eretmochelys imbricata: Broderick 

et al. 1994; Bass et al. 1996; loggerheads Caretta caretta: 

Encalada et al. 1998; Engstrom et al. 2002; green turtles 

Chelonia mydas: Meylan et al. 1990; Allard et al. 1994). 

Therefore, mitochondrial DNA haplotypes and haplotype 

frequencies characteristic of each region serve as 

a form of ‘genetic tag,’ linking juveniles in mixed 

aggregations with their specific nesting beach origins 

(Norman et al. 1994). 

In a method originally developed to resolve the origins 

of salmon stocks (Millar 1987), estimates of marine 

turtle origin can be made using a maximum likelihood 

(Pella & Milner 1987) or Bayesian (Pella & Masuda 

2001) mixed stock analysis (MSA), where haplotype frequencies 

for genetically mixed aggregations are compared 

with potential source populations. MSA has 

recently proven valuable in elucidating migratory patterns 

and range states in hawksbill (Bowen et al. 1996, 

2007a; Bass 1999; Diaz-Fernandez et al. 1999; Troëng 

et al. 2005; Velez-Zuazo et al. 2008), loggerhead (Bowen 

et al. 1995; Laurent et al. 1998; Engstrom et al. 2002; 

Maffucci et al. 2006) and green turtles (Lahanas et al. 

1998; Luke et al. 2004). While mixed stock analysis has 

traditionally been used to estimate contributions of 

many potential source rookeries to a single foraging 

ground (‘many-to-one’ analysis), a new approach has 

recently been developed which more realistically estimates 

the contributions of many rookeries to many for- 

aging grounds within a metapopulation context (‘manyto-many’ 

analysis; Bolker et al. 2007). Caribbean hawksbills 

represent ideal candidates for many-to-many 

analysis: rookeries are sufficiently differentiated (Bass 

et al. 1996), populations may be relatively contained in 

the Caribbean region (Bowen et al. 1996) and data from 

multiple mixed stocks have recently been published 

(Bowen et al. 2007a; Velez-Zuazo et al. 2008). 

Tagging and satellite tracking have demonstrated 

that hawksbill developmental and reproductive migrations 

span the territorial waters of multiple jurisdictions 

(Meylan 1999; Horrocks et al. 2001; Troëng et al. 

2005; Whiting & Koch 2006; van Dam et al. 2008) and 

genetic research is beginning to elucidate links 

between nesting beaches and foraging grounds (Bowen 

et al. 1996, 2007a; Bass 1999; Diaz-Fernandez et al. 

1999; Troëng et al. 2005; Velez-Zuazo et al. 2008). It 

has also been determined that Caribbean hawksbill 

foraging aggregations show shallow but significant 

genetic structure (Bowen et al. 2007a). As in green turtles 

(Bass et al. 2006), this suggests that rather than the 

oceanic phase being a homogeneous mixture (the ‘turtle 

soup’ model: Engstrom et al. 2002), dispersal is 

non-random. However for many populations links 

between nesting beaches and foraging areas have not 

been identified (Bowen et al. 1996) and little is known 

regarding movements of oceanic juveniles during the 

lost year or years (Musick & Limpus 1997; Bolten 

2003) and factors which drive dispersal during this 

phase (Bowen et al. 2007a). 

In previous genetic studies of green (Lahanas et al. 

1998; Bass & Witzell 2000; Luke et al. 2004) and loggerhead 

turtles (Engstrom et al. 2002; Reece et al. 2006) 

source population size and geographic distance have 

proven inconsistent in determining recruitment from 

rookeries to foraging grounds. For Caribbean hawksbills, 

these factors were significantly correlated with foraging 

aggregation genetic composition, but correlations 

were weak and significant only for a small proportion 

of individual foraging grounds (Bowen et al. 2007a). 

Ocean currents have been postulated as playing a major 

role in distribution of oceanic juvenile marine turtles 

(Carr 1987) and recent studies have linked genetic composition 

of marine turtle foraging aggregations to ocean 

current patterns (Luke et al. 2004; Okuyama & Bolker 

2005; Bass et al. 2006; Carreras et al. 2006). However, 

for hawksbills, attempts to account for the role of ocean 

currents through incorporation of a current correction 

factor (increasing or decreasing geographic distances in 

a regression model by 10–20%) did not increase the 

strength of correlations (Bowen et al. 2007a). 

To evaluate population connectivity for marine organisms, 

empirical data must be linked with biophysical 

modelling of oceanic dispersal (Botsford et al. 2009). 

Ó 2009 Blackwell Publishing Ltd

Generalized ocean current diagrams can aid in consideration 

of the role of ocean currents in marine turtle 

dispersal (Bass et al. 2006; Carreras et al. 2006; Bowen 

et al. 2007a) but this method falls short when current 

patterns are complex. Trans-Atlantic drift has been 

modelled for oceanic juvenile loggerheads (Hays & 

Marsh 1997) and the availability of high-resolution 

ocean current data for the Caribbean and other regions 

now opens up the possibility of modelling dispersal of 

oceanic juvenile hawksbills in dynamic ocean currents. 

In this study, characterization of stock composition at 

the Cayman Islands hawksbill foraging site was 

extended by development of a hatchling drift model 

incorporating source population sizes and regional 

ocean current data to answer fundamental questions of 

hawksbill ecology: (i) how are oceanic juvenile hawksbills 

distributed during the lost year or years? (ii) how 

are foraging stocks geographically structured or regionally 

mixed? (iii) what role might ocean currents play in 

determining these patterns? 


Study area 

The Cayman Islands are located in the Caribbean Sea, 

approximately 240 km south of Cuba (Fig. 1). The 

three low-lying islands are exposed peaks on the 

Cayman Ridge formation, with nearly vertical slopes 

extending to depths in excess of 2000 m on all sides 

(Roberts 1994). Hawksbill nesting, while described as 

abundant in historical records (Lewis 1940), appears to 

have been largely extirpated in recent decades (Bell 

et al. 2007). However, the islands host foraging aggregations 

of neritic juvenile hawksbill turtles, inhabiting 

colonized pavement, coral reef and reef wall habitats 

(Blumenthal et al. 2009a, b). For this study, two sampling 

sites were selected: Bloody Bay, Little Cayman 

(19.7°N, 81.1°W) and western Grand Cayman (19.3°N, 

81.4°W). 

Capture and sampling 

Juvenile hawksbills (20–60 cm straight carapace length) 

were hand-captured in neritic foraging habitat and flipper 

and PIT tagged according to standard protocols 

(Blumenthal et al. 2009b) to prevent repeated sampling 

of individuals. Genetic sampling for this study was 

undertaken year-round between 2000 and 2003. Skin 

biopsies were obtained from a rear flipper with a sterile 

4 mm biopsy punch and preserved in a solution of 20% 

DMSO saturated with NaCl (Dutton 1996). Blood samples 

were collected from the dorsal cervical sinus 

(Owens & Ruiz 1980) and preserved in lysis buffer 


HAWKSBILL TURTLE DISPERSAL 4843 

Fig. 1 Distribution of hawksbill aggregations studied in the 

Caribbean region. Circles represent locations of Caribbean 

hawksbill rookeries: filled circles are genetically characterized. 

Haplotype frequency data from Antigua, Barbados, Belize, 

Costa Rica, Cuba, Mexico, Puerto Rico and the US Virgin 

Islands were used in many-to-many mixed stock analysis; 

rookeries in Venezuela are presently insufficiently characterized 

to permit inclusion. Triangles represent genetically characterized 

hawksbill foraging grounds also incorporated in mixed 

stock analysis: Bahamas, Cayman, Cuba, Dominican Republic, 

Mexico, Puerto Rico, Texas and the US Virgin Islands. Marine 

ecoregions (1) Gulf of Mexico (2) western Caribbean (3) southwestern 

Caribbean (4) Greater Antilles (5) southern Caribbean 

(6) eastern Caribbean (7) Bahamian. Source of published 

genetic data: Antigua (Bass 1999), Barbados (Browne et al. in 

press), Belize (Bass 1999), Cuba (Diaz-Fernandez et al. 1999), 

Mexico (Bass 1999; Diaz-Fernandez et al. 1999), USVI (Bass 

1999; Bowen et al. 2007a), Costa Rica (Troëng et al. 2005; 

Bowen et al. 2007a) and Puerto Rico (Diaz-Fernandez et al. 

1999; Velez-Zuazo et al. 2008). 

(100mM Tris-HCl, pH 8, 100mM EDTA, pH 8, 10mM 

NaCl and 1–2% SDS: Dutton 1996). 

Molecular analysis 

Following overnight digestion at 55 °C with proteinase 

K, DNA extraction was conducted via standard phenol 

chloroform extraction (Milligan 1998), Qiagen DNEasy 

tissue kit, or a modification of a protocol by Allen et al. 

(1998) (Formia et al. 2006, 2007). Fragments of 486 or 

550 base pairs (bp) were amplified via polymerase 

chain reaction (PCR), using primer pairs TCR6 (Norman 

et al. 1994) ⁄ L15926 (Kocher et al. 1989) or LTEi3 ⁄ HDEi1 

(LTEi3 5¢-CCTAGAATAATCAAAAGAGAAGG-3¢; 

HDEi1 5¢- AGTTTCGTTAATTCGGCAG-3¢; Abreu-Grobois 

et al. 2006) respectively. PCR reactions [PCR 

Ready-To-Go Beads (Amersham) or 1.5 mM MgCl2, 1· 

PCR buffer, 200 lM of each dNTP, 0.5 lM of each 

primer, 0.5 U Invitrogen Taq DNA polymerase, 1 lL


template DNA and sterile H2O to a volume of 10 lL) 

were carried out in a Perkin Elmer GeneAmp PCR 

system 9700 (3 min at 94 °C, 35 cycles of: 45 s at 

94 °C, 30 s at 55 °C and 1.5 min at 72 °C, followed by 

72 °C for 10 min; Formia et al. 2006). PCR products 

were cleaned with a Geneclean Turbo Kit (Qbiogene) 

or QIAquick spin columns (Qiagen), sequenced in 

both directions with a BigDye Terminator Cycle 

Sequencing Kit v. 2.0 (Applied Biosystems), purified 

via ethanol precipitation and run on an Applied Biosystems 

model 3100 automated DNA sequencer at 

Cardiff University, or analysed at the University of 

Florida Sequencing Core on an Amersham Pharmacia 

Biotech MegaBACE 1000 capillary array DNA 

sequencing unit. Negative controls (template-free PCR 

reactions) were utilized throughout to test for contamination. 

To identify haplotypes, sequences were aligned with 

published hawksbill mtDNA sequences (Bass et al. 

1996; Bowen et al. 1996; Bass 1999; Diaz-Fernandez 

et al. 1999; Troëng et al. 2005; Bowen et al. 2007a; 

Velez-Zuazo et al. 2008; Browne et. al. in press) in Sequencher 

2.1.2 (Gene Codes Corp). Haplotype diversity 

(h), nucleotide diversity (p, and population pairwise 

FST values (10 000 permutations; Kimura 2-parameter 

model, a = 0.50) were calculated in Arlequin v. 3.11 

(Excoffier et al. 2005). 

Mixed stock analysis 

Weighted and unweighted many-to-many analyses (Bolker 

et al. 2007) were also conducted, incorporating all 

previously published Caribbean hawksbill genetic data 

(haplotype frequencies: Antigua (Bass 1999), Barbados 

(Browne et al. in press; windward and leeward rookeries 

combined), Belize (Bass 1999), Cuba (Diaz-Fernandez 

et al. 1999; all foraging grounds combined), Mexico 

(Bass 1999; Diaz-Fernandez et al. 1999), USVI (Bass 

1999; Bowen et al. 2007a), Costa Rica (Troëng et al. 

2005; Bowen et al. 2007a) and Puerto Rico (Diaz-Fernandez 

et al. 1999; Velez-Zuazo et al. 2008). To enable comparison 

with previously published rookery haplotypes, 

sequences were truncated to 384 bp for analysis. Source 

population size (number of nests) was used as a strict 

constraint in the ‘weighted’ many-to-many model 

(Bolker et al. 2007), with population sizes taken from 

Mortimer & Donnelly (2007). 

Hatchling drift model 

Movement of particles was modelled using high resolution 

ocean current data from Aviso (Archiving, Validation 

and Interpretation of Satellite Oceanographic data, 

http://www.aviso.oceanobs.com). Aviso geostrophic 

velocity vector (GVV) data (maps of absolute geostrophic 

velocities derived from maps of Absolute 

Dynamic Topography combining all satellites, obtained 

from http://www.aviso.oceanobs.com) have a spatial 

resolution of 1 ⁄ 3 degree and a temporal resolution of 

1 day. To model the movement of passively drifting 

hawksbill hatchlings, post-hatchlings and oceanic juveniles, 

virtual particles were released from the coordinates 

of genetically characterized Caribbean hawksbill 

rookeries locations (Fig. 1). To simulate peak hatchling 

emergence, particles were released 60 days after the 

peak of the nesting season at each location (nesting season 

data: Chacón 2004; Garduño-Andrade 1999; Moncada 

et al. 1999), with one particle released per day over a 

60-day period and the resulting particle profiles 

weighted by source population size (taken from Mortimer 

& Donnelly 2007). Drift of virtual particles was initiated 

approximately 50 km offshore from each rookery to 

account for the phase of directed hatchling swimming 

that occurs prior to beginning passive drift (Hasbún 

2002; Chung et al. 2009a,b) and to bring particles into 

the area covered by Aviso data, as nearshore currents 

are too complex to map reliably. The u (eastward) and v 

(northward) ocean current vector components were sampled 

at the location of each particle from the daily GVV 

data file using a bilinear interpolation [Generic Mapping 

Tools (GMT 4.11; Wessel & Smith 1991)]. The u and v 

values (cm ⁄ s) were converted to m ⁄ day and the particle 

advected that distance in the x and y direction, respectively, 

and a new location obtained for that particle. Particles 

that left the GVV field (i.e. pushed towards the 

coastline) were removed from the model, as there is no 

information on how an oceanic juvenile hawksbill would 

behave in this situation. Also, while natural mortality 

during the hatchling, post-hatchling and oceanic juvenile 

phase is high, this factor was not incorporated into the 

model. One location per day was saved for each particle 

for analysis. All current modelling was carried out using 

custom perl scripts, the geod program, part of the 

PROJ.4 Cartographic Projections Library (http:// 

www.remotesensing.org/proj/) and the GMT package. 

Comparison of the hatchling drift model with mixed 

stock analysis 

To examine the possible influence of ocean currents on 

patterns of dispersal, we compared foraging aggregation 

genetic profiles (determined via many-to-many 

analysis) with patterns of particle distribution (particle 

profiles) produced by the hatchling drift model 

(Table 1). To produce particle profiles, we used the Global 

Maritime Boundaries Database (GMBD) to delineate 

Exclusive Economic Zones of nations containing genetically 

characterized hawksbill foraging aggregations. 


Table 1 Comparison of genetic profiles from many-to-many analysis and particle profiles derived from the hatchling drift model 

We then quantified the number of particles from each 

source to enter these territorial waters during the modelled 

first year of drifting (though it should be noted that 

a longer oceanic phase could occur; Musick & Limpus 

1997). Euclidean distance matrices were calculated for 

particle and genetic profiles (treating each estimate of 

proportional contribution as a character) and compared 

with a Mantel test (PopTools v. 3.0; Hood 2009). Additionally, 

to facilitate comparison with the results of 

Bowen et al. (2007a), we investigated the relationship 

between genetic and particle profiles with linear regression, 

regressing arcsine transformed proportions (Graph- 

Pad InStat 3.10, GraphPad Software). 

Results 

Cay Tex Bah Cuba PR USVI DR Mex 

MSA Drift MSA Drift MSA Drift MSA Drift MSA Drift MSA Drift MSA Drift MSA Drift 

Anti 6.0 13.1 1.9 0.0 5.2 13.2 2.7 4.3 5.3 18.5 10.2 50.2 4.4 23.1 6.7 3.8 

Barb 46.1 40.3 3.3 0.0 22.7 25.9 15.7 13.5 47.4 28.6 27.7 21.2 65.7 35.3 5.8 13.8 

Belz 0.7 0.0 0.6 0.0 0.8 0.0 0.9 0.0 1.5 0.0 0.7 0.0 2.1 0.0 0.7 0.6 

Cuba 21.9 45.7 2.4 0.0 26.1 0.0 44.3 64.6 8.0 0.0 23.0 0.0 10.1 0.0 5.8 0.0 

Mexi 13.2 0.0 85.3 100.0 28.4 46.6 10.5 17.1 8.5 0.0 14.1 0.0 7.7 0.0 71.6 81.3 

USVI 3.0 0.3 2.0 0.0 3.7 0.7 2.4 0.2 8.1 8.5 2.3 26.4 3.9 4.0 2.5 0.2 

CR 0.5 0.6 0.3 0.0 0.5 0.5 0.7 0.3 1.4 0.0 0.4 0.0 1.5 0.0 0.4 0.3 

PR 8.7 0.0 4.1 0.0 12.6 13.0 22.9 0.0 19.7 44.4 21.6 2.1 4.7 37.6 6.3 0.0 

Rows represent potential source rookeries – Antigua, Barbados, Belize, Cuba, Mexico, US Virgin Islands, Costa Rica and Puerto Rico; 

columns represent genetically characterized foraging grounds – Cayman Islands, Texas, Bahamas, Cuba, Puerto Rico, US Virgin 

Islands, Dominican Republic and Mexico (for sources of published genetic data see Fig. 1). Numbers are mean proportional 

contribution from each rookery to each foraging ground, estimated via weighted many-to-many mixed stock analysis (MSA) and 

proportion of particles from each rookery to enter each foraging ground during the first year of drifting, from the hatchling drift 

model (Drift). 

Genetic structure 

Among 92 neritic juvenile hawksbills from the Cayman 

Islands, we detected 11 mitochondrial DNA (mtDNA) 

control region haplotypes: Ei-A1, Ei-A2, Ei-A3, Ei-A9c, 

Ei-A11c, Ei-A18, Ei-A20, Ei-A24, EiA28, Ei-A29 and a 

previously undetected haplotype, Ei-A72 (GenBank 

accession number GQ925509). The Cayman Islands foraging 

aggregation represented a diverse mixed stock 

(h = 0.72 ± 0.04; p = 0.01 ± 0.005). Haplotype frequencies 

from Grand Cayman and Little Cayman were not 

significantly different (population pairwise FST = )0.01, 

P = 0.83). Therefore results for the two study sites were 

pooled for subsequent analyses. 

Rookeries of origin 

Using unweighted and weighted many-to-many analysis, 

we estimated the contributions of genetically character- 



ized Caribbean rookeries to the Cayman Islands foraging 

aggregation. Shrink factors for all chains were


Fig. 2 Genetic composition at the Cayman Islands foraging 

aggregation. Among the 92 individuals sequenced, 11 haplotypes 

were detected: Ei-A1 (44); Ei-A2 (2); Ei-A3 (1); Ei-A9c (8); 

Ei-A11c (17); Ei-A18 (1); Ei-A20 (1); Ei-A24 (11); Ei-A28 (4); Ei- 

A29 (1); Ei-A72 (2). (a) Using an unweighted many-to-many 

model (white bars), estimated contributions (mean proportion, 

2.5% and 97.5% confidence intervals) of genetically characterized 

hawksbills rookeries to the Cayman Islands foraging aggregation 

were Antigua (21.3%, 3.0–41.8%), Barbados (20.5%, 

1.1–48.1%), Belize (8.7%, 0.4–24.9%), Cuba (12.6%, 0.6–34.1%), 

Mexico (9.1%, 0.8–16.0%), USVI (11%, 0.4–27.6%), Costa Rica 

(10.7%, 2.9–21.3%), Puerto Rico (6.1%, 0.8–16.6%). When 

source population size was used as a constraint (grey bars), estimates 

were Antigua (6.0%, 0.7–15.5%), Barbados (46.1%, 20.6– 

69.0%), Belize (0.7%, 0.0–2.7%), Cuba (21.9%, 3.7–43%), Mexico 

(13.2%, 7.4–20.6%), USVI (3%, 0.1–9.4%), Costa Rica (0.5%, 

0.0–2.0%), Puerto Rico (8.7%, 1.5–18.3%). (b) Arrows are scaled 

in proportion to estimated mean contribution (weighted manyto-many) 

to indicate potential scale of recruitment. 

365 days of drifting) and genetic profiles (many-tomany 

results for all genetically characterized Caribbean 

foraging aggregations) (Fig. 4). 

Discussion 

Because hawksbill turtles spend the vast majority of 

their lives at sea, for many populations links between 

nesting beaches and foraging grounds are unknown. 

To estimate origins of neritic juvenile hawksbill turtles 

foraging in the Cayman Islands, we applied many-tomany 

modelling using data from this study and other 

published genetic studies of Caribbean hawksbills. For 

the Cayman Islands foraging aggregation potentially 

contributing source rookeries spanned the Caribbean 

basin – delineating a scale of recruitment of 200– 

2500 km (straight-line distance) and highlighting the 

complex spatial ecology of the species. 

We then investigated the role of ocean currents as a 

mechanism underlying patterns of dispersal. Bowen 

et al. (2007a) previously tested the role of geographic 

distance (both straight-line and modified in order to 

account for a likely influence of ocean currents) in determining 

recruitment of hawksbills from nesting populations 

to foraging aggregations. Here, we compared 

results of mixed stock analysis to particle profiles, which 

take source population size, geographic distance and 

oceanographic circulation patterns into account – an 

important consideration as oceanic juveniles are unlikely 

to follow a direct route between nesting beaches and foraging 

grounds. A strong correlation was detected 

between patterns of stock composition at Caribbean 

hawksbill foraging aggregations and patterns of particle 

distribution at these sites – indicating that ocean currents 

likely play a substantial role in determining geographic 

patterns of genetic diversity, and that models of 

oceanic drift may illustrate movements of oceanic juvenile 

turtles during the lost year or years. Putative dispersal 

patterns for oceanic juvenile hawksbills varied 

regionally: particles from many rookeries were broadly 

distributed across the Caribbean (a ‘turtle soup’), while 

particles from other rookeries appeared to be regionally 

constrained (forming ‘turtle groups’). Thus, because of 

the complexities of regional and local current patterns, 

some areas will be more diverse (turtles recruiting from 

multiple jurisdictions) while others will experience 

greater levels of proximate or local recruitment. 

Ultimately, population resolution may allow demographic 

parameters such as abundance, survival, sex 

ratio and growth to be linked across broad spatiotemporal 

scales and incorporated into population modelling 

(Bowen et al. 2004; Reece et al. 2006). However, at present, 

the accuracy of mixed stock estimates is limited by 

insufficient baseline data from nesting beaches (Troëng 

et al. 2005). Indeed, detection of a previously unknown 

haplotype at the Cayman Islands foraging aggregation 

indicates that nesting beaches in the Caribbean or source 

rookeries farther afield have been incompletely or insufficiently 

sampled. Longer periods of sampling and larger 

sample sizes (Reece et al. 2006), standardized use of 

primers which amplify larger mtDNA fragments (Abreu- 

Grobois et al. 2006), and expanded geographic coverage 



Fig. 3 Trajectories of modelled particles representing drifting oceanic stage juvenile turtles, released from hawksbill index beaches 

in (a) Gulf of Mexico (Isla Holbox, Punta Xen and Las Coloradas Mexico) (b) Greater Antilles (Doce Leguas Cuba, Mona Island 

Puerto Rico) (c) eastern Caribbean (Long Beach Antigua, Hilton Beach Barbados, Buck Island USVI) (d) southern Caribbean (Archipiélago 

Los Roques and Península de Paria Venezuela) (e) southwestern Caribbean (Tortuguero Costa Rica) (f) western Caribbean 

(Gales Point Belize) (g) depicts overall particle trajectory patterns in the wider Caribbean. 



Fig. 4 Comparison of hatchling drift (black bars) with weighted (grey bars) and unweighted (white bars) many-to-many results for 

the Cayman Islands and other genetically characterized foraging grounds (for sources of published genetic data see Fig. 1). Data are 

mean proportion (±2.5–97.5% confidence intervals for many-to-many analysis). 

(Engstrom et al. 2002) are priorities for improving estimates. 

Ocean current modelling may serve to identify 

potential locations of regional foraging aggregations 

and priorities for studies of unsurveyed source rookeries: 

for example, particles from the southern Caribbean 

(Venezuela) would appear to be widely dispersed, yet 

rookeries are presently insufficiently characterized to 

permit inclusion in mixed stock estimates. 

Within the context of developing a hatchling drift 

model, much remains to be resolved or refined regarding 

biological parameters (e.g. sizes of hawksbill source 

populations, timing of peak hatching, duration of the 


oceanic phase, behaviour of oceanic juveniles pushed 

toward landmasses, and roles of active swimming and 

orientation in hatchlings, post-hatchlings, and oceanic 

juveniles) and modelling ocean currents (e.g. incorporating 

wind-induced components; Hays & Marsh 1997; 

Girard et al. 2009). In this study, our hatchling drift 

model was limited to determining exposure of foraging 

sites to particles during the first year of drift. This is 

useful as a measure of potential for recruitment from 

each of the sources, as the timeframes within which 

hawksbills begin actively swimming and recruit to foraging 

grounds is unknown. However, a longer oceanic 

phase may occur (Musick & Limpus 1997), calling for 

extended modelling of oceanic drift when such longterm 

high-resolution oceanographic data become available. 

Comparison of multiple years of Aviso data may 

also be informative in determining inter-annual variations 

in recruitment and implications for management: 

if, as in green turtles, there is temporal structuring in 

the genetic composition of neritic juvenile foraging 

aggregations, then marine turtle management plans 

should not be based on the ‘snapshot’ of short-term 

genetic studies (Bjorndal & Bolten 2008). 

In coral reef fishes, behaviour of larvae has been 

shown to influence population connectivity (Paris et al. 

2007) but to date, it has proven difficult to separate the 

role of oceanic currents from behaviour in determining 

distribution of oceanic juvenile marine turtles (Naro- 

Maciel et al. 2007). Under experimental conditions, loggerhead 

hatchlings have been shown to exhibit directed 

swimming which is consistent with that which would 

be needed to remain within oceanic gyres (Lohmann 

et al. 2001) and in the wild, oceanic juvenile loggerheads 

may actively select foraging areas at locations 

closely correlated with the latitudes of their natal beaches 

(Monzón-Argüello et al. 2009) and home toward 

their natal regions at the conclusion of the oceanic stage 

(Bowen et al. 2004). However, the ability to move 

against prevailing currents appears to be linked to 

increasing body size (Monzón-Argüello et al. 2009). 

Oceanic juvenile loggerheads in downwelling lines 

show minimal activity and positive buoyancy (Witherington 

2002) and as hawksbill hatchlings at least in 

some populations appear to be less active in the initial 

days of dispersal than other marine turtle species 

(Chung et al. 2009a) it is likely that small oceanic juvenile 

hawksbills are also relatively passive surface drifters. 

Therefore, while vertical movement of reef fish 

larvae limits the application of models based on surface 

current data (Fiksen et al. 2007) these models are especially 

applicable to marine turtles. 

Occurrence of active orientation, particularly at the 

end of the oceanic stage, may nevertheless explain 

contributions of hawksbill rookeries against prevailing 



currents to foraging sites. Alternatively, unsurveyed 

hawksbill rookeries may contribute to foraging stocks 

(i.e. contributions assigned to a down-current source 

may instead originate from an unsurveyed or incompletely 

surveyed up-current source). It is also possible 

that a portion of Caribbean hawksbills could circle the 

Atlantic before re-entering the Caribbean, following a 

similar route to oceanic juvenile loggerheads – or perhaps 

a ‘short-cycle’ of the Atlantic could occasionally 

occur where hawksbills might become entrained in 

Atlantic eddies which more rapidly re-enter the Caribbean. 

In our comparisons between many-to-many 

results and the hatchling drift model, estimated contributions 

from some rookeries were high using genetic 

markers while the drift model predicted no contributions. 

These findings may be indicative of an Atlantic 

cycle or short-cycle: for instance, Mexican contributions 

to seemingly up-current foraging sites in the eastern 

Caribbean may be explained by hawksbills cycling a 

portion of the Atlantic before re-entering the Caribbean. 

Integration of better biological data with heuristic 

modelling of oceanic drift will assist in resolving migratory 

connectivity for marine turtles. Patterns of dispersal 

for oceanic juveniles may be confirmed by 

documentation of stranding patterns (Meylan & Redlow 

2006) and genetic studies (Carreras et al. 2006; Bowen 

et al. 2007a). In surveys to date, magnitude of hawksbill 

genetic diversity varies regionally – being lowest in the 

Gulf of Mexico, where mixed stock analysis indicates 

that oceanic juveniles originate almost exclusively from 

Mexican rookeries (Bowen et al. 2007a), and higher near 

the eastern Caribbean gyres and in foraging areas 

passed by the Caribbean current. Sightings and strandings 

of oceanic phase hawksbills in Florida (Meylan & 

Redlow 2006) and rarely on the east coast (Parker 1995) 

support transport from the Caribbean through the 

Florida Straits, and the presence of a neritic juvenile 

hawksbill foraging aggregation in Bermuda (Meylan 

et al. 2003) suggests some transport in the Gulf Stream. 

However, further genetic sampling of stranded and 

free-living oceanic hawksbills and genetic characterization 

of additional neritic foraging grounds is required. 

Efforts to resolve movements are particularly timely, 

as management of hawksbill turtles has been the subject 

of considerable controversy in recent years. Hawksbills 

are designated as ‘critically endangered’ by the IUCN 

(2007) and listing on Appendix I of the Convention on 

the International Trade in Endangered Species (CITES) 

bars international trade among parties to the Convention. 

Nevertheless, commercially valuable hawksbill 

products are still in high demand in some areas. Recent 

debate has centred on conservation status and priorities, 

scale and extent of transboundary movements (Bowen 

& Bass 1997; Mrosovsky 1997) and sustainable use of


mixed stocks (Bowen et al. 2007b; Godfrey et al. 2007; 

Mortimer et al. 2007a,b). It has been argued that harvesting 

of hawksbills from foraging grounds should be 

prohibited, as exploitation of mixed stocks could potentially 

impact rookeries on a regional scale – or alternatively, 

that sustainability of harvesting on hawksbill 

foraging aggregations could be determined on a caseby-case 

basis (Godfrey et al. 2007). 

Many-to-many analysis and hatchling drift models 

facilitate an integrative, rookery-centric approach 

(Bolker et al. 2007) in which contributions of both small, 

vulnerable rookeries and large, regionally important 

rookeries are evaluated. Oceanic juveniles from some 

rookeries appear to be dispersed among multiple foraging 

grounds, while those from other rookeries appear to 

be more locally constrained. This diversity of distribution 

represents both a challenge and an opportunity for 

marine turtle management. Broadly dispersed stocks 

are difficult to manage, yet threats are often geographically 

widely dispersed and their impacts on individual 

stocks will depend on how they interact. In contrast, in 

areas with greater levels of local or proximate recruitment, 

threats – or conservation efforts – may have a 

concentrated effect (Bowen et al. 2004, 2005). Indeed, 

Caribbean hawksbill rookeries have experienced varying 

population trends, ranging from near-extirpation 

(Cayman Islands: Aiken et al. 2001) to dramatic increase 

(Antigua: Richardson et al. 2006; Barbados: Beggs et al. 

2007) – raising the possibility that variations in dispersal 

across an oceanographically complicated region 

may be a factor in these differing trajectories. 

While much remains to be determined regarding 

movements and management needs of hawksbill turtles, 

integration of many-to-many analysis and oceanographic 

data represents a promising approach. In this 

study, we delineated links between regional management 

units by conducting many-to-many mixed stock 

analysis across the range of Caribbean hawksbill rookeries 

and foraging aggregations, developed a tool with 

which to illustrate a possible role of ocean currents in 

determining distribution of oceanic juveniles, and highlighted 

gaps in knowledge and priorities for future 

sampling. Overall, results facilitate a broader understanding 

of Caribbean hawksbill movements – filling an 

important gap in knowledge of life-history and potentially 

informing regional management. 

Acknowledgments 

For invaluable logistical support and assistance with fieldwork, 

we thank Cayman Islands Department of Environment 

research, administration, operations and enforcement staff and 

numerous volunteers. For advice on analysis, we thank J. Hunt 

and W. Pitchers at University of Exeter, Cornwall campus. 

Vincente Guzmán (CONANP-México) and Eduardo Cuevas 

(Pronature-Península de Yucatán A.C.) generously provided 

information on population sizes of Campeche, Yucatán and 

Quintana Roo rookeries. Work in the Cayman Islands, the UK 

and the USA was generously supported by the European 

Social Fund, the Darwin Initiative, the Department of Environment, 

Food & Rural Affairs (DEFRA), Eckerd College, the Foreign 

and Commonwealth Office for the Overseas Territories, 

the Ford Foundation, the National Fish and Wildlife Foundation 

(NFWF) and the Turtles in the Caribbean Overseas Territories 

(TCOT) Project. We also acknowledge support to J. 

Blumenthal (University of Exeter postgraduate studentship and 

the Darwin Initiative). The manuscript was improved by the 

input of three anonymous reviewers. 

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J.M.B. is a research officer at the Cayman Islands Department 

of Environment, where her work centres on using spatial ecology 

to aid in understanding management requirements of sea 

turtles and other marine species. G.E.-P. is the director of the 

Department of Environment and T.J.A. is the deputy director 

for the research section. M.S.C. coordinates a gobal sea turtle 

network as director of seaturtle.org. F.A.A.-G.’s research on 

conservation genetics spans marine turtle populations in Mexican 

and Wider Caribbean sites. P.A.M. is RR Hallin Professor 

of Natural Science at Eckerd College; A.B.M. leads the marine 

turtle research program for the Florida Fish and Wildlife Conservation 

Commission; together they study the reproductive 

biology, ecology and migrations of sea turtles in the Western 

Atlantic with long-term projects in Panama and Bermuda. A.F. 

works on marine turtle conservation genetics in West Africa 

and coordinates the Marine Turtle Partnership in Gabon. 

M.W.B. is head of the Biodiversity and Ecological Processes 

Group at Cardiff University. A.C.B. and B.J.G. coordinate the 

Marine Turtle Research Group at a range of sites around the 

world including Ascension Island, Northern Cyprus and the 

UK Overseas Territories.

The Elusive Manatee -- 

An ethological approach to understanding behavior in the West Indian manatee 

Caryn Self Sullivan, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843-2258 

Last updated 19 October 2000 

CONTENTS 

Preface 

Part I: Introduction -- 

Ethology, Proximate & Ultimate, and Sirenians 

Part II: Problem Solving -- 

Social, Reproductive & Physical 

References 

Recommended Reading 

Glossary 


PREFACE 

This Species Brief originated in WFSC 422, an 

ethology course taught by my academic advisor, Dr. Jane 

M. Packard, at Texas A&M University in 1998. It was 

updated this year for distribution to Earthwatch Institute 

volunteers. Please consider it a work in progress – a “draft 

document” as it is continuously being revised and updated 

with better references and new information. Designed to be 

used by schools, zoos, wildlife parks, and oceanaria, it 

makes an excellent starting place for students, teachers, and 

others who are interested in learning about animal behavior 

and/or sirenians (manatees & dugongs). But, remember, it 

is only a briefing document. Use it to catapult yourself into 

the exciting world of animal behavior -- using manatees as 

an example. For more details, start with the 

Recommended Reading section; scientists and university 

students are encouraged to delve into the primary literature 

listed in the References section. 

PART I: INTRODUCTION 

As we idled around the corner of Swallow Caye I 

sighted two manatee noses in the distance. They were 

barely visible as they broke the surface of the clear 

Caribbean water. Patch, our boat operator, spotted the 

manatees at almost the same instant – he probably saw 

them first -- because before I could motion to him, he had 

already shut down the engine. We waited in silence, hoping 

they would surface again. So it goes with research on the 

elusive manatee. Most behavioral observations of manatees 

have been conducted on Florida manatees, either in 

captivity or in the clear spring waters of Florida during 

winter aggregations. Only recently have we attempted to 

observe behavior in Antillean manatees, which are sparsely 

distributed throughout the Caribbean, including the tropical 

waters of Belize. 

Five minutes passed - how long can these guys stay 

down? What are they doing down there? One reason we 

know so little about these incredibly well adapted animals 

is because they spend the majority of their time underwater, 

1 

regularly staying submerged 3-5 minutes between breaths. 

We heard them before we saw them. Both noses broke the 

water with a forceful exhalation at virtually the same 

moment. Then they were down again. I quietly entered the 

water and stealthily snorkeled the 50 meters towards their 

last location. Where did they go? Stop. Look. Listen. I 

heard them breathe again. When they finally came into 

view underwater, I thought, "Uh oh... a mother calf pair -- 

they are going to run away". 

The larger animal was about 3 meters long, almost 

twice as big as the smaller. Readings and previous 

experience led me to assume a mother-calf relationship 

based on this size differential. But they didn't run. The 

larger animal was gently nuzzling the smaller one's back 

with its big prehensile lips. The next time they surfaced to 

breath, they were nose to nose in a manatee "kiss". When 

they noticed us, the nuzzling stopped and they both sank 

slowly to the soft muddy bottom. As they sank, I heard a 

few squeaks, similar to manatee vocalizations I’d recorded 

between mother-calf pairs last year. There they rested, side 

by side in typical mother-calf position, for three minutes. 

When the smaller one rose to the surface to breathe, I could 

tell it was a female by the location of a genital slit near the 

anus. But, what a surprise I had when the larger animal 

surfaced and I saw by a genital slit near the umbilicus scar 

that it was a male. I'll make no more assumptions about 

mother-calf pairs based on size differentials! 

Ethology 

Do manatees breath simultaneously? If so, why? 

Why was the large male manatee nuzzling the smaller 

female? Why do manatees "kiss"? How did they sink to 

the bottom and stay - without moving a muscle? Why did 

they vocalize during their descent? How do manatees 

create sound? Do manatees often lie side by side on the 

bottom? Are manatees usually found in pairs, or groups, or 

alone? Why? How long can manatees stay underwater 

without breathing? Why did the smaller animal surface to 

breath before the larger animal did? These are just a few of 

the questions raised by the brief observation. Some 

answers to these "how" and "why" questions are known; 

other answers may come through long-term ethological 

studies. 

Ethology is a relatively new, multi-perspective 

scientific approach to the study of animal behavior. Made 

famous by the work of 1973 Nobel Prize winners, Konrad 

Lorenz, Karl von Frisch, and Nikolaas Tinbergen 

(www.nobel.se/medicine/laureates/1973/index.html), it 

focuses on animal behavior in a natural setting. By using a 

Scientific Perspective, it differs from Folk Psychology, 

which is often used to explain animal behavior to the

general public. Folk psychology perspectives are intuitive 

in nature, usually based on personal experiences and 

observations. They are considered anthropomorphic 

because they describe and explain behavior in human terms 

– which are often the only terms we have to start with! 

These perspectives are appropriate and very useful when 

communicating with non-scientists, such as audiences in 

zoos, oceanaria, and wildlife parks. An interpreter will 

often use folk psychology to describe and explain animal 

behaviors based on the “model” that animals have desires, 

beliefs, and emotions like humans. Scientists also use these 

perspectives in developing hypotheses about specific 

behaviors. For example, I was using folk psychology when 

I assumed that the manatees in the anecdote above were a 

mother-calf pair. My intuition was based on the size 

differential and behavioral patterns typical of mother-calf 

pairs. 

Ethology encourages us to develop additional 

Scientific Perspectives in understanding, explaining, 

and/or describing animal behavior; the classical ethological 

perspectives include cause, development, evolution, and 

function (Martin & Bateson 1993, Lehner 1996). Modern 

ethologists agree that the behavior of an animal is the result 

of complex interactions between the genetic makeup of an 

individual and environmental factors that act upon the 

individual (Alcock 1998). However, many aspects of an 

animal's behavior can be explained from two very different 

perspectives: proximate and ultimate (Martin and Bateson 

1993, Lehner 1996). This often results in 

miscommunication among observers who are looking at 

behavior from different perspectives. Proximate and 

ultimate comparisons are equivalent to apple and orange 

comparisons – i.e. they are both valid fruits, but they are 

different things. "How" questions are usually asked from a 

proximate perspective; how questions seek explanations 

about the physical and chemical mechanisms that trigger an 

individual animal's behavior at any given point in time. 

"Why" questions, on the other hand, are usually based on 

ultimate perspectives; answers to these questions attempt 

to explain why certain behaviors exist within a population 

(or species) of animals. In other words, what pressures of 

natural selection led to the existence of a particular 

behavior within a population or species. Ethologists 

further divide proximate and ultimate into the subcategories 

of cause, development, evolution, and function 

based on the work of Niko Tinbergen (Martin and Bateson 

1993, Lehner 1996). 

Proximate: Cause and Development are 

proximate perspectives, which look at the behavior of an 

individual animal. Proximate Cause perspectives include 

looking at both internal mechanisms (hormones, 

neurotransmitters) and external stimuli (pheromones, photoperiod, 

temperature) that interact to trigger specific 

behaviors in a mature animal. Dr. Jane M. Packard 

explains it using the analogy of a camera, “Think of 

Proximate Cause as a snapshot in time that shows what is 

causing the behavior at that particular moment.” For 

2 

example, in our observation above, what “caused” the 

manatees to kiss? Was the female was giving off some 

signal (vocal, chemical, or behavioral) that attracted the 

male? Did the tactile stimulation by the male cause 

hormone production in the female, which triggered the 

“kiss”? Most likely, it was is a complex interaction 

between both the internal state of each animal and the 

resulting external behavioral stimuli. Proximate 

Development perspectives look at behavioral changes that 

occur as an individual animal matures. Think of Proximate 

Development as a "video" that shows how a behavior 

develops and changes over time as an individual animal 

matures. How might the behavior of manatees at different 

ages compare to the interactions we observed? 

Ultimate: Evolution and Function are ultimate 

perspectives, which look at specific behaviors present in a 

population of animals. These behaviors are thought to 

have evolved over time through the process called Natural 

selection. For Natural selection to act on a behavioral 

characteristic, the behavior must meet certain criteria – the 

same criteria necessary for natural selection to act on a 

physical trait such as coloration: (1) the trait must vary 

among individuals within a population; (2) the variation 

must be heritable; (3) if the heritable variation results in 

differential fitness (i.e. variations in the trait result in some 

individuals reproducing more successfully than others); 

then (4) we would expect the behavior to become 

genetically fixed in the population as the proportion of 

individuals displaying the trait increased (i.e. changes in 

the proportion of genotype and resulting phenotype). 

Ultimate Evolution perspectives include the 

comparison of behaviors among different, closely related 

species. This is our “video” perspective. From an 

Ultimate Evolution perspective, we hypothesize about how 

a behavior has changed (or remained the same) at the 

population and/or the species level over many generations. 

In my study of Antillean manatees, I will be comparing 

behavior to previous observations of behavior in Florida 

manatees. Although these sub-species are very closely 

related, they share different habitats. The Florida manatee 

inhabits a temporal/sub-tropic region where its behaviors 

are shaped by dramatic changes in water temperature during 

the year. On the other hand, the Antillean manatee inhabits 

a tropical region where the water temperature is relatively 

constant year round. We expect some behaviors to differ 

between the two sub-species as they evolved in different 

habitats. If behaviors, which we think are driven by water 

temperature today, exist in both sub-species, then perhaps 

they had some other function in the past. 

Ultimate Function perspectives attempt to explain 

what the function of a specific behavior is within a 

population, (i.e. why animals that display this behavioral 

trait are more reproductively successful than individuals 

who do not). This is our “snapshot” perspective. If 

variation exists within the behavior, Ultimate Function is 

the perspective used to explain why. Some Florida 

manatees travel long distances into more temperate regions

during the summer months while others stay in the same 

area year round – but we are not sure why the traveling 

behavior exists. The traveling animal must use more 

energy than the year round resident. Perhaps male animals 

that travel are exposed to more potential mates – thereby 

increasing their reproductive success. Chessie, a famous 

male manatee first sighted in the Chesapeake Bay in 1994, 

is known to have traveled between Florida in the winter and 

Rhode Island in the summer of 1995! Sweet Pea, a female 

rescued near Houston, Texas, later traveled along both 

coasts of Florida. Gina, a female manatee first sighted in 

Tampa Bay on the west coast of Florida is currently 

hanging out in the Bahamas! One of my questions is: Do 

Antillean manatees exhibit similar long distance traveling 

behaviors? 

Hypotheses about “why” these behaviors exist in 

manatees are different from hypotheses about “how” these 

behaviors are executed. The “why” questions are from 

ultimate perspectives of evolution and function, the “how” 

questions are from proximate perspectives of cause and 

development. These four basic concepts of ethology can 

be arranged in a 2 x 2 table comparing TIME FRAME and 

ANALYSIS PERSPECTIVES: 

TIME/ 

ANALYSIS 

Proximate 

Perspective 

Individual Animals 

“How Questions” 

Ultimate 

Perspective 

Populations/Species 

“Why Questions” 

Pattern-Static 

“Snapshot” 

CAUSE 

(control) 

behavioral 

triggers: 

internal state/ 

external 

stimuli 

FUNCTION 

adaptive 

significance: 

effect on 

reproductive 

fitness 

Process-Dynamic 

“Video” 

DEVELOPMENT 

(ontogeny) 

changes in 

behavior as an 

animal ages: 

maturation and/or 

learning 

EVOLUTION 

(phylogeny) 

changes in 

behavior 

(genotype) as 

populations/ 

species diverge 

We can remember the concepts of ethology with the 

acronym AB=CDEF (Animal Behavior = Cause, 

Development, Evolution, Function). On the TIME axis, 

Cause and Function are “snapshot” perspectives that look 

at internal state and external stimuli in an individual animal 

or at reproductive success in a population of animals. 

Development and Evolution are “video” perspectives that 

look at changes in behaviors over time, either as the 

individual animal matures or as the population evolves. 

On the ANALYSIS axis, Cause and Development are 

proximate perspectives that attempt to answer "how" 

questions at the level of individual animals. Evolution and 

Function are ultimate perspectives that attempt to answer 

"why" questions at the level of populations and/or species. 

3 

For more information on Ethology, I encourage you to visit 

Dr. Packard’s website at canis.tamu.edu/wfscCourses/. 

Sirenians 

So what are manatees anyway, and why should we 

study their behavior? Manatees belong to the order Sirenia 

of which there are only 4 extant species in 2 families, 

Trichechidae and Dugongidae. Although scientists often 

lump sirenians together with the order Cetacea (whales 

and dolphins) as totally aquatic marine mammals, manatees 

and the dugong are actually more closely related to 

elephants, hyraxes, and aardvarks than to any other marine 

mammal (Fischer 1990, Maluf 1995, Springer et al. 1997, 

Gaeth et al. 1999). Until a few years ago, very few people 

had ever heard of manatees, dugongs, or sea cows. But, as 

we learn more about these elusive and highly specialized 

creatures that share our coastal habitats, they are becoming 

more and more popular among both scientists and 

conservationists. The West Indian manatee (Trichechus 

manatus), the West African manatee (Trichechus 

senegalensis), and the Amazonian manatee (Trichechus 

inunguis) are members of the family Trichechidae. The 

dugong (Dugong dugon) is the only surviving member of 

the family Dugongidae (Reynolds and Odell 1991). 

Steller's sea cow (Hydrodamalis gigas) is usually included 

when we talk about modern sirenians; it was in the family 

Dugongidae (Reynolds and Odell 1991), but the species 

was extirpated by humans in 1768, just 27 years after it 

was discovered by Russian explorers in 1741 (Stejneger 

1887). Today, local and international laws protect all four 

living species, but they are also either threatened or 

endangered by humans wherever they exist. 

Florida Manatees: There is little evidence that 

Florida manatees were ever harvested commercially. But 

subsistence use, habitat destruction, and competition for 

space with recreational boaters have taken their toll on both 

prehistoric and modern populations. The USGS Sirenia 

Project, the U. S. Fish and Wildlife Service, and the Florida 

Fish and Wildlife Conservation Commission (formerly the 

Florida Department of Environmental Protection) have 

funded much of the manatee research in the United States. 

Over the past three decades, conservation efforts in Florida 

resulted in significant scientific research on the distribution, 

population biology, and behavior of the Florida manatee 

subspecies, T. m. latirostris (see O'Shea et al. 1995). 

Ecological and behavioral studies on localized populations 

such as those in Crystal and Homosassa Rivers (Hartman 

1979), St. John's River (Bengtson 1981), and Sarasota Bay 

(Koelsch 1997) have added to our understanding of Florida 

manatee behavior. However, relatively little research has 

been conducted outside of Florida. Therefore, most of the 

referenced information contained herein refers to the 

Florida subspecies. 

Antillean Manatees: Even before Russian sailors 

were exploiting Steller’s sea cow meat in the North Pacific, 

European explorers were provisioning their ships with 

Antillean manatee meat from the Caribbean area. Besides 

harvesting manatees for subsistence, some Native

Americans also sold manatee meat to the Europeans 

(O’Shea 1994). Today, the Antillean subspecies, T. m. 

manatus, is classified as endangered throughout its sparse 

distribution in the Caribbean Sea and Western Tropical 

Atlantic Ocean (Lefebvre et al. 1989). O'Shea and 

Salisbury (1991) suggest that Belize (formerly British 

Honduras), where manatees have been protected since the 

1930s (Auil 1998), may be the last stronghold for Antillean 

manatees in the Caribbean. Current research in Belize by 

James A. "Buddy" Powell, Nicole Auil, Greg Smith, Katie 

LaCommare, and myself is expanding our knowledge of the 

Antillean manatee. Most of the anecdotes included in this 

brief come from my personal experiences in Belize. 

PART II: PROBLEM-SOLVING 

One way to interpret animal behavior is as a method 

of problem solving. Over geological time, animals have 

evolved behaviors that enable them to solve problems. 

Some of these behaviors are identical from one individual 

to another. We describe such a behavior as a Fixed Action 

Pattern (FAP), because the individual’s genes control the 

trait. In other words, the genetic trait has become fixed in 

the population and all individuals perform the behavior in 

exactly the same way because they inherited the trait from 

their ancestors. At the other end of the behavioral scale, we 

find behaviors that vary a great deal among individuals. 

We describe such a behavior as a Variable Action Pattern 

(VAP), because the environment controls the trait. In other 

words, each individual performs the behavior differently 

due to different environmental factors during development. 

Additionally, any individual may perform the behavior 

differently at different times, depending its internal state 

(hormones, chemicals, neurons) and on external stimuli 

(environment). Of course FAP and VAP are not specific 

categories, but are the end points along a continuum. If a 

behavior falls near the middle of this continuum, we 

describe it as a Modal Action Pattern (MAP). In other 

words, the behavior is controlled in part by genetics and in 

part by the environment. 

We can divide problem solving into three major 

categories: reproductive, physical, and social. Manatees 

have evolved some interesting behaviors to overcome 

reproductive and physical problems. But, they are not 

considered to be very social animals. Although they tend 

to aggregate on resources, they do not appear to live in 

social groups and significant social behaviors have not been 

observed outside of reproductive activities. This species 

brief will use the concepts of ethology to introduce you to 

the behavioral methods manatees use to solve some of their 

reproductive and physical problems. We will examine 

specific behaviors using the different perspectives of 

proximate cause, proximate development, ultimate 

evolution, and ultimate function to answer a few questions 

regarding "how" and "why" manatees behave as the do. 

4 

Reproductive Problem Solving 

We idled into one of my favorite coves at the end of 

Bogue C in the Drowned Cayes near Belize City. I had 

taken volunteer researchers to this spot on previous 

occasions and ALWAYS, there had been a manatee resting 

in the manatee hole on the far side of the cove. As if on 

cue, before we could even cut the engine and anchor the 

boat, a single manatee surfaced in the vicinity of the 

manatee hole. Within minutes a second manatee surfaced 

in the middle of the cove. Two minutes later, a third animal 

entered the cove. "Gee...” I thought, "This must be a 

popular resting cove!" But, the two animals in the center of 

the cove were too active to be resting. I didn’t think they 

could be feeding, either, because previous habitat snorkels 

had found NO vegetation on the bottom. Another four 

minutes passed and two more manatees swam under the 

boat to join the active pair in the middle of the cove. "This 

is great,” I told the volunteers, "we'll be able to see how 

long it takes them to settle into a resting pattern". But they 

didn't settle. For the next hour we watched the four 

manatees in the middle of the cove breathe, roll, dive, and 

kiss while the first animal appeared oblivious to all the 

activity less than 50 meters away. Were we observing a 

mating herd? 

Mating System: One parameter of the West Indian 

manatee mating system is known as the mating herd. A 

mating system is the species-typical pattern of problem 

solving that includes how an individual finds a mate, how 

long it remains with the mate, and how much energy it 

invests in its offspring (Drickamer, et al. 1996). The West 

Indian manatee mating system can be broadly defined as 

promiscuous with the estrous female exhibiting 

polyandrous behavior and the male exhibiting polygynous 

behavior (Hartman 1979). A manatee-mating herd 

consists of a group of males in pursuit of an estrous female. 

The group is ephemeral, lasting only from a week to a 

month (Hartman 1979) and consisting of up to 20 males. 

The group does not remain together afterwards. Males will 

participate in multiple mating herds and attempt to 

copulate with many estrous females; similarly, females will 

copulate with multiple males among those in the herd. 

When we discuss why this mating system exists in 

manatees, we are using the ultimate function perspective. 

From the perspective of proximate cause, we do not 

know exactly what external signal stimulates males to 

aggregate around and attempt to copulate with the estrous 

female. Females must produce some sort of signal, 

possibly a chemical or acoustical signal, which stimulates 

an internal hormonal mechanism in males causing them to 

pursue her. Likewise, the male’s internal state must be such 

that he responds to the signal. Proximate development 

perspectives would look at how the males’ reaction to such 

a signal might differ at other stages of maturity. 

Daniel S. Hartman, one of the first scientists to 

make long-term observations of manatee behavior in the 

wild, found similarities between manatee mating herds and 

elephant mating, noting that female elephants are also

polyandrous - often mating with several males over a 

period of several hours. When Hartman (1979) compares 

the mating behavior of manatees to that of elephants, he is 

writing from an ultimate evolution perspective. In other 

words, he is hypothesizing that this aspect of the mating 

system evolved millions of years ago in an ancestor shared 

by both the manatee and the elephant. Since sirenians and 

proboscideans are two of only four extant orders that share 

a common ancestor among them, manatees are often 

compared to elephants using the ultimate evolution 

perspective [NOTE: The other two orders contain the 

hyraxes and the aardvarks, which are rarely compared to 

manatees in the literature]. Another promiscuous aspect of 

the manatee mating system is scramble-polygyny, where 

multiple males attempt to mate with the estrous female, but 

- without overt competition. Although males aggregate on 

the estrous female and jockey for the best position - they 

exhibit little agonistic behavior. Interestingly, male 

dugongs appear to be more agonistic during mating events. 

They set up territories and exhibit lek mating behaviors 

(Anderson 1997). What perspective would we use to 

compare mating strategies between manatees and dugongs? 

Timing: Let's assume that our observation was of a 

mating herd. That is, the group of manatees in the center 

of the cove consisted of 1 estrous female and 3 males. 

Why was the first manatee, the one originally sighted in the 

resting hole, not involved in the mating herd? Looking at 

the situation from a proximate perspective, there are 

several possibilities, and all involve timing. Suppose the 

resting manatee was a female. If she was sexually mature, 

but not in estrous, the mating herd would have no interest 

as she would not be producing an estrous signal. An 

estrous signal is the proximate cause of the mating herd 

behavior. It's "how" the males know the female is ready to 

conceive. Similarly, if the female were sexually immature, 

she could not be in estrous and therefore would not be 

sending a signal. Scientists have only recently answered 

the question of when a female manatee becomes sexually 

mature, thanks to the development of a new aging technique 

by Miriam Marmontel, et al. (1990). Since manatees 

continuously regenerate new teeth throughout their lives 

(Domning and Hayek 1984), they cannot be aged by their 

dentition like many other marine mammals. But, by 

looking at growth layers in manatee ear bones, we are now 

reasonably confident that female manatees in Florida reach 

sexual maturity between the age of 3 and 4 years - most 

giving birth to their first calf at age 4 (Marmontel 1995). 

Questions of "how" the behavior of signaling develops in 

females as they mature fall under the proximate 

development perspective. 

On the other hand, if the resting manatee was a 

male, why wasn't he attracted to the estrous female in the 

middle of the cove? He could have been either sexually 

immature or sexually inactive. Using the presence or 

absence of sperm in the testes as an indicator, Hernandez et 

al. (1995) found that sexual maturity (proximate 

development) varied among Florida male manatees with 

5 

both size and age with some males becoming 

physiologically mature as young as 2 years and as small as 

237 cm. But, from a proximate cause perspective, they 

also found that the reproductive system varied in 

functionality among mature male manatees depending on 

season in Florida, with little evidence of spermatogenesis 

present during winter months (December – February). In 

many mammals, reproductive activity varies seasonally 

with photoperiod, or the number of light hours per day. 

The pineal gland is usually the organ associated with 

behavioral changes affected by photoperiod. However, no 

pineal gland has ever been found in manatees or dugongs 

(Ralph et al. 1985, W. Welker personal communication 

2000). From an ultimate evolution perspective, it is 

interesting that the literature is unclear regarding the 

existence of a pineal gland in elephants (Ralph et al. 1985). 

Whether the resting manatee was inactive or 

immature, his timing would have been out of sync with the 

female and the estrous signal would have no effect on his 

behavior. From an ultimate function perspective, we say 

that those manatees whose sexual behavior is triggered at 

the appropriate time (i.e. when both the male and female are 

sexually mature, active, and receptive) are more 

reproductively successful than manatees that waste energy 

on futile sexual encounters. From an ultimate evolution 

perspective, there have been some behaviors observed in 

Antillean manatees that might be associated with seasonal 

spermatogenesis (G. Smith unpublished data). More 

studies are necessary before we can determine if seasonality 

affects the reproductive behavior of manatees in Belize. 

Parental Care: The final aspect of reproductive 

problem solving discussed here is parental care. Like many 

mammals, female manatees invest considerable time and 

energy into a relatively small number of offspring as their 

reproductive strategy. From an ultimate function 

perspective, data collected by scientists in Florida suggest 

that those females that invest 2 years of parental care in 

each offspring prior to becoming pregnant again are more 

successful than other females (Marmontel 1995). Although 

calves begin eating on their own within 3 months of birth, 

they continue to nurse periodically (Hartman 1979) as they 

grow and learn migration routes from their mothers (R. 

Bonde, personal communication 1999). When we ask 

"why" this behavior exists, we are asking ultimate function 

questions. Perhaps calves need the extra protein and fat 

provided by mother's milk during developmental years. Or, 

perhaps it takes calves almost two years to learn the routes 

to warm water effluents and good foraging grounds 

necessary for survival through the temperate winters in 

northern and central Florida. 

In an ongoing study of Antillean manatees in the 

Southern Lagoon of Belize, Buddy Powell is also seeing 

mother-calf pairs remain together for long periods of time 

(www.wesave.org/manatee/). When we compare this 

behavior between the Florida and Antillean subspecies, we 

are using the ultimate evolutionary perspective. On the 

other hand, "how" the mother-calf pair remains together

during this period is a proximate cause question. It 

appears that calves remain in close association with their 

mothers via vocalizations (Hartman 1979; Reynolds 1981; 

Bengtson and Fitzgerald 1985; personal observations). 

Although manatees usually have only one calf at a 

time, there are rare occurrences of manatees giving birth to 

twins (Hartman 1979; O'Shea and Hartley 1995; Rathbun et 

al. 1995). Twinning is often followed by the death of one 

(O'Shea and Hartley 1995) or both (L. Lefebvre, personal 

communication; personal observation) offspring. From an 

ultimate function perspective, this alternative behavior 

raises the questions (1)"why" aren't females that have twins 

more successful than those that have singles?" and (2) "why 

has the variation (single vs. twins) in birthing behavior 

persisted within the West Indian manatee?" From an 

ultimate evolution perspective, the variation could be 

studied by looking at closely related species. 

Unfortunately, there are little data available on the 

occurrence of twins within other manatee species, but 

Marsh (1995) references vague reports of twin fetuses in 

dugongs. This is one line of evidence that twinning is a 

characteristic shared with other sirenians and not recently 

derived within the Florida population. 

Before we leave parental care, we should ask, "could 

the observation described in the introduction have been a 

manatee father caring for his offspring?" Probably not, 

there is no evidence that male manatees participate in any 

form of parental care. A better hypothesis, based on what 

we now know about manatee reproductive behavior, is that 

perhaps the large male was attracted to little female because 

she was sending an estrous signal. 

Summary: We have learned much about Florida 

manatee reproductive strategies over the past three decades. 

Studies on free-ranging manatee populations at warm 

water effluents and data collected from carcasses through 

the salvage network agree on many life history traits 

(O’Shea et al. 1995). Female manatees appear to reach 

sexual maturity at age 3, producing their first calf at age 4. 

Single births are the norm with rare cases of twins. More 

twins are reported in carcasses than observed in live 

manatees, leading to the assumption that uniparity is the 

more successful behavior. Gestation is about 1 year and 

calves stay with their mothers for about 2 years, making the 

minimum interval between successful reproductions about 3 

years. However, females who abort fetuses or lose a young 

calf may reproduce again sooner. Florida males exhibit 

seasonal spermatogenesis, which correlates with seasonal 

observations of females with neonate calves. 

PHYSICAL PROBLEM-SOLVING 

Sirenians (manatees and dugongs) belong to group 

of animals commonly referred to as marine mammals. 

Other marine mammals include whales and dolphins; seals, 

sea lions, and walruses; sea otters; and polar bears. 

Although they are not closely related to each other 

(remember, manatees are more closely related to elephants 

than to other marine mammals), these groups share 

6 

convergent characteristics that evolved as they solved the 

physical problems associated with adaptation from a 

terrestrial to a marine environment. For example, all 

marine mammals must breathe air, and they have evolved in 

various ways that enable them to survive in an aquatic 

environment. In the dolphins, nostrils have migrated up the 

rostrum to the top of the head and become a single 

blowhole. Many large whales and seals have physiological 

adaptations that enable them to remain underwater for hours 

at a time. 

From an ultimate evolutionary perspective, one 

interesting hypothesis is that the common ancestor between 

manatees and elephants was an aquatic (rather than a 

terrestrial) mammal. If true, this would make the elephant 

the only known animal to move from the sea to the land (as 

all mammal ancestors did when their remote ancestors 

evolved from fish to amphibians), back to the sea (as did 

the cetaceans, pinnipeds, and sirenians) and then back to 

the land again. This idea was originally based on the 

thought that the elephant's trunk evolved to enable the 

negatively buoyant animal to breath air from beneath the 

surface of the water. The longer the proboscis, the deeper 

the animal could forage - eventually resulting in the long, 

snorkel-like trunk we see today. This hypothesis has 

recently been supported by a study on elephant embryos, 

which indicates that the shared ancestor between sirenians 

and elephants was an aquatic mammal (Gaeth et al. 1999). 

All marine mammals have had to solve the problem 

of breathing in an aquatic environment, but the sirenians 

have additional unique physical problems: (1) the extant 

species are NOT well adapted to cold water; and (2) 

sirenians are the only marine mammal herbivores. Only 

one extinct species of sirenian was found in extreme cold 

waters: Hydrodamalis gigas, commonly known as Steller's 

giant sea cow. These animals were three times as large as 

manatees, ranging from 25 to 35 feet in length and 

weighing up to 8000 pounds. Their extremely large size 

enabled them to survive in the frigid Bering Sea where they 

feed on giant kelp. All extant species of sirenians are 

limited to tropical and sub-tropical waters year round; some 

individuals migrate into temperate areas during the 

summer. As herbivores, all sirenians are limited to 

shallow coastal waters, estuaries, and rivers where aquatic 

vegetation is abundant. The West Indian manatee inhabits 

riverine and marine systems from Florida to Brazil. But 

their distribution is patchy, and appears to be a function of 

physical problem solving such as thermoregulation, 

foraging, predator avoidance (Hartman 1979), and 

osmoregulation. These are the problems we will focus on 

here. 

Thermoregulation: Water temperature is well 

known to be a controlling factor in Florida manatee 

distribution in the United States (Hartman 1979, Irvin 

1983). Rarely, manatees have been sighted in North 

Carolina (Schwartz 1995); they are routinely sighted in 

South Carolina and Georgia; but the Chesapeake Bay has 

always been considered north of any expected range - even

in the summer. Chessie, a male Florida Manatee, earned 

his name by showing up in the Chesapeake Bay during the 

summer of 1994. Sirenian biologists agreed that Chessie 

would die from the cold of oncoming winter if he remained 

in the Bay, so they flew him back to Florida, put a satellite 

transmitter tag on him and let him go. When the water 

began to warm the next summer, Chessie headed north 

again. Not only did he temporarily enter the Chesapeake 

Bay, but when he came out, he continued his northern 

journey up the Atlantic seaboard. Upon reaching Port 

Judith, Rhode Island, he finally reversed direction and 

began working his way back to Florida for the winter! 

[NOTE: For more details go to 

www.sirenian.org/chessie.html] 

Each winter, hundreds of West Indian manatees 

aggregate in Crystal River, Florida, where they are soon 

joined by thousands of humans who want to swim with 

them. Why does the otherwise elusive manatee tolerate this 

human behavior? Why do they keep coming back, year 

after year? 

These are excellent examples of how manatees have 

adapted behaviors to solve the physical problem of 

thermoregulation. While most marine mammals have 

adapted to cold water by evolving high metabolic rates, the 

West Indian manatees have exceptionally low metabolic 

rates (Irvin 1983). When metabolic rates are graphed 

against body size, most mammals fall along a predictable 

curve where the rate decreases as the size increases. If we 

compare where manatees should fall on this curve to where 

they actually plot out on the graph, we find that manatee 

metabolism is only about 20% of what we would expect. 

The same comparison with other marine mammals shows 

that their metabolic rates are almost twice what we would 

expect - enabling them to easily live in cold water. This 

physiological problem should limit the West Indian 

manatee to warm tropical waters. 

In the United States, however, the Florida 

subspecies thermoregulates behaviorally by migrating to 

both natural and artificial warm water effluents during the 

winter months, enabling them to extend their habitat range. 

From a proximate cause perspective, the migration 

behavior is triggered when the water temperature drops 

below 20 degrees Celsius (Hartman 1979; Irvin 1983). But, 

from a proximate development perspective, how do adult 

manatees know where to find warm water effluents? We 

touched on this earlier, when we talked about why manatee 

calves remain dependent on their mothers for up to 2 years. 

Long term studies of radio tagged females with calves 

indicate that manatees initially learn migration routes from 

their mothers during the extended parental care period (R. 

Bonde, personal communication). Because of this learned 

behavior, interruption of man-made thermal effluents may 

have negative impacts on manatee survival in areas where 

no natural warm water effluents are nearby (Packard et al. 

1989). 

What about manatees in tropical habitats where 

water temperatures are relatively constant? If 

7 

thermoregulation were the only function of long distance 

travel, we would not expect Antillean manatees to exhibit 

the same degree of seasonal migration as Florida manatees. 

Buddy Powell (personal communication 2000) is working 

on that ultimate evolution question through telemetry 

studies of Antillean manatees in Belize (see Satellite 

Tracking of W.I. Manatees in Belize 

www.wesave.org/manatee/). After almost two years of 

data, it appears that several manatee mother-calf pairs 

remain in the Southern Lagoon area year round. On the 

other hand, Greg Smith (personal communication) finds 

male manatees seasonally absent on the reef at Basil Jones, 

Ambergris Caye, during the winter months of December - 

February. In my limited personal observations, I have not 

observed manatees on the reef at Gallows Point Reef, near 

Belize City, from November through April; but they were 

there daily in July and August 1999. Temperature changes 

between summer and winter on Gallows Reef vary from 

about 28 – 32 degrees Celsius (unpublished data), well 

above the 20 degree trigger found in Florida manatees. If 

temperature is not driving this apparent seasonal migration, 

what other factors could be the cause? Greg Smith 

hypothesizes that it is driven by seasonal reproductive 

cycles. Perhaps the males "hang out" at the reef during the 

summer months looking for an estrous female (see 

previous section on reproductive problem solving). More 

data are required before we can answer these questions. 

Foraging: As we explored the bogues (channels) 

that snake their way through the mangrove islands off the 

coast of Belize, it became apparent that Antillean manatees 

preferred certain micro-habitats within the larger habitat 

we call the Drowned Cayes. We reliably found manatees 

just west of the cayes feeding on turtle grass beds; and we 

always found manatees resting in narrow bogues or quiet 

coves among the cayes. They tended to travel in the deeper 

channels when moving between areas. One of the 

parameters of quality manatee habitat is the close 

availability of food (Hartman 1979). It appears that 

Antillean manatees using the Drowned Cayes are more 

likely to rest in areas that are linked to turtle grass beds by 

deep channels. Like all sirenians, manatees are 

opportunistic herbivores, feeding on a variety of fresh and 

saltwater vegetation. Although they may consume fish in 

some areas (Powell 1978) and incidentally ingest 

invertebrates (Powell 1978; Powell 1984; personal 

observations), the main component of their diet is aquatic 

vegetation: sea grasses in the marine and estuarine 

environment; floating, submerged, and emergent plants in 

the riverine environment. Sea grasses, like all plants, 

require sunlight for growth, which limits their presence to 

relatively shallow coastal waters. From an ultimate 

function perspective, the relationship between sea grasses 

and water depth has probably prevented manatees from 

dispersing into deeper oceanic waters. 

I snorkeled up to an Antillean manatee feeding 

underwater just west of Swallow Caye – at first, I thought it 

was dead... I can still recall the adrenalin rush as options

flashed through my mind regarding what to do with a dead 

manatee! It was lying perfectly still on the bottom in about 

3 meters of water and appeared to be missing its head. As I 

floated closer, (heart racing) I began to hear chewing 

noises and realized that the manatee had buried its head 

into the muddy substrate and was feeding on the sea grass 

roots. I soon learned that this is typical of how manatees 

feed on the sea grass beds near the Drowned Cayes - eating 

both roots and leaves and probably other benthic organisms 

living in the mud. Looking for muddy disturbances became 

another method of finding the elusive manatee. 

If you’ve ever tried to dive down and recover a lost 

item in deep water, you know that you, like most mammals, 

are positively buoyant and must work to get and stay 

submerged. Manatee bones are pachyostoic -- very dense 

and lacking marrow -- except in the vertebrae and sternum 

(Odell and Reynolds 1991). Because of this, manatees are 

negatively buoyant and can lie on the sea bottom without 

exerting any energy to stay down. The less energy they 

use, the longer manatees can remain submerged between 

breaths - making feeding more efficient. Indeed, we think 

manatees have the ability to control the volume of air their 

lungs, enabling them to rise to the surface, take a breath, 

and return to the bottom with no noticeable effort. 

Manatees exhibit different problem-solving 

behaviors related to foraging in different habitats. In rivers, 

manatees are often observed feeding on floating vegetation. 

They use their forelimbs like we use our hands to 

manipulate aquatic plants towards the mouth. The large 

prehensile upper lip is then used to work the plants into the 

mouth. When I was observing Georgia and Peaches in 

Florida, I was fascinated to see Georgia reach her head out 

of the water to feed on plants growing along the shoreline 

of the Hontoon Dead River. At times it looked as if she 

was going to climb out onto the bank! In fact, Florida 

manatees feeding on grasses have been sighted with up to 

one third of their body awash (Powell 1984). 

Although they are considered opportunistic feeders, 

manatees are known to prefer certain species of plants to 

others (Bengtson 1981). Hunters of West African manatees 

use cassava to lure the animals into box traps (O’Shea 

1994). Other traditional hunters attract manatees by 

dangling a favorite flower over the water's edge to entice 

their approach. While West Indian manatees in Florida and 

Belize feed on a variety of vegetation including floating, 

submergent, emergent, and over-hanging vegetation, the 

Amazonian and the West African manatees feed primarily 

on surface vegetation. 

In Gambia, when feeding on overhanging 

vegetation, West African manatees grasp the leaves of 

branches with their lip pads near the water's surface (Powell 

1984). They pull the branch into the water; use their 

forelimbs to hold it down; and then eat the leaves - but not 

the woody petiole or branches. They appear to prefer the 

young leaves and shoots of mangroves, as they are known 

to return to areas where they have previously fed to crop 

any new growth. Amazonian manatees face an even more 

8 

challenging problem. During the rainy season, floodwaters 

allow manatees to literally "forage among the tree tops", but 

in the dry season, they are often confined to isolated lakes 

and pools devoid of any vegetation. Robin Best calculated 

that Amazonian manatees could fast for up to seven months 

a year - surviving on stored fat reserves they build up 

during the rainy season (O'Shea 1994). 

Daryl Domning of Howard University describes 

morphological variation in the rostrum deflection among 

manatee species and subspecies and suggests that the 

variation results from differential foraging behavior among 

sirenian species (1980). For example, the rostral deflection 

in both the Amazonian and the West African species is 

relatively less than it is in the West Indian manatee. These 

comparisons of foraging behavior and rostral deflection 

represent ultimate perspectives. Comparing foraging 

behaviors among the species is an example of ultimate 

evolution. Hypothesizing about why the rostral deflection 

varies among species (because of different foraging 

behaviors) is an example of ultimate function. From an 

ultimate perspective, it is interesting to compare the 

foraging behavior of manatees to the dugongs. Dugongs 

forage exclusively on submerged marine sea grasses and 

their rostra are significantly deflected downward when 

compared to manatees. The divergence in foraging 

behavior between the two families of Sirenia may be due to 

the evolution of true grasses in the Caribbean and 

continuously regenerating teeth in manatees. Unique to the 

Trichechus genus, is the fact that manatees generate new 

molars throughout their lifespan (Domning and Hayek 

1984). As older molars are worn down from the abrasive 

silica content in true grasses, new molars gradually move 

forward at the rate of a few millimeters per month. The 

forward most molars eventually fall out and are replaced 

from the rear in a horizontal manner. This would be 

analogous to humans continuously generating new wisdom 

teeth at the rate of four - 2 lower and 2 upper - every few 

months! Daryl Domning (1982) convincingly argues that 

this trait enabled manatees to out compete dugongs in the 

Atlantic a few million years ago. While manatees are only 

found in the Atlantic and continue to forage on a variety of 

vegetation, dugongs are only found in the Indo-Pacific and 

forage exclusively on marine sea grasses. 

Predation: Although they may have existed in the past, we 

know of few natural predators on modern West Indian 

manatees...EXCEPT for humans. Large aquatic predators 

(crocodiles, alligators, sharks, and hippopotamus) have 

been hypothesized to take the occasional small or weak 

animal (Odell 1982; Powell 1984). But, in one of the few 

documented cases, Johnson (1937, as reported in Powell 

1984) found that only one out of one hundred crocodiles cut 

open contained the remains of a manatee. 

Amazonian manatees, on the other hand, still have to 

contend with predation by aquatic and terrestrial carnivores 

such as jaguars, caimans, and sharks (Reynolds and Odell 

1991) – especially during the dry season when then are 

stranded by receding flood waters. Both fossil and historical

ecords indicate that manatees have been hunted both for 

subsistence and commercially throughout the history of 

humans (Lefebvre et al. 1989, Reynolds and Odell 1991). 

While illegal poaching still exists – especially in remote 

areas -- most modern predation is incidental – resulting 

from entanglement in fishing gear, shark nets, and water 

control devices, and from collisions with watercraft. From 

an ultimate function perspective, we may hypothesize that 

the reason manatees are elusive creatures is to avoid 

predation. In other words, those animals that inherited a 

natural tendency towards elusive behavior were more 

reproductively successful. 

The story of Steller’s sea cow demonstrates how 

quickly humans can extirpate a species, particularly when 

population numbers are already reduced. The sea cow was 

discovered and described by Georg Wilhelm Steller, a 

German naturalist assigned to Captain Vitus Bering during 

a Russian Expedition to Alaska (Steller 1988). This giant 

sirenian was 25-35 feet long and weighed ~8000 pounds 

with flukes than spanned 8 feet. Unlike modern sirenians, 

it lived in extremely cold waters in the North Pacific. It had 

no teeth, but two grooved plates - one upper and one lower 

with which it crunched giant sea kelp. During the summer 

of 1741, Captain Bering set sail from Kamchatka in NE 

Russia with 2 ships, the St. Peter and the St. Paul. During 

the voyage, a storm separated his ships; Bering, Steller, and 

the crew of the St. Peter were shipwrecked on an unknown 

island (later named Bering Island). Although Bering did 

not survive the winter, Steller and many of the crew did. In 

his book, A Voyage with Bering, Steller credits their 

survival to the giant sea cow. Only after the crew learned 

to hunt the sea cow did they begin to regain the strength to 

repair their ship. When they returned to Kamchatka in the 

summer of 1742, they told of the wonderful sea cow meat. 

New hunting expeditions were formed almost immediately 

and every year thereafter. The expeditions would return to 

Bering Island where they spent 8-9 months hunting furanimals 

and eating sea cow meat to survive. Indeed, many 

of the expeditions are reported to have wintered on Bering 

Island for the express purpose of collecting sea cow meat to 

provision their ships for the rest of their 3-4 year voyage to 

America. As a result, the last sea cow was reported killed 

in 1768, only 27 years after modern humans had discovered 

the island and the species. 

Even before Russian sailors were hunting Steller’s 

sea cow to extinction, European buccaneers and explorers 

were provisioning their ships with Antillean manatee meat, 

which they harvested themselves or purchased from the 

indigenous people (Reynolds and Odell 1991). In the 

Panama area, it is estimated that at one time, 7-8 thousand 

manatees were being harvested annually. The Amazonian 

manatee continued to be commercially harvested for it's 

tough skin (which was made into leather products) into the 

1950's. From an ultimate function perspective, it stands to 

reason that manatees that behaved in an elusive manner 

lived to produce more offspring during the last several 

centuries. 

9 

The greatest documented predation on manatees 

today occurs incidentally in Florida due to competition for 

space between manatees and humans. Government 

agencies have been documenting manatee mortality in 

Florida for almost three decades. The proportion of deaths 

related to collisions with watercraft tends to increase each 

year as more and more people move to Florida. For current 

statistics on Florida manatee mortality, visit the FMRI and 

FFWCC websites at www.fmri.usf.edu/manatees.htm and 

www.state.fl.us/fwc/psm/manatee/manatee.htm. Even the 

most elusive manatee has a difficult time avoiding 

interaction with people as the human population and 

development continue to grow. 

Osmoregulation: Unlike the Amazonian manatee, 

which is endemic to the fresh waters of the Amazon River 

basin, and the dugong, which is only found in marine 

habitats, the West Indian and West African manatees 

appear to move freely between fresh and marine 

environments. Although the Florida subspecies is usually 

associated with fresh or brackish water, it is occasionally 

found far offshore in high salinity water (Reynolds and 

Ferguson 1984). Large amounts of barnacle growth suggest 

that some individuals spend prolonged periods in marine 

environments (Husar 1977, Hartman 1979). Antillean 

manatees are found year round in totally marine 

environment of red mangrove islands in Belize (personal 

observation). How does this species osmoregulate as it 

moves among fresh, brackish, and saltwater? Two 

alternative hypotheses come to mind: (1) West Indian 

manatees have physiological adaptations that enable them 

to maintain water balance and/or (2) W. I. Manatees 

behaviorally maintain water balance by seeking out fresh 

water sources in marine environments. Graham Worthy, a 

physiologist at Texas A&M University, and his students are 

working on this and proximate cause questions involving 

physiology. Preliminary results indicate that W. I. 

Manatees are “good osmoregulators regardless of the 

environment” (Ortiz et al. 1998). 

A FEW THOUGHTS… 

As we examine problem-solving behavior in the 

West Indian manatee using the ethological perspectives of 

cause, development, evolution, and function, we begin to 

realize how many questions remain un-answered about this 

elusive marine mammal. Although we know (from the 

study of other mammals) that the proximate cause of 

behavior is a complex interaction between internal 

mechanisms and external stimuli, we don't know the 

specific triggers for many manatee behaviors. Proximate 

development has not been well studied for several reasons. 

Free ranging female manatees with new calves tend to 

isolate themselves in secluded areas making behavior 

difficult to observe. Observations of captive raised 

manatees may not be indicative of normal development. 

The West Indian manatee is an endangered species making 

experimental manipulation difficult, yet extremely 

important to the successful rehabilitation and release of

injured manatees. For example, how will a captive raised 

calf learn to find warm water effluents during cold spells? 

Can adult manatees learn successful migration routes or 

must they be learned during early development? From an 

ultimate perspective, manatees are also quite challenging 

due to the lack of closely related extant species and to the 

sparse fossil record. But, paleo-sirenian research by Daryl 

Domning, and others, continues to offer insight to the 

evolution and function of modern manatee behaviors. 

Why are there fewer sirenian species today than during the 

past? Does the evolution of the species Homo correlate 

with the decline of sirenians or were other environmental 

factors the reason for their extinctions? Will answers to 

these and other ultimate questions aid in our conservation 

efforts? 

Although manatees are generally considered elusive, 

there are cases where they appear to be curious and actually 

initiate contact with humans. Likewise, many behaviors 

tend vary between individuals, populations, and species. 

Because of the variable nature of manatee behavior, we 

must be careful in applying what we know about the Florida 

population to other areas. The Florida subspecies is 

fortunate to have the efforts of many US citizens and 

agencies working toward conservation issues and manatee 

behavior plays and important role in making management 

decisions in Florida. However, West Indian manatees are 

considered endangered throughout their range. Continued 

research effort on populations in the more tropical regions 

of the Caribbean is necessary for decision makers in those 

countries to make effective management decisions. 

REFERENCES 

Alcock, John. 1998. Animal Behavior. Sixth edition. 

Sunderland, Massachusetts: Sinauer Associates, 

Inc. 640 pp. 

Anderson, Paul K. 1997. Shark Bay dugongs in summer. I: 

Lek mating. Behaviour. 134(5-6):433-462. 

Auil, Nicole. 1998. Belize Manatee Recovery Plan. 

UNDP/GEF Coastal Zone Management Project, 

BZE/92/G31, Belize/UNEP Caribbean 

Environment Programme, Kingston, Jamaica. 67 

pp. 

Bengtson, John L. 1981. Ecology of Manatees Trichechus 

manatus) in the St. Johns River, Florida. Ph. D. 

thesis. University of Minnesota. 

Bengtson, John L., and Shannon M. Fitzgerald. 1985. 

Potential role of vocalizations in West Indian 

manatees. Journal of Mammalogy. 66(4):816- 

819. 

Domning, Daryl P. 1980. Feeding position preference in 

manatees (Trichechus). Journal of Mammalogy 

61(3):544-547. 

Domning, Daryl P. 1982. Evolution of manatees: a 

speculative history. Journal of Paleontology. 

56(3):599-619. 

10 

Domning, Daryl P., and Lee-Ann Hayek. 1984. Horizontal 

tooth replacement in the Amazonian manatee. 

Mammalia 48:105-127. 

Drickamer, Lee C., Stephen H. Vessey, and Doug Meikle. 

1996. Animal Behavior: Mechanisms, Ecology, 

Evolution. Fourth edition. Boston: William C. 

Brown Publishers. 447 pp. 

Fischer, M. S. 1990. The unique ear of elephants and 

manatees (Mammalia): a phylogenetic paradox. 

C. R. Acad. Sci., Paris, SER. III, vol. 31, no. 4, pp. 

157-162. 

Gaeth, A. P., R. V. Short and M. B. Renfree. 1999. The 

developing renal, reproductive, and respiratory 

systems of the Africa elephant suggest an aquatic 

ancestry. Proceedings of the National Academy of 

Sciences of the United States of America 

96(10):5555-5558. 

Hartman, Daniel S. 1979. Ecology and behavior of the 

manatee (Trichechus manatus) in Florida. Special 

publication no. 5. American Society of 

Mammalogists. 153 pp. ISBN 0-9436-1204-7. 

Hernandez, Patricia, John E. Reynolds, III, Helene Marsh, 

and Miriam Marmontel. 1995. Age and 

seasonality in spermatogenesis of Florida 

manatees. pp. 84-95 in Thomas J. O'Shea, Bruce 

B. Ackerman, and H. Franklin Percival, editors. 

Population biology of the Florida manatee. 

National Biological Service Information and 

Technology Report 1. 

Husar, Sandra L. 1977. The West Indian manatee 

Trichechus manatus. Wildlife Research Report 

No. 7. U. S. Department of the Interior, Fish and 

Wildlife Service, Washington, D.C. 22 pp. 

Irvin, A. Blair. 1983. Manatee metabolism and its 

influence on distribution in Florida. Biological 

Conservation. 25:315-334. 

Koelsch, Jessica K. 1997. The Seasonal Occurrence and 

Ecology of Florida Manatees (Trichechus manatus 

latirostris) in Coastal Waters near Sarasota, 

Florida. Masters thesis. University of South 

Florida. Tampa, Florida. 

Lefebvre, Lynn W., Thomas J. O'Shea, Galen B. Rathbun, 

and R. C. Best. 1989. Distribution, status, and 

biogeography of the West Indian manatee. pp. 

567-610 in Biogeography of the West Indies. ed. 

Charles A. Woods. Gainesville, FL: Sandhill 

Crane Press. ISBN 0-8493-2001-1. 

Lehner, Philip N. 1996. Handbook of Ethological 

Methods, 2 nd edition. Cambridge University Press. 

672 pp. 

Maluf, N. S. R. 1995. Kidney of elephants. Anatomical 

Record 242(4):491-514. 

Marmontel, Miriam. 1995. Age and reproduction in 

female Florida manatees. Pages 98-119 in Thomas 

J. O'Shea, Bruce B. Ackerman, and H. Franklin 

Percival, editors. Population biology of the

Florida manatee. National Biological Service 

Information and Technology Report 1. 

Marmontel, Miriam, Thomas J. O'Shea, and S.R. 

Humphrey. 1990. An evaluation of bone growthlayer 

counts as an age determination technique in 

Florida manatees. National Technical Information 

Service, Springfield, Va. Document PB 91- 

103564. 104 pp. 

Marsh, Helene. 1995. The life history, pattern of breeding, 

and population dynamics of the dugong. pp. 75- 

83 in Thomas J. O'Shea, Bruce B. Ackerman, and 

H. Franklin Percival, editors. Population 

biology of the Florida manatee. National 

Biological Service Information and Technology 

Report 1. 

Martin, Paul, and Patrick Bateson. 1993. Measuring 

Behaviour – An introductory guide, 2 nd edition. 

Cambridge University Press. 222 pp. 

Odell, Daniel K. 1982. West Indian Manatee Trichechus 

manatus. in Wild Mammals of North America 

Biology, Management, and Economics. Joseph A. 

Chapman and George A. Feldhamer, editors. The 

Johns Hopkins University Press. Baltimore and 

London. 

O'Shea, Thomas J. 1994. Manatees. Scientific American. 

July 1994. 

O'Shea, Thomas J. Bruce B. Ackerman, and H. Franklin 

Percival. 1995. Population Biology of the 

Florida manatee. National Biological Service 

Information and Technology Report 1. 

O’Shea, Thomas J., and Wayne Hartley. 1995. 

Reproduction and early-age survival of manatees 

at Blue Spring, upper St. Johns River, Florida. pp. 

157-170 in Thomas J. O'Shea, Bruce B. 

Ackerman, and H. Franklin Percival, editors. 

Population biology of the Florida manatee. 


Technology Report 1. 

O'Shea, Thomas J. and Charles A. 'Lex' Salisbury. 1991. 

Belize - a last stronghold for manatees in the 

Caribbean. Oryx. 25(3): 156-164. 

Ortiz, Rudy M., Graham A. J. Worthy and Duncan S. 

MacKenzie. 1998. Osmoregulation in wild and 

captive West Indian manatees (Trichechus 

manatus). Physiological Zoology 71(4):449.457. 

Packard, Jane M., R. Kipp Frohlich, John E. Reynolds, III, 

and J. Ross Wilcox. 1989. Manatee response to 

interruption of a thermal effluent. Journal of 

Wildlife Management 53(3):692-700. 

Powell, James A. 1978. Evidence of carnivory in manatees 

(Trichechus manatus). Journal of Mammalogy. 

59(2):442. 

Powell, James A. 1984. Manatees in the Gambia River 

Basin and potential impact of the Balingho 

Antisalt Dam with notes on Ivory Coast, West 

Africa. Trip Report. Institute for Marine Studies. 

11 

University of Washington. Seattle Washington 

98195. 

Ralph, C. L., S. Young, R. Gettinger and T. J. O’Shea. 

1985. Does the manatee have a pineal body? 

Acta Zoologica 66(1):55-60. 

Rathbun, Galen B., James P. Reid, Robert K. Bonde, and 

James A. Powell. 1995. Reproduction in freeranging 

Florida manatees. pp. 135-156 in T.J. 

O'Shea, B.B. Ackerman, and H.F. Percival, 

editors. Population biology of the Florida 

manatee. National Biological Service Information 

and Technology Report 1. 

Reynolds, John E., III. 1981. Aspects of the social 

behaviour and herd structure of a semi-isolated 

colony of West Indian manatees, Trichechus 

manatus. Mammalia. 45(4):431-451. 

Reynolds, John E., III, and John C. Ferguson. 1984. 

Implications of the presence of manatees 

(Trichechus manatus) near the Dry Tortugas 

islands. Florida Scientist 47(3):187-189. 

Reynolds, John E. III, and Daniel K. Odell. 1991. 

Manatees and Dugongs. New York: Facts on File, 

Inc. 192 pp. ISBN 0-8160-2436-7. 

Schwartz, F. J. 1995. Florida manatees, Trichechus 

manatus (Sirenia: Trichechidae) in North Carolina 

1919-1994. Brimleyana 22:53-60. 

Springer, M. S., G. C. Cleven, O. Madsen, W. W. De Jong, 

V. G. Waddell, H. M. Amrine, M. J. Stanhope. 

1997. Endemic African mammals shake the 

phylogenetic tree. Nature (London) 388 

(6637):61-64. 

Steller, Georg Wilhem. 1988. Journal of a Voyage with 

Bering 1741-1742. Stanford, California: Stanford 

University Press. 252 pp. 

Stejneger, Leonhard. 1887. How the great northern seacow 

(Rytina) became exterminated. The American 

Naturalist 21(12):1047-1054. 

RECOMMENDED READING 

Caldwell, David K., and Melba C. Caldwell. 1985. 

Manatees - Trichechus manatus, Trichechus 

senegalensis, and Trichechus inunguis. pp. 33-36 

in Handbook of Marine Mammals, vol. 3, The 

Sirenians and Baleen Whales. eds. S. H. 

Ridgway and R. J. Harrison. London: Academic 

Press. ISBN 0-1258-8503-2. 

Hartman, Daniel S. 1979. Ecology and behavior of the 


Publication no. 5. American Society of 

Mammalogists. 153 pp. ISBN 0-9436-1204-7. 

Reynolds, John E. III, and Daniel K. Odell. 1991. 

Manatees and Dugongs. New York: Facts on File, 

Inc. 192 pp. ISBN 0-8160-2436-7.

Zeiller, Warren. 1992. Introducing the Manatee. 

Gainesville, Florida: University Press of Florida. 

151 pp. ISBN 0-8130-1152-3. 

World Wide Web Internet URLs: 

Animal Behavior by Dr. Jane M. Packard: 

www.tamu.edu/ethology/ 

Call of the Siren by Caryn Self Sullivan: 

www.sirenian.org/caryn.html 

The Nobel Prize in Physiology or Medicine 1973 – Karl 

von Frisch, Konrad Lorenz, Nikolaas Tinbergen, for their 

discoveries concerning organization and elicitation of 

individual and social behaviour patterns: 

www.nobel.se/medicine/laureates/1973/index.html 

Satellite Tracking West Indian Manatees in Belize: 

www.wesave.org/manatee/ 

Florida Fish and Wildlife Conservation Commission: 

www.state.fl.us/fwc/psm/manatee/manatee.htm 

Florida Marine Research Institute: 

www.fmri.usf.edu/manatees.htm 

USGS Sirenia Project: 

www.fcsc.usgs.gov/sirenia/ 

Sea World Education Department: 

www.seaworld.org/manatee/manatees.html 

Florida Power & Light Company: 

www.dep.state.fl.us/psm/webpages/manatees/booklet.html 

University of Wisconsin - The Brain of the Florida 

Manatee: 

www.neurophys.wisc.edu/manatee/ 

University of Florida - Manatee Research Group: 

www.vetmed.ufl.edu/ufmrg/manatee/ 

GLOSSARY 

agonistic: a general term that includes aggressive, 

submissive, and defensive behaviors that appear when the 

adrenal hormones are activated. 

anecdote: a short story or observation which has not been 

"tested" by the scientific method. 

anthropocentric: considering human beings as the most 

significant entity of the universe; interpreting or regarding 

the world in terms of human values and experiences. 

anthropogenic: of, relating to, or resulting from the 

influence of human beings on nature. 

anthropomorphic: described or thought of as having a 

human form or human attributes; ascribing human 

characteristics to nonhuman things. 

bogue: the local term for a channel of water that flows 

through a mangrove caye in Belize, C.A. 

cause: stimulus outside the animal plus the internal 

physiological state of the animal. 

Cetacea: the order of aquatic mostly marine mammals that 

include the whales, dolphins, porpoises, and related forms 

and that have a torpedo-shaped nearly hairless body, 

paddle-shaped forelimbs but no hind limbs, one or two 

nares opening externally at the top of the head, and a 

horizontally flattened tail used for locomotion. 

convergent: similar traits in species from very different 

genetic lineages, due to similar environmental functions. 

12 

development: changes in behavioral traits as an individual 

ages. 

divergent: different traits in species from similar genetic 

lineages due to differences in their environments. 

endemic: restricted or peculiar to a locality or region. 

Amazonian manatees are only found in the Amazon River 

Basin. 

ephemeral: short period of existence; opposite of eternal. 

estrous: the period during which a female has produced an 

egg ready to fertilize and is receptive to copulation. 

evolution: change in proportion of genotypes within the 

gene pool of a population over many many generations. 

extant: currently or actually existing; not destroyed or lost. 

extinct: no longer existing. 

extirpated: to destroy completely. 

folk psychology: a non-scientific way of talking about 

animal behavior. Uses human terms to describe non-human 

animal behavior. Intuitive – based on anecdotes, 

experiences, observations. Anthropomorphic. Assumes 

that animals have beliefs, feelings, desires. 

function: the meaning of a behavior in terms of survival 

and reproduction in a given environment. 

gestation: the carrying of young in the uterus. 

herbivores: animals that feed exclusively on plants. 

individual: a single organism; a way of understanding the 

biological hierarchy of concepts - those pertaining to 

physiological processes and experiences of each organism; 

in contrast to population, which focuses more on gene 

pools of groups of animals that interbreed. 

lactation: the secretion of milk. 

manatee hole: concave depression in sandy or muddy 

substrate where manatees habitually rest. 

mating herd: the name given an estrous female and the 

aggregation of males which follow her around attempting to 

mate. 

mating system: males strategies and female strategies as 

observed in a population. 

morphology: the form and structure of an organism or any 

of its parts. 

natural selection: the process that produces evolutionary 

changes in a population due to heritable traits in some 

individuals which result in those individuals being more 

reproductively successful; the process only occurs IF (1) 

there are variances in traits within a population, (2) the 

variances are heritable, (3) individuals with certain 

variances have greater reproductive success than 

individuals with other variances, then over time, we would 

expect to see the trait selected "for" become more common 

in the population. 

neonate: term used distinguish a newborn cetacean or 

sirenian calf from an older calf – you can still see the fetal 

folds on a neonate and the skin is usually darker than on an 

older calf. 

osmoregulation: regulation of osmotic pressure especially 

in the body of a living organism. how an organism 

regulates the amount of water entering and leaving its body.

parturition: the action or process of giving birth to 

offspring; birth, whelping. 

pinniped: any of a suborder (Pinnipedia) of aquatic 

carnivorous mammals (as a seal or walrus) with all four 

limbs modified into flippers. 

polyandry: a mating system where one female mates with 

two or more males at a time. (adj: polyandrous) 

population: a group of animals that interact and interbreed. 

postpardum: following parturition; after giving birth. 

prehensile: an appendage adapted for seizing or grasping 

especially by wrapping around - examples: a monkey has a 

prehensile tail and an elephant has a prehensile trunk. 

proboscis: the trunk of an elephant; also any long flexible 

snout; any of various elongated processes of the oral region 

of an invertebrate. 

promiscuity: a mating system where there is no prolonged 

association between the mating pair and at least one sex 

engages in multiple mates. (adj: promiscuous) 

proximate: immediately preceding or following as in a 

chain of events, causes, or effects; in ethology - the 

perspective that looks at the cause and development of 

behavior at the individual animal level. 

13 

scramble-polygyny: a mating system where many males 

try to mate with many females, but without overt 

competition among themselves. 

Sirenia: the taxonomic order of aquatic herbivorous 

mammals including the manatee, dugong, and Steller's sea 

cow. Sirenians are members of the Order Sirenia. 

social animals: tending to form cooperative and 

interdependent relationships with others of one's kind; 

living and breeding in more or less organized communities. 

taxonomy: orderly classification of plants and animals 

according to their presumed natural relationships; the study 

of the general principles of scientific classification; 

systematics. 

thermoregulate: the maintenance or regulation of 

temperature; specifically the maintenance of a particular 

temperature of the living body. 

ultimate: most remote in space or time; last in a 

progression or series; in ethology - the perspectives of 

evolution and function that look at behavior at the 

population and/or species level. 

uniparous: producing one offspring at a time. 

ACKNOWLEDGMENTS 

Financial support for my research on manatees comes from the National Science Foundation Graduate Fellowship 

Program (1998-2001), the Oceanic Society of San Francisco (1998-1999), the Lerner-Gray Fund for Marine Research at the 

American Museum of Natural History (2000), and Earthwatch Institute (2001). A special thank you goes out to all the 

volunteers who have participated in field research with me in Belize. Many sirenian researchers from around the world have 

been quite generous in answering the multitude of questions I asked of them. Special thanks go to Jane Packard and Bill 

Evans of Texas A&M University, Bob Bonde of the USGS Sirenia Project, and Daryl Domning of Howard University, for 

their perpetual availability via email. I thank Nicole Auil of the Belize Coastal Zone Management Institute and Authority; 

Sidney Turton, Elda Cabellos, and the staff of Spanish Bay Resort; Greg Smith of the Belize National Manatee Working 

Group (BNMWG); and Buddy Powell of the Florida Marine Research Institute & the BNMWG for their continuing support. 

Most importantly, I offer an extra special thank you to my primary boat operator, Armando "Patch" Muñoz, for his hours of 

tolerance and patience as we searched for the Elusive Manatee among the Drowned Cayes in Belize. Many others have 

helped me along the way by taking me into the field or assisting me in the field, sharing their personal knowledge and 

experiences, donating slides to my educational programs, directing me towards the proper references, and just by being there 

to listen. In no particular order, they include: Maxine Monsanto, Heidi Petersen, Kate Schafer, Eleno “Landy” Requena, 

Kecia Kerr, Barbara Bilgre, Katie LaCommare, Leszek Karcmarski, Birgit Winning, Jaime Gilardi, Beth Wright, Lenisa 

Tipton, Tami* Gilbertson, Jessica Koelsch, Graham Worthy, Angela Garcia-Rodriguez, Mike Bragg, Edmund Gerstein, Rich 

Harris, Lizz Singh, Chocolate Heredia, Hans Rothauscher, Joe Olson, Patti Thompson, Bruce Ackerman, Cathy Beck, Chip 

Deutsch, Lynn Lefebvre, Tom O'Shea, Tom Pitchford, Roger Reep, Wally Welker, John Reynolds, Butch Rommel, Peter 

Tyack, Andrea Gill, Kevin Andrewin, Elaine Perez, Rob Young, and my extended family of relatives and friends. 

Want to learn more about manatees? Visit my homepage: www.sirenian.org/caryn.html

Aquatic Mammals 2003, 29.3, 342–354 

Seasonal occurrence of male Antillean manatees (Trichechus manatus 

manatus) on the Belize Barrier Reef 

Caryn Self-Sullivan 1,2 , Gregory W. Smith 3 , Jane M. Packard 1,2 and 

Katherine S. LaCommare 2,3 

1 Texas A&M University, Department of Wildlife & Fisheries Sciences, Mail Stop 2258, College Station, 

Texas 77843–2258, USA 

2 Sirenian International, Inc., 200 Stonewall Drive, Fredericksburg, Virginia 22401–2110, USA 

3 P.O. Box 142, San Pedro Town, Belize, Central America 

4 University of Massachusetts-Boston, Department of Biology, Boston, Massachusetts 02125, USA 

Abstract 

A fragment of manatee habitat that crosses the 

border of Belize and Mexico includes both activity 

centres and travel routes linking rivers, lagoons, 

seagrass beds and mangrove islands near Chetumal 

Bay. Little is known about how geophysical 

features like coral reefs may in uence manatee 

movements within and between habitat fragments 

like this. In this inductive study (1995–2001), we 

documented the seasonal occurrence of Antillean 

manatees at breaks in the northern Belize Barrier 

Reef. Survey locations were at: (1) Bacalar Chico 

National Park and Marine Reserve on Ambergris 

Caye (Basil Jones Cut) and (2) breaks in the reef 

70 km south near the Drowned Cayes (Gallows 

Reef). The probability of sighting at least one 

manatee on a 20-min point scan survey was 40% 

(n=382). Sighting probability was signi cantly 

higher during the summer season (May–August) 

compared to winter months (December–March). 

Group size ranged from one to ve manatees, 

peaking earlier (May) at the northern than southern 

site (August). Seventeen identi able individuals 

accounted for 87% of the sightings at Basil Jones 

Cut, with re-sightings within and between years. 

One individual from Basil Jones Cut was re-sighted 

at Gallows Reef. Of the manatees for which sex was 

determined, 100% were males. No calves were 

sighted. To better understand manatee activity 

centres and travel routes, we identi ed potential 

hypotheses relating seasonal in uences, stopover 

sites for travelling males, and habitat connectivity. 

To protect this highly vulnerable species, we recommend 

inclusion of the Belize Barrier Reef as an 

important component of manatee habitat within 

the coastal zone of Belize. 

Key words: Antillean manatee, Trichechus manatus 

manatus, Caribbean, Belize, habitat connectivity, 

? 2003 EAAM 

stopover sites, coastal zone management, Belize 

Barrier Reef, fragmented populations, seasonal 

habitat use. 

Introduction 

A sub-species of the West Indian manatee, the 

Antillean manatee (Trichechus manatus manatus) 

occurs in rivers and coastal marine systems of at 

least 19 countries in the Wider Caribbean Region, 

including the Greater Antilles, Mexico, Central 

America, and South America (CEP/UNEP, 1995; 

Lefebvre et al., 2001). It is listed by the IUCN 

(Hilton-Taylor, 2001) as vulnerable, in continuing 

decline, with severely fragmented populations (VU 

A1cd, C2a), and has been identi ed as one of the 

‘priority protected species of regional concern’ 

(CEP/UNEP, 1995 pp. 1). 

One population of this focal species spans the 

border of Belize and Mexico, a diverse habitat 

including Chetumal Bay and the northern Belize 

Barrier Reef Lagoon System (Fig. 1). With a 

relatively short coastline extending from the Gulf 

of Honduras in the south to Chetumal Bay in 

the north, Belize reports the largest number of 

Antillean manatees in the Caribbean region 

(O’Shea & Salisbury, 1991). The contiguous 

Chetumal Bay is one of the most important areas 

for manatees in Mexico (Morales et al., 2000) and 

Northern Belize (Auil, 1998). Primary habitat consists 

of rivers, coastal lagoons and bays, and mangrove 

islands between the Belize Barrier Reef and 

the mainland (Bengtson & Magor, 1979; O’Shea & 

Salisbury 1991; Gibson, 1995; Auil, 1998; Morales- 

Vela et al., 2000). OVshore atoll systems, such as 

TurneVe Atoll, are considered secondary habitat for 

manatees (Gibson, 1995; Auil, 1998; Morales-Vela 

et al., 2000).

Manatees on the Belize Barrier Reef 

Figure 1. Northern Belize Barrier Reef Lagoon System and Southern Chetumal Bay showing survey 

locations and the 100-fathom line (100 fathoms=183 m, map modi ed from Purdy et al., 1975). 

343

344 C. Self-Sullivan et al. 

As identi ed by Packard & Wetterqvist (1986) 

in Florida, the components of manatee habitat 

systems include activity centres, travel routes, 

resources for expansion (potential feeding areas for 

recovering populations), essential areas (necessary 

to survive seasonal extremes), and the supporting 

ecosystem. For the purpose of the present study, we 

focused on the former two. We de ned activity 

centres as areas where manatees were frequently 

observed using resources such as vegetation and 

freshwater, in all seasons. For Belize, previous 

studies (Gibson, 1995; Lefebvre et al., 2001) indicated 

activity centres were located in silty substrates 

at 1–3 m depth. Activity centres could have 

attracted both residents and travellers (Reid et al., 

1991; Koelsch, 1997). We de ned travel routes as 

connections between activity centres used by individual 

manatees for daily, seasonal, or migratory 

movements (Sanderson, 1966). We were interested 

in whether geophysical characteristics such as a reef 

could have been used as landmarks by traveling 

manatees. 

Traditional knowledge in local communities indicated 

manatees were often sighted on the Belize 

Barrier Reef in the summer. However, the reef had 

not been included in descriptions of manatee habitat 

in Belize, possibly due to a bias from research 

done in Florida where reefs were not present in 

areas where manatees had been studied. Only one 

section of Belize Barrier Reef was included in 

national standardized surveys i.e., in the north 

where it lies within several 100 m of Ambergris 

Caye and has been classi ed as the caye habitat 

type (Auil, 1998). As recommended by Weeks & 

Packard (1997), we listened to local residents and 

chose to document in a systematic manner the 

patterns of manatee occurrence that they perceived. 

Using an inductive approach, we examined whether 

the seasonal trend was robust, and explored the 

reasons that this component of the habitat system 

would be most attractive to manatees in the 

summer. 

In this paper, we describe the seasonal occurrence 

of predominately male manatees at two locations 

along the Belize Barrier Reef: (1) Basil Jones Cut, 

which was isolated by Ambergris Caye from a 

manatee activity centre in Chetumal Bay, and (2) 

Gallows Reef, which was adjacent to a manatee 

activity centre in the Belize Barrier Reef lagoon 

system (the Drowned Cayes) and exposed to frequent 

boat traYc. The study was initiated at Basil 

Jones Cut and extended to Gallows Reef. If 

manatee presence on the reef was in uenced by 

access to warm or fresh water during the winter, we 

expected to nd manatees at Gallows Reef when 

they were not at Basil Jones. Similarly, if the 

predominance of males was in uenced by isolation 

from an activity centre, we expected to nd female 

manatees and calves at Gallows Reef when they 

were not at Basil Jones. 


Study site 

The Belize Barrier Reef extends from the Mexican 

border, where it is only a few meters from the coast, 

to the Gulf of Honduras where it is 50 km oVshore 

(Purdy et al., 1975). It forms an important geophysical 

barrier between the shallow coastal lagoon 

system and the deep Caribbean Sea. The Belize 

Barrier Reef, an extensive fringing and barrier 

reef, developed along an escarpment that abruptly 

terminates the 250 km-long Belize continental shelf; 

the sea oor plunges to over 183 m (100 fathoms) 

just beyond the reef crest (Fig. 1). 

In this tropical area of the Caribbean, seasons are 

less de ned by temperature and more by rainfall. 

The average air temperature ranges from 24 C in 

November–January, to 27 C in May–September 

(Purdy et al., 1975). The dry season extends from 

February through May; the rainy season extends 

from June through November (corresponding to 

the peak probability of hurricanes in July–October); 

December and January are referred to as the transition 

season (Auil, 1998). Average annual rainfall 

increases in a north to south direction, with 124 cm 

near Chetumal Bay, 178 cm at Belize City, and 

380 cm near the Gulf of Honduras (Purdy et al., 

1975). 

The two sampling locations are approximately 

70 km apart (Fig. 1). These locations diVer substantially 

in both geophysical characteristics and human 

activity, as described in more detail below. The 

northern location, Basil Jones, is relatively far from 

boat traYc centres and manatee resources (abundant 

seagrass beds, freshwater, deep channels). 

Both locations could provide shelter from surf 

surge, with areas suitable for resting and socializing 

with other manatees. Compared to Gallows Reef, 

seagrass beds appear sparser near Basil Jones. 

Northern location 

Basil Jones Cut (Fig. 2a), is a few hundred 

metres east of Ambergris Caye (18 5 38 N, 

87 52 12 W). Inside the Bacalar Chico National 

Park and Marine Reserve, this cut is one of several 

dozen small breaks in a 50 km, continuous section 

of Belize Barrier Reef that hugs the windward shore 

(Purdy et al., 1975). Basil Jones Cut (>3 m) is used 

by powerboats travelling to a shrimp hatchery, 

about a dozen local residents, and a few shermen 

or tour operators. The reef lagoon is narrow 

(

(a) 

(b) 


Figure 2. Aerial photographs of (a) the northern survey location at Basil Jones Cut (manatees were 

observed resting in the deep water channel, i.e. the darker water in the photo), and (b) the southern 

survey location east of the Drowned Cayes (Gallows Reef is located along the right margin of 

photograph; mainland Belize is approximately 15 km to the west). Photographs by Jimmie C. Smith. 

345


Caye is a solid landmass that blocks manatee travel 

from Belize Barrier Reef to Chetumal Bay, a core 

centre of manatee activity (Morales-Vela et al., 

2000). Manatees at Basil Jones Cut could travel to 

activity centres via two routes (Fig. 1): (1) about 

7 km north via Bacalar Chico, a secluded narrow 

canal that connects Chetumal Bay to the Caribbean 

Sea along the border between Belize and Mexico, or 

(2) about 30 km south, around the southern tip of 

Ambergris Caye where San Pedro Town is located 

(a highly developed tourist destination). 

Southern location 

Gallows Reef (Fig. 2b), is a section of Belize Barrier 

Reef with two breaks: North Gallows Cut 

(17 30 32 N, 88 3 4 W) and South Gallows Cut 

(17 27 25 N, 88 2 17 W). This central section of 

the Belize Barrier Reef is discontinuous, with large 

breaks in the reef crest, which provide many connections 

between deep water and the Belize Barrier 

Reef lagoon. Gallows Reef is about 2 km east of the 

Drowned Cayes (Fig. 1), an area of mangrove 

islands and associated seagrass beds used by 

manatees in both winter and summer (Auil, 1998; 

Sullivan et al., 1999; LaCommare et al., 2001). 

About 15 km due east of Belize City, this string of 

islands provides potential navigational ‘stepping 

stones’ from the reef to the Belize River, a longterm 

manatee activity centre identi ed from 

modern aerial survey data (Auil, 1998) and prehistoric 

archaeological data (McKillop, 1984). 

Throughout this shallow coastal zone, boat traYc is 

frequent, including shing boats, tugboats pulling 

sugar barges, recreational boats, tour boats, and 

water taxis. English Channel, a deep-water shipping 

route into the major port at Belize City, is used by 

cargo ships, tankers, and cruise ships. Cruise ships 

and sugar ships, which are too large for the port, 

have berths within the barrier reef lagoon. Small 

fast boats transport tourists in all directions from 

the cruise ships and Belize City, including welltravelled 

routes through the cuts at Gallows Reef 

to TurneVe Atoll. Tugboats tow barges of sugar 

from points north to temporary sites within the 

Drowned Cayes and then to the sugar ship. 

Sampling methods 

Based on year-round eVort at Basil Jones Cut, 

seasonal periods representing winter (December 

through March) and summer (June through 

August) were chosen for eYcient allocation of 

sampling eVort at Gallows Reef. At Basil Jones 

Cut, opportunistic observations of manatees by a 

local resident (the second author) began prior to 

1995 and extended beyond 1997 (Smith, 2000). A 

2-year period (April 1995–March 1997) of consistent 

eVort was selected for the purpose of the present 

analysis (Fig. 3). Preliminary studies indicated that 

manatees were not present in December-February; 

hence, more eVort was allocated to summer 

months. To determine whether manatees from Basil 

Jones Cut were re-sighted further south, surveys 

were extended to Gallows Reef during a study of 

the Drowned Cayes by the primary author (Sullivan 

et al., 1999). Sampling eVort was limited to winter 

(December–March) and summer (June–August) at 

Gallows Reef (1999–2001). 

Observation and recording procedures were 

similar at both locations, following a protocol that 

minimized disturbance by in-water observers 

(Smith, 2000). Each sample consisted of a 20-min 

continuous scan (Lehner, 1996) around a xed 

survey point. One to two snorkellers continuously 

scanned 360 around the survey point, while oating 

at the water’s surface. All samples were collected 

between 0800 and 1600 h local time. Only one 

sample was taken at each survey point on any given 

day at Gallows Reef; no more than two samples 

(one in the morning about 1000 h and one in the 

afternoon about 1600 h) were taken at the survey 

point at Basil Jones Cut. 

To determine sighting probability, any manatee 

observed during the scan, was recorded as a 

‘sighting’. If a manatee approached after the end of 

the scan, it was not recorded as a sighting although 

it could have been photographed, if feasible. 

‘Group size’ was recorded as the total number of 

individual manatees present in a scan. In other 

words the number of sightings within a 20-min scan 

was limited (0, 1); group size was unlimited (0, 1, 2, 

3, . . ., N). Group sizes greater than 1 were recorded 

only if more than one manatee was observed 

simultaneously or if sequential observations were of 

uniquely marked individuals. Sketches and photographs 

were used to record individual identities at 

Basil Jones Cut; photographs and video tapes were 

used to record individual identities at Gallows 

Reef. When visibility was too poor for positive 

identi cation of an individual, it was recorded as an 

‘unknown’. 

Behaviours (resting, feeding, socializing, milling, 

and travelling), body size (calf, adult) and gender 

(male, female) were recorded when possible. 

De nitions of behavioural activities were: (a) when 

‘resting’, the manatee was stationary, either in contact 

with the sea oor or at mid-water, occasionally 

rising in the vertical direction for breaths, but with 

no horizontal movement, no rooting or chewing, 

and no reaction to observer, (b) when ‘feeding’, the 

manatee was rooting or chewing in a seagrass bed 

or had seagrass parts trailing from it’s mouth when 

it rose above the bottom, (c) when ‘socializing’, one 

manatee touched or followed another, (d) when 

‘milling’, the direction of movement changed both 

vertically and horizontally with no consistent orientation 

to other manatees, to food, or in any one

direction, and (e) when ‘travelling’, the manatee was 

moving horizontally in one consistent direction, 

either towards or away from the survey point. 

To aid in interpretation of results at Gallows 

Reef, additional data were collected regarding the 

context of samples. As a check on visibility bias, 

assistants on a boat (anchored at the survey point) 

recorded surface behaviours of manatees relative to 

the in-water observer(s). Environmental measurements 

collected immediately following the sample 

included: (1) sea-surface water temperature using a 

thermometer (analogue or digital), (2) sea-surface 

salinity using a refractometer, and (3) vertical 

visibility using an eight-inch Secchi disk. In no 

instance was a manatee sighted by above-water 

assistants that was not also sighted by the in-water 

observer(s). 

The analyses were designed to account for diVerences 

in sampling eVort at Basil Jones (n=336) and 

Gallows Reef (n=45). Independent variables were 

season (winter, summer) at Gallows Reef and 

month (January through December) at Basil Jones. 

Dependent variables at both locations included: (a) 

group size, (b) frequency of surveys with manatees 

present or absent. Environmental measures of sea 


Figure 3. Individual manatee sightings at Basil Jones (April 1995–March 1997). Black boxes indicate the manatee was 

sighted at least once during the month; seasonal code indicates dry (white), rainy (dark grey), and transitional (light grey) 

months. Monthly probability of sighting (S/T) is de ned as the number of surveys that manatees were present, divided 

by the total number of surveys for each month. Note: BJ14 (an unmarked male) is included with unknowns in this gure. 

surface temperature, salinity, and visibility were 

also analysed at Gallows Reef. Non-parametric 

statistical tests of continuous variables included 

the Mann–Whitney U, and the Kruskal–Wallis 

(Lehner, 1996). Contingencies were tested using the 

Fisher’s exact test and the Freeman–Tukey deviate 

(Bishop et al., 1975). 

Results 

347 

Manatees were documented at both locations on 

the Belize Barrier Reef during the summer months, 

but not during the winter months. On 40% of all 

surveys, at least one manatee was sighted. As 

follows, analyses were speci c to each location. 

Basil Jones Cut 

At least one manatee was sighted on 42% of the 336 

surveys at Basil Jones Cut (Fig. 3), and mean group 

size varied signi cantly among survey months 

(Kruskal–Wallis H=119, df=6, P


Figure 4. At Basil Jones, group size varied signi cantly by 

month (1995–1997). Horizontal bars indicate means and 

circles indicate the range of values. 

were present at Basil Jones during the rainy season 

(June through November) and absent from 

December through March (Fig. 3). They returned 

at the end of the dry season (April/May). 

Manatees stayed in the calm, deep water of the 

channel inside the reef crest. The primary activity 

was resting, with occasional socializing. During one 

sighting two manatees were observed with seagrass 

trailing from their mouths. During another sighting, 

two manatees were observed rooting in an area 

of sparse seagrass approximately 20 m east of the 

resting area. On one occasion, a bull shark was 

observed with the manatees, with no interaction. 

Travel into the shallower areas of the lagoon system 

was rare. Trends in direction of travel by manatees 

outside the reef crest could not be determined. 

For 87% of the manatees sighted, identity was 

determined (Fig. 3). Seventeen individual manatees 

had unique markings and were documented by 

sketches; most were photographed at least once. 

Fifteen of these individuals were observed to be 

males. No calves or females were sighted; the sex of 

only two identi able individuals was undetermined. 

The sex of unknowns (13% of the sightings for 

which individual identity could not be determined) 

was undetermined in most cases. 

Group composition was uid, with no detectable 

long-term associations among individuals (Fig. 3). 

Two males (BJ01 and BJ08) were re-sighted in each 

of 3 years sampled. All seven males that were rst 

identi ed in 1995 were re-sighted the next year. Ten 

individuals, eight males and two undetermined, 

were newly identi ed in 1996. The pattern of 

re-sightings within each year was variable; some 

individuals were present only one month each 

season, others departed and returned after a break 

Figure 5. At Gallows Reef, manatees were absent on all 

18 winter surveys and present on 12 of 27 summer 

surveys. 

of 1–3 months. One individual ‘White Patch’ (BJ01) 

came and went regularly (1994–1997), being sighted 

17 times over seven consecutive months in 1996. 

The most frequently sighted individual (BJ03) was 

present in 41 surveys between April and August 

1996; however, he was not re-sighted again until 

June of 1998. 

Gallows Reef 

At least one manatee was sighted on 27% of the 45 

surveys at Gallows Reef (Fig. 5). Presence diVered 

signi cantly between seasons (Fisher’s exact 

phi=0.492, df=1, P=0.001). Manatees were absent 

on 100% of surveys during the winter season 

(Freeman–Tukey deviate z= "3.494) and present 

during 44% of the surveys in the summer season 

(Freeman–Tukey deviate z=1.611). Group size 

ranged from one to three, with the larger groups 

occurring only in late July and August. ‘White 

Patch’ (BJ01) who was frequently re-sighted at Basil 

Jones, was re-sighted at Gallows Reef in 1999. 

Sex was determined to be male for 10 of the 17 

manatees observed during all sightings. No calves 

or females were sighted, although the sex of seven 

manatees was undetermined. 

In general, manatees approached the in-water 

observer, paused momentarily and then retreated 

beyond visible range, remaining within view of 

assistants in the boat. On several occasions, the 

same manatee approached the in-water observer 

and retreated multiple times during a 20-min scan. 

On two occasions, more than one identi able 

manatee approached the in-water observer, both 

simultaneously and sequentially. Only once did a 

second individual approach the in-water observer 

after the end of the scan. The primary activity 

was milling, with occasional socializing. Rarely 

manatees were observed with seagrass trailing from 

their mouths; however, they were not observed 

rooting into the substrate for rhizomes.

Season signi cantly aVected mean sea surface 

temperature (Mann–Whitney U=33, n=18, 27, 

P20 C) such as natural springs and 

human-made attractions such as the warm-water 

eZuents of power plants (Packard & Wetterqvist 

1986). However, the concept of an essential area is 

open to critique based on more recent studies 

of individual manatee movements using satellite 

telemetry. Individual manatees from the Florida 

population vary widely in seasonal movements 

(Deutsch et al., 2000). Some travel long distances 

along the east coast of the USA, others travel short 

distances within Florida or between Florida and 

Georgia, and still others appear to be year-round 

residents remaining in one activity centre. Since 

some southern-most ranges overlap with other 

northern-most ranges of Florida manatees (T. m. 

latirostris), factors other than ambient water 

temperature appear to interact in determining 

seasonal movements. Perhaps ‘seasonal activity 

centre’ would be a better term for resident 

manatees. 

We hypothesize that access to freshwater is more 

of a directive factor than temperature in in uencing 

seasonal manatee use of the reef in the Belize 

coastal zone. Alternatively, individual manatee 

movements may be determined by a complex interaction 

of many factors experienced during a lifetime, 

including learning processes in uencing how 

travel routes are stored and retrieved from memory. 

Our reasoning is as follows. 

Even though manatee presence/absence on the 

reef was associated with water temperature, the 

same variation in seasonal water temperature was 

found in the adjacent Drowned Cayes where 

manatees were observed year-round during the 

same sampling period (Sullivan et al., 1999; 

LaCommare et al., 2001). Water temperature in the 

study area ranged between 25 C in the winter 

and 31 C in the summer, well above the incipient 

lethal level (as de ned by Fry, 1947) of cold 

tolerance for manatees (20 C c.f. Irvine, 1983). 

Temperature may have been correlated with 

another, undetermined, directive factor or gradient. 

An alternative hypothesis might be that manatees 

move further from estuaries during the summer 

rainy season when freshwater plumes from rivers 

are more likely to penetrate further into the coastal 

zone, meaning that manatees are more likely to be


at the reef in the summer. Annual salinity range at 

Gallows Reef was 34.5–38.0 ppt. Osmoregulation 

experiments on Florida manatees indicate that: (1) 

they are good osmoregulators in both fresh (0‰) 

and marine (34‰) environments (Ortiz et al., 1998); 

and (2) although they drink large amounts of 

freshwater when available, they do not drink 

marine water, but possibly oxidize fat to meet their 

water needs when restricted to eating seagrass in the 

marine environment (Ortiz et al., 1999). Manatees 

are considered to be dependent on freshwater in 

Florida (Hartman, 1979), and periodic access to 

freshwater is thought to be important to manatees 

in Belize (Gibson, 1995). However, it is not known 

whether nor how often manatees might move from 

the oVshore activity centres to mainland sources of 

freshwater in Belize. Although this distance is all 

well within 1-day’s travel range, manatees within 

the Drowned Cayes area are often sighted with 

dozens of salt-water barnacles covering their bodies 

(Self-Sullivan, unpublished data), an indication 

of long periods of time spent in the marine 

environment (Husar, 1997). 

Alternatively, underwater springs near our study 

locations may dry up or become unpalatable during 

winter. One manatee, sighted three times at Basil 

Jones in January and February 2001, was near a 

spring adjacent to the channel (G. Smith, unpublished 

data). Whether the manatee was drinking 

from the underwater spring could not be determined; 

the water was sulphurous as determined by 

smell and colour. Since we documented higher 

surface salinity in the summer compared to the 

winter at Gallows Reef, we do not believe that 

rainfall provides a lens of fresh surface water at the 

reef. Possibly the higher salinity was related to 

evaporation during summer months. 

Another hypothesis might be that the breaks in 

the reef could serve as a stopover site for manatees 

travelling in search of fresh water, in an east–west 

direction to and from oVshore atolls. Gallows Reef 

is midway between the Belize River (a fresh 

water source) and TurneVe Atoll, located further 

oVshore. Manatees have been opportunistically 

sighted at TurneVe Atoll, a large complex mangrove 

island-seagrass-coral reef system similar to 

the Drowned Cayes (Auil, 1998; Barbara Bilgre, 

pers. comm.). 

Seasonal distribution also might be related to 

winter storms from the northwest. Cold air masses 

from North America frequently aVect both temperature 

and wind strength during October through 

January (Purdy et al., 1975). ‘Northers’, as the local 

people call these events, may lower the sea surface 

by as much as 0.8 m. These events have a greater 

eVect than spring tides (0.5 m) on water depth in 

shallow northern lagoons. If manatees move away 

from shallow areas inside the reef, then absence 

would be more likely after storm events in the 

winter. 

Alternatively, manatees may have learned that 

the reef provides shelter from high surf during the 

summer hurricane season. For example, three 

manatees were at Gallows Reef 2 days after 

Tropical Storm Chantal hit the coast of Belize in 

2001 (Self-Sullivan, unpublished data). This is the 

largest group sighted at Gallows Reef. If manatees 

that move into the protected lagoon system sense 

protection from strong currents created by storm 

surge, breaks in the reef might serve as stopover 

sites for individuals moving back out to the atolls or 

continuing their north-south travel outside the 

reef. For obvious logistical reasons, such movements 

during hurricanes would be better studied by 

satellite telemetry than boat-based surveys. 

Clearly, there are several physical factors that are 

correlated with seasonal changes in the habitat used 

by manatees in Belize. To tease out the relative 

importance of these factors, we would recommend 

a combination of regional studies of individual 

manatee movements using satellite telemetry as well 

as simultaneous site-speci c studies at breaks in the 

reef. This type of approach would also provide a 

better understanding of how external environmental 

conditions interact with physiological states, 

as outlined below. 

Relation between travel and seasonal male 

reproductive activity 

Noting the distinctive absence of females at the 

breaks in the reef that we studied, a hypothesis 

emerged related to potential seasonal changes in 

reproductive activity of males. The evidence that 

manatees show seasonal patterns in reproductive 

behaviour is still ambiguous. Early reports by 

Hartman (1979) and Marsh et al. (1978) found no 

evidence for strong seasonality in Sirenian reproductive 

behaviour. However, Best (1982) reported 

seasonal breeding in the Amazonian manatee (T. 

inunguis). More recently, seasonal spermatogenesis 

has been reported in both Florida manatees 

(Hernandez et al., 1995) and dugongs (Dugong 

dugon) (Marsh, 1995). Similarly, seasonal variation 

in female reproductive hormones has been shown in 

captive Florida manatees (Larkin, 2000). However, 

seasonal reproductive activities were not tightly 

coordinated within populations (Larkin, 2000; Best, 

1982; Marsh et al., 1984; Marsh, pers. comm.). 

By tracking manatees using VHF radio and 

satellite tags since 1997, Powell et al. (2001) found 

more variation in male than female movement 

patterns in coastal lagoons south of Belize City. For 

example, females and some males remained inside 

the enclosed estuary year-round. However, a few 

males wandered outside the lagoon system, north 

and south along the mainland coast of Belize; one

male travelled at least as far as Belize City, 33 km 

north (Powell, pers. comm.). 

Based on published literature and our observations 

of only males on the reef with seasonal 

peaks and absences, we hypothesized that male 

manatees use the reef as a landmark during searches 

for oestrous females throughout the coastal lagoon 

system. If there is a winter low in spermatogenesis, 

then movement rates might decline. If there is a 

peak in both oestrous females and searching behaviour 

of males in summer, then male movement rates 

may increase. Variations in seasonal reproductive 

activity within a population might explain the 

diVerence in sighting peaks between Basil Jones 

(May–June) and Gallows Reef (July–August). 

Alternatively, sighting peaks could indicate 

clustered movements by males along the reef. 

To test these alternate hypotheses, we would 

recommend satellite-telemetry studies of both males 

and females in activity centres adjacent to the reef 

(Drowned Cayes and Chetumal Bay), combined 

with simultaneous site-speci c studies of individually 

identi able manatees. Such studies could 

answer the critical question of the degree to which 

there is a seasonal peak in reproductive activity 

of manatees in Belize and the degree to which 

male manatees move along the reef during peak 

reproductive periods. 

Implications for expanding populations in 

fragmented habitat 

Based on our sightings of ‘White Patch’ (BJ01) at 

both the northern (1994–1997) and southern (1999) 

sampling locations, we hypothesized manatees 

move along the reef in a north-south direction. 

However, we were not able to monitor both locations 

simultaneously. Extensive studies based on 

re-sightings of individually marked manatees have 

been successful in Florida (Reid et al., 1991) and 

should be continued in Belize. Over the long-term, 

these studies can be combined with satellite-tagging 

studies to determine variation in movement patterns 

during the lifetimes of individuals within a 

population (Beck & Reid, 1995; Reid et al., 1995). 

By comparing records at TurneVe Atoll (Bilgre, 

unpublished data), the Drowned Cayes, Gallows 

Reef (Smith, 2000; Self-Sullivan, unpublished data), 

and Basil Jones (Smith, 2000), a more accurate 

model of what in uences manatee movements in the 

centre of the species’ range may emerge for comparison 

with what is known from the northern 

extreme of the range, as studied in Florida. 

Long distance movements in uence gene ow 

among subpopulations, as re ected in complex patterns 

of genetic variation among manatees in the 

greater Caribbean area (Garcia-Rodriguez et al., 

1998). Movements of individual Florida manatees 

along the Atlantic coast of North America range 


351 

from 44 km to 2360 km (median=309 km) at rates 

of 25 km to 87 km per day (Deutsch et al., 2000). In 

comparison, the Belize Barrier Reef extends only 

about 220 km, with many breaks that could be used 

as stopover sites or for ingress to manatee activity 

centres such as Chetumal Bay, Cayes oV Belize 

City, Southern Lagoon, the Gulf of Honduras, and 

numerous coastal rivers and bays (Auil, 1998). 

Considering the long travel range of Florida 

manatees, Antillean manatees could move among 

population centres along the Yucatan Peninsula 

from Mexico through Belize to Guatemala and 

Honduras (Auil, 1998). During population expansion 

following historical exploitation, manatees 

from Belize may colonize unoccupied habitat 

between population centres in a wider region, with 

positive in uences on gene ow. 

The reef may also in uence connectivity within 

the Belize Barrier Reef lagoon system, decreasing 

the probability of inbreeding by increasing movements 

between southern areas and Chetumal Bay. 

The deep water just east of the barrier reef oVers an 

unobstructed north-south travel corridor and the 

reef oVers a physical feature that could be used for 

navigation. Use of this travel route by manatees 

could be an alternative to movement through the 

complex labyrinth created by the mangroveseagrass-coral 

lagoon system inside the barrier reef. 

An analogy might be a loop highway around a 

metropolitan maze of small roads. 

Consistent with knowledge of ‘bachelor males’ in 

other marine mammals species, we hypothesize that 

the turnover of individuals using stopover sites on 

the reef could be related to turnover in male access 

to breeding females. In 2001, local tour guides and 

staV at Bacalar Chico Reserve reported that they 

‘regularly’ observed manatees in a side lagoon 

adjacent to Bacalar Chico and at another cut in the 

reef between Bacalar Chico and Basil Jones (Smith, 

unpublished data). Another local tour guide 

reported that he observed a group of ve manatees 

inside the reef crest at GoV’s Caye (a sand caye on 

the Belize Barrier Reef just south of Gallows Reef) 

in November 2001 (Self-Sullivan, unpublished 

data). And a third tour guide reported seeing a 

manatee outside the reef crest at South Water Caye 

(a sand caye on the Belize Barrier Reef still further 

south) in June 2002 (Self-Sullivan, unpublished 

data). We recommend studies to determine if these 

are young dispersing males, prime males between 

periods of breeding activity, or old males unlikely to 

breed again. Answering these questions will provide 

insight to how genetic heterogeneity may be maintained 

in relatively isolated subpopulations of 

manatees. 

We recommend that the broader implications of 

this highly speci c study should be considered in the 

context of eVorts to design marine reserve systems


within the Caribbean. The concept of ‘connectivity’ 

was used by Roberts (1997:1454) to draw attention 

to how ‘local populations may depend on processes 

occurring elsewhere’. Although Roberts referred to 

patterns of larval transport among coral reefs, the 

concept also should be applied to large-bodied 

vulnerable species that use the lagoon systems protected 

by reefs e.g., manatees. We use the concept of 

‘stopover sites’ in a manner similar to its use in 

studies of migratory bird species. For example, 

Higuchi et al. (1996) identi ed stopover sites where 

migratory cranes paused for less than 10 days 

during travel between breeding and non-breeding 

locations. Although Antillean manatees clearly are 

not migratory as a species, the concept of a stopover 

site may be applied to a relatively short 

interruption of travel by individuals. Protecting 

stopover sites within local lagoon systems could be 

as important for conserving genetic heterogeneity, 

as protecting long-distance travel routes connecting 

fragmented populations on a regional scale. 

Conclusions 

Developing eVective strategies for conservation of 

manatee habitat requires knowledge of activity 

centres and movements among them. We documented 

manatee presence at breaks in the Belize 

Barrier Reef, with signi cantly more sightings in 

the summer (rainy) season than in the winter 

(transition/dry) season. Groups were small (average 

of two manatees), some individuals were repeatedly 

sighted and others were not. At least one individual 

moved between the northern and southern breaks 

that we monitored. All of the manatees for which 

sex was determined were male and no calves 

were sighted. However, we are cautious about 

interpretation of these data, due to the inductive 

nature of this study. We proposed several hypotheses 

related to physical (temperature, salinity, 

depth, storm surge) and physiological (thermoregulation, 

osmoregulation, reproductive status) 

factors potentially aVecting manatee use of breaks 

in the reef. To test these hypotheses, we recommend 

simultaneous studies of identi able manatees at 

several locations on the reef. In addition, satellitetagging 

techniques would be appropriate for determining 

the seasonality and extent of individual 

manatee movements among activity centres and 

stopover sites along travel routes associated with 

geophysical characteristics of the Belize Barrier 

Reef. Based on results of this study, we propose 

that reefs should be considered part of the network 

of travel routes and stopover sites identi ed as 

important components maintaining connectivity 

within manatee habitat in Belize and between fragmented 

populations of Antillean manatees in the 

Caribbean. 


This research project was reviewed by the Belize 

National Manatee Working Group, Coastal Zone 

Management Authority and Institute, and conducted 

under Scienti c Research Permits issued by 

the Belize Forestry Department, Conservation 

Division. Funding and in-kind support were provided 

by The Oceanic Society of San Francisco, The 

Lerner–Gray Marine Science Research Fund, The 

Earthwatch Institute, Spanish Bay Resort, Texas 

A&M University, University of Massachusetts- 

Boston, and the National Science Foundation 

Graduate Fellowship Program. We are extremely 

grateful to our Belizean eld assistants Pach 

Muñoz, Landy Requena, Jerry Requena, and 

Gilroy Robinson; our Belizean student interns 

Maxine Monsanto, Seleem Chan, and Clifton 

Williams; our logistics interns Liz Johnstone 

and Pam Quayle; and our Oceanic Society and 

Earthwatch Institute volunteers for their assistance 

in data collection. We thank Jimmie C. Smith for 

providing aerial photographs of our study area. 

Our gratitude is extended to Nicole Auil, Miriam 

Marmontel, and Leon David Olivera-Gomez for 

comments on previous drafts of this manuscript. 


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NEWS OF THE WEEK 

MEETINGBRIEFS>> 

1070 

AAAS ANNUAL MEETING | 18 TO 22 FEBRUARY 2010 | SAN DIEGO, CALIFORNIA 

A symposium organized at the last minute at 

the annual meeting of the American Association 

for the Advancement of Science (the 

publisher of Science) by two of the world’s 

most prominent scientific organizations 

addressed recent attacks on an increasingly 

beleaguered climate science community. The 

panel met in the uncertain aftermath of the 

stolen e-mails affair and critiques of the 

Intergovernmental Panel on Climate Change 

(IPCC) (Science, 12 February, p. 768). 

The symposium was convened by U.S. 

National Academy of Sciences President 

Ralph Cicerone, in conjunction with AAAS, at 

a time when flaws in the latest 

IPCC report, and even the legitimacy 

of climate science, have 

made headlines. E-mails 

uncovered late last year 

revealed instances of scientists 

on the panel discussing 

withholding data and documents 

from those with opposing 

views, conspiring to keep 

contradictory papers out of 

influential reports, and 

encouraging colleagues to 

delete e-mails. 

Despite a drumbeat of studies that corroborate 

the conclusion that the planet is warming 

and human activities are largely responsible, 

these recent skirmishes “have really shaken 

the confidence of the public in the conduct of 

science [overall],” said Cicerone, citing a number 

of recent polls on the public perception of 

science. “The situation is completely out of 

hand,” said climate scientist Gerald North of 

Not so fast. Critics have hit IPCC over a false assertion 

that Himalayan glaciers would melt away by 2035. 

Scientists Grapple With ‘Completely 

Out of Hand’ Attacks on Climate Science 

E-mail etiquette. Gerald North 

says scientists should not sound 

like bloggers. 

Texas A&M University in College Station, 

who has served as an IPCC reviewer. “One 

guy e-mailed me to say I’m a ‘whore for the 

global warming crowd.’ ” His PowerPoint 

presentation at the meeting included a slide 

quoting conservative talk show host Glenn 

Beck, who suggested that scientists commit 

“hara-kari” to atone. “Scientists cannot use 

the same tone and rhetorical style as commentators 

and bloggers,” North said. 

Although much of the session at the 

meeting, titled “Ensuring the Transparency 

and Integrity of Scientific Research,” focused 

on what Harvard University oceanographer 

and former AAAS head James 

McCarthy called the “abominable” 

press coverage, scientists 

owned up to their share of 

the blame. Small errors in the 

2007 report were “careless,” 

said McCarthy, but IPCC 

should have done a full and 

public examination to describe 

how they had come about: 

“The names of the authors, 

who was on the review, what 

happened—it all should have 

been up there, and it wasn’t 

done. And I think that the institution was hurt 

as a result,” he said. 

The community allowed “the situation to 

get out of control,” said Sheila Jasanoff of 

Harvard University. She said in general scientists 

had to connect better to the public. 

“There is a kind of arrogance—we are scientists 

and we know best,” Jasanoff said. 

“That needs to change.” –ELI KINTISCH 

26 FEBRUARY 2010 VOL 327 SCIENCE www.sciencemag.org 

Published by AAAS 

The Latest on 

Geoengineering 

Preliminary findings presented here suggest 

that some proposed techniques to cool the 

planet manually may have fewer barriers 

than previously thought. But many technical 

and societal barriers remain. 

Even before they got to the sessions, the 

scientists had to contend with a smattering of 

activists with drums, cameras, and a megaphone 

alleging that the government is already 

performing geoengineering through the 

spraying of particles, in so-called chemtrails. 

Physicist David Keith of the University 

of Calgary in Canada addressed the concept 

of spreading aerosol droplets in the stratosphere, 

where they could block a small fraction 

of the sun’s rays. A paper published last 

year in Environmental Research Letters suggested 

that the leading proposal, spraying 

Is a Dolphin a Person? 

Are dolphins as smart as people? And if 

so, shouldn’t we be treating them a bit better? 

Those were the questions scientists 

and philosophers debated at a session here 

on Sunday. 

Dolphins, it turns out, are pretty darn smart. 

Panelist Lori Marino, an expert on cetacean 

neuroanatomy at Emory University in Atlanta, 

said they may be Earth’s second smartest creature, 

after humans, of course. 

Bottlenose dolphins have bigger brains than 

humans (1600 grams versus 1300 grams), and 

they have a brain-to-body-weight ratio greater 

than that of great apes (but smaller than that of 

humans), said Marino. “They are the second 

most encephalized beings on the planet.” 

But it’s not just size that matters. Dolphins 

also have a very complex neocortex, the part 

of the brain responsible for problem solving, 

self-awareness, and various other traits we 

associate with human intelligence. And 

researchers have found spindle neurons in 

dolphin brains called von Economo neurons 

that in humans and apes have been linked to 

emotions, social cognition, and even theory of 

mind: the ability to sense what others are 

thinking. Overall, said Marino, “dolphin 

brains stack up quite well to human brains.” 

What dolphins do with their brains is also 

impressive. Cognitive psychologist Diana 

CREDITS (TOP TO BOTTOM): PHOTOS.COM; CONSERVATION HISTORY ASSOCIATION OF TEXAS 

on March 11, 2010 

www.sciencemag.org 

Downloaded from

CREDIT: PHOTOS.COM 

sulfur dioxide gas, wouldn’t work. Sulfur 

dioxide is converted in the atmosphere into 

droplets of sulfuric acid, which would clump 

and fall out of the sky before they could have 

much cooling effect. To get around this 

problem, Keith and colleagues have proposed 

using airplanes to spray droplets of 

the acid itself, rather than sulfur dioxide. In 

unpublished data, the team found that injecting 

only “a few megatons per year” of sulfuric 

acid could be more than twice as effective 

at blocking radiation as starting with 

sulfur dioxide. 

While scientists are finding ways to overcome 

the engineering challenges, the environmental 

effects of planet-hacking techniques 

remain uncertain. One challenge in geoengineering 

a warmed planet is simultaneously 

restoring temperatures while minimizing disruption 

of rain and precipitation. (Stratospheric 

particles lower the total amount of energy striking 

Earth, the driver of precipitation.) 

In previous modeling efforts, adding 

sun-blocking particles uniformly across the 

globe has tended to undercool the poles 

while overcooling the equator. So Kenneth 

Reiss of Hunter College of the City University 

of New York has been working with dolphins in 

aquariums for most of her career, and she said 

their social intelligence rivals that of the great 

apes. Dolphins can recognize themselves in a 

mirror, a sign of self-awareness. They can 

understand complex gesture “sentences” from 

humans. And they can learn to poke an underwater 

keyboard to request toys. “Much of their 

learning is similar to what we see with young 

children,” said Reiss. 

So if dolphins are so similar to people, 

shouldn’t we be treating them more like people? 

“The very traits that make dolphins interesting 

to study,” said Marino, “make confining 

them in captivity unethical.” She noted, for 

example, that, in the wild, dolphins have a 

home range of about 100 square kilometers. In 

captivity, they roam one 10-thousandth of one 

percent of this area. 

Far worse, Reiss said, is the massive dolphin 

culling ongoing in some parts of the world, 

which she documented with a graphic video of 

dolphins being drowned and stabbed in places 

like the Japanese town of Taiji. 

Thomas White, a philosopher at Loyola 

Marymount University in Redondo Beach, 

California, suggested that dolphins aren’t 

merely like people—they may actually be people, 

or at least, “nonhuman persons.” Defining 

exactly what it means to be a person is difficult, 

White said, but dolphins seem to fit the check- 

Caldeira, a climate scientist at the Carnegie 

Institution for Science in Stanford, California, 

modeled various approaches to try to 

counteract a severe warming—the result of a 

doubling of preindustrial CO 2 concentration. 

In work yet to be published, he distributed 

the particles unevenly to try to minimize 

those effects; for example, by putting 

more at the poles versus the equator. (Global 

warming is greatest in the Arctic.) In models, 

that strategy helped fix the undercooling/overcooling 

problem, but it worsened 

the effects on precipitation. “There’s a 

complex problem of how do you balance 

the damage that you do against the benefit,” 

said Caldeira. 

That said, simulating either geoengineering 

approach to counteract global warming— 

distributing particles globally or focusing on 

the poles—suggests a cooler world with less 

disruption of rain patterns than one in which 

warming continues unabated. “In a highglobal-warming 

world, more people would be 

better off with geoengineering, but some people 

would be worse off,” he said. 

–ELI KINTISCH 

Social smarts. Dolphins display many of the 

same behaviors humans do. 

list many philosophers agree on. There are the 

obvious ones: They’re alive, aware of their environment, 

and have emotions; but they also 

seem to have personalities, exhibit self-control, 

and treat others appropriately, even ethically. 

When it comes to what defines a person, said 

White, “dolphins fit the bill.” 

Still, experts caution that the scientific 

case for dolphin intelligence is based on relatively 

little data. “It’s a pretty story, but it’s 

very speculative,” says Jacopo Annese, a 

neuroanatomist at the University of California, 

San Diego. Despite a long history of research, 

scientists still don’t agree on the roots of intelligence 

in the human brain, he says. “We don’t 

know, even in humans, the relationship 

between brain structure and function, let alone 

intelligence.” And, Annese says, far less is 

known about dolphins. –DAVID GRIMM 

With reporting by Greg Miller. 

More Highlights 

From AAAS 2010 

NEWS OF THE WEEK 

Science reporters posted more than two 

dozen blog entries and podcasts from the 

meeting. Here is a sample. For full coverage, 

see www.sciencenow.org. And to see what 

our guest bloggers had to say, see 

news.sciencemag.org/sciencebloggers. 

A Sexy Treatment for Traumatic Brain Injury 

The hormone progesterone is best known for 

its work in the female reproductive system, 

where it plays various roles in supporting 

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brain injury. Researchers hope an infusion 

of progesterone given within a few hours 

of a car accident or other trauma will help 

prevent brain damage. 

The Mathematics of Clumpy Crime 

Even in a sprawling city like Los Angeles, 

California, crimes still clump together. Mathematical 

models presented at the meeting 

show that such crime hot spots form when 

previous crimes attract more criminals to a 

neighborhood. By understanding how these 

blobs form, researchers hope to help police 

break them up. 

Are ‘Test Tube Babies’ Healthy? 

When Louise Brown was born on 25 July 

1978, she kicked off an era. The first “test 

tube baby” is a mother herself now, and she’s 

been joined by millions of others born with 

the help of in vitro fertilization (IVF). But are 

babies born via IVF the same as those born 

naturally? Researchers have discovered some 

subtle genetic differences. 

Drive Green, Make Money 

Widespread adoption of plug-in electric vehicles 

could dramatically cut greenhouse gas 

pollution and reduce U.S. dependence on 

foreign oil. And results of a new electric-car 

pilot project provide added incentive to go 

electric: Car owners could return unused 

electricity to the grid and make real money 

doing so. 

Science Is Kryptonite for Superheroes 

Hollywood has a message for scientists: If 

you want something that’s 100% accurate, 

go watch a documentary. A panel of screenwriters 

for superhero-driven movies and TV 

shows like Watchmen and Heroes said that 

their job is to get the characters right, not 

the science. 

www.sciencemag.org SCIENCE VOL 327 26 FEBRUARY 2010 1071 

Published by AAAS 

on March 11, 2010 

www.sciencemag.org 

Downloaded from

Functional Ecology 2008, 22, 

284–288 doi: 10.1111/j.1365-2435.2007.01354.x 

Blackwell Publishing Ltd 

Infant carrying behaviour in dolphins: costly parental 

care in an aquatic environment 

S. R. Noren* 

Institute of Marine Science, Center for Ocean Health, University of California at Santa Cruz, 100 Shaffer Road, Santa Cruz, 

CA 95060, USA 

Functional doi: 10.1111/j.1365-2435.2007.0@@@@.x 

Ecology (2007) 

xx, 

000–000 

Summary 

1. Infant carrying behaviour occurs across diverse taxa inhabiting arboreal, volant and aquatic 

environments. For mammals, it is considered to be the most expensive form of parental care after 

lactation, yet the effect of infant carrying on the energetics and performance of the carrier is 

virtually unknown. 

2. Echelon swimming in cetacean (dolphin and whale) mother–infant dyads, described as calf in 

very close proximity of its mother’s mid-lateral flank, appears to be a form of aquatic ‘infant 

carrying’ behaviour as indicated by the hydrodynamic benefits gained by calves in this position 

which enables them to maintain proximity of their travelling mothers. Although this behaviour 

provides a solution for minimizing separations of mother–infant dyads, it may be associated with 

maternal costs. 

3. Through kinematic analyses this study demonstrates empirically that ‘infant carrying’ impacts 

the locomotion of dolphin ( Tursiops truncatus) 

mothers as evident by decreased swim performance 

and increased effort. 

4. The mean maximum swim speed of mothers swimming in echelon only represented 76% of the 

mean maximum swim speed of these mothers swimming solitarily. In addition, there was a 

concomitant 13% reduction in distance per stroke for mothers swimming in echelon compared to 

periods of solitary swimming. 

5. Thus, ‘infant carrying’ in an aquatic environment is associated with maternal costs, and could 

ultimately impact maternal energy budgets, foraging efficiency and predator evasion. 

Introduction 

Key-words: 

cetacean, echelon position, hydrodynamics, kinematics, swimming 

Maternal investment in mammals includes gestation, 

lactation and other forms of parental care. Infant carrying is 

considered to be the most costly form of parental care after 

lactation (Altmann & Samuels 1992; Kramer 1998) and has 

been described in 6 of 19 eutherian mammalian orders (for 

review, see Ross 2001). This behaviour provides a solution for 

mothers of diverse taxa that must manoeuvre within their 

environment to forage and avoid predators while accompanied 

by their young offspring (Ross 2001), which are 

handicapped by small body size, undeveloped tissues and 

naïveté (Carrier 1996). This behaviour is only thought to 

evolve when offspring are unable to independently follow 

their mothers, as in arboreal (i.e. primates) and volant (i.e. 

bats) environments (Ross 2001). 

*Correspondence author. E-mail: snoren@biology.ucsc.edu 

The aquatic environment also appears to require ‘infant 

carrying’ to ensure that mother–infant dyads remain intact 

during travel as manatees and sea otters are observed 

physically carrying their young. Cetaceans (whale and dolphin), 

however, cannot physically carry their young. Yet similar to 

that observed for primates (Altmann & Samuels 1992; Doran 

1992; Wells & Turnquist 2001), mature locomotor performance 

in dolphins is precluded for several years postpartum (Noren, 

Biedenbach & Edwards 2006). Echelon position is the 

predominant behaviour displayed by cetacean mother–infant 

dyads (Fig. 1; McBride & Kritzler 1951; Tavolga & Essapian 

1957; Norris & Prescott 1961; Au & Perryman 1982; Taber & 

Thomas 1982; Mann & Smuts 1999; Noren & Edwards 2007) 

and appears to represent an aquatic form of ‘infant carrying’ 

because it enables neonatal cetaceans to maintain close 

proximity to their mothers during travel (Norris & Prescott 

1961; Lang 1966) by increasing the swimming efficiency of the 

infant (Kelly 1959; Weihs 2004; Noren et al. 

2008). Thus 

cetaceans, like primates, appear to ‘carry’ their young. 

© 2007 The Author. Journal compilation © 2007 British Ecological Society

Fig. 1. Three bottlenose dolphin mother–calf pairs swimming in echelon 

position. Echelon position is described as calf in very close proximity 

with its mother’s mid-lateral flank in the region near her dorsal fin. 

Photo © and courtesy of Dolphin Quest Hawaii. 

Only a few studies have examined the energetic and 

locomotor consequences of infant carrying for the carrier, 

and these studies have focused on primates (Altmann & 

Samuels 1992; Schradin & Anzenberger 2001) and marsupials 

(Baudinette & Biewener 1998). Meanwhile the maternal 

consequences of infant carrying in other taxa and environments 

(i.e. volant and aquatic) remain unexplored. In view of this, I 

examined the kinematics of dolphin mothers swimming with 

their calf in echelon (Fig. 1) and swimming solitarily (> 1 m 

from their calf and all other dolphins) to elucidate the effect of 

‘infant carrying’ on maternal locomotor performance and 

effort in an aquatic environment. The advantages gained by 

calves in echelon position are examined in the accompanying 

paper (Noren et al. 

2008). 

Materials and methods 

Three captive bottlenose dolphin ( Tursiops truncatus) 

mother–calf 

pairs housed at Dolphin Quest Hawaii provided a controlled 

experimental approach to investigate cetacean locomotor performance 

and effort (Fish 1993; Skrovan et al. 

1999; Noren et al. 

2006, 2008). 

Methodologies regarding the dolphin enclosure, placement of the 

SCUBA diver-videographer, and placement of the dolphins in the 

water column are described in detail elsewhere (Noren et al. 

2008). 

Experimental swim sessions included both opportunistic (no reward) 

and directional swimming between two trainers (reward-based). 

Echelon swimming was recorded only when the mothers’ calves 

were 0–34 days postpartum. Thus, the present study only provides 

details regarding the maternal costs of echelon for mothers with 

very young calves (0–34 days postpartum). Solitary swimming was 

recorded at several intervals 0–2 years past parturition. Thirty-three 

hours of swimming were recorded and 334 short 1–6 s video clips 

were extracted and digitized (Fig. 2). Clips were divided into two 

association categories: (i) echelon position (Fig. 1); and (ii) solitary 

swimming (mother > 1 m away from calf and all other dolphins). In 

all clips the mothers were continuously stroking. 

A quantitative assessment of swim effort was obtained by 

calculating peak-to-peak fluke stroke amplitude and tailbeat 

oscillation frequency. Higher amplitudes and frequencies are 

associated with greater energy expenditure (Kooyman & Ponganis 

1998). Normalized tailbeat frequency (ratio of tailbeat frequency to 

© 2007 The Author. Journal compilation © 2007 British Ecological Society, Functional Ecology, 

22, 


Infant carrying in dolphins 

285 

Fig. 2. A tracing from a digitized video clip of a solitarily swimming 

mother dolphin. Anatomical points of interest (rostrum tip, cranial 

insertion of the dorsal fin, and fluke tip) were digitized at a rate of 60 

fields per second of video using a motion-analysis system (Peak 

Motus 6·1; Peak Performance Technologies, Inc. Englewood, CO, 

USA) following methods similar to Skrovan et al. (1999) and Noren 

et al. (2006). A distinct trace represents the movements of each 

digitised anatomical point. From left to right, the trace from the 

rostrum leads (pink), followed by the trace from the cranial insertion 

of the dorsal fin (yellow), and last is the trace from the fluke tip (blue). 

The brown dot is a digitized reference point indicating that the 

camera was steady while filming this video clip. 

swim speed; Rohr & Fish 2004) and distance per stroke were also 

calculated. Methods for video analysis and swim effort calculations 

are described in detail elsewhere (Noren et al. 

2006). 

The goal of this study was not to address individual variation, but 

to quantify changes in locomotor performance associated with swim 

style (echelon vs. solitary), thus similar to other kinematic studies 

data across individuals were pooled (Fish 1993; Skrovan et al. 

1999; 

Noren et al. 

2006, 2008). Pearson product moment correlation 

coefficients were used to determine the correlations of peak-to-peak 

fluke stroke amplitude and tailbeat frequency with swim speed for 

echelon swimming and also for solitary swimming; linear regression 

analyses were then used to determine the relationship for the parameters 

that demonstrated a strong correlation. Swim speed, normalized 

tailbeat frequency, and distance per stroke during echelon swimming 

and solitary swimming were compared using student’s t-tests 

when normally distributed, or Mann–Whitney rank sum tests when 

normality failed ( α = 0·05). The maximum swim performance of 

each individual during echelon swimming and solitary swimming 

was compared using a paired t-test 

( α = 0·10). Statistical analyses 

were performed using Sigma 

Stat 

2·03 (Systat Software, Inc. Point 

Richmond, CA, USA). Means ± 1 SEM are presented. 

Results 

Our experimental approach adequately captured swimming 

behaviours representative of wild dolphins (Noren et al. 

2008). The average swim speed of mother dolphins was 

–1 

significantly slower during echelon swimming (2·11 ± 0·06 m s ; 


n = 178) than during solitary swimming (3·88 ± 0·09 m s ; 

n = 156; T = 36534·00, P < 0·001). Given that 53% of the 

echelon swim data were from directional swim trials, compared 

to 94% for the solitary swim data, swim speed data from 

directional trials only were also compared to ensure that the 

previous result was not due to experimental design. The result

286 

S. R. Noren 

Fig. 3. Swimming kinematics of the mother in relation to the 

swimming speed of the mother. Peak-to-peak fluke stroke amplitude 

(a) and tailbeat frequency (b) were both correlated with swim speed 

for mother dolphins swimming in echelon with their calf (white 

symbols; r = 0·400, P < 0·001, n = 178 and r = 0·799, P < 0·001, n = 

178, respectively) and swimming solitarily (black symbols; r = 0·277, 

P < 0·001, n = 156 and r = 0·885, P < 0·001, n = 156, respectively). 

The relationship between swim speed and peak-to-peak fluke stroke 

amplitude appears to be nonlinear. Given the strong linear correlation 

between swim speed and tailbeat frequency (SF) linear regressions 

are provided for echelon (speed = 1·61 SF + 0·27; r 2 = 0·638, F = 

310·794, P < 0·001) and solitary (speed = 2·09 SF + 0·13; r 2 = 0·783, 

F = 555·610, P < 0·001) swimming. A different symbol is used for 

each of the three individual dolphins. 

was the same; average swim speed during echelon swimming 

was significantly slower than during solitary swimming 

( t = −11·644, 

P < 0·001, n = 94, 145). The absolute maximum 

swim speed for each mother swimming with their calf in 


echelon was 4·23, 4·39 and 4·32 m s for animals 1, 2 and 3, 


respectively. This compares to 5·65, 6·32 and 5·11 m s for 

animals 1, 2 and 3 swimming solitarily, respectively. As a 

result, mean maximum swim performance was significantly 


slower when mothers were swimming in echelon (4·31 ± 0·05 m s ) 


compared to solitary swim periods (5·69 ± 0·35 m s ; t = −4·816, 

n = 3, P = 0·053). 

Peak-to-peak fluke stroke amplitudes (Fig. 3a) and tailbeat 

frequencies (Fig. 3b) were correlated with swim speed for 

mother dolphins swimming in echelon and swimming 

solitarily. Because average swim speed was significantly different 

between the two swim categories, swim effort was standardized 

for swim speed. Mothers in echelon demonstrated significant 

increases in effort compared to periods of solitary swimming 

as evident by greater normalized tailbeat frequency 

Fig. 4. ‘Infant carrying’ imparted maternal costs. Mother dolphins 

swimming in echelon with their calf (white bar) demonstrated 

significantly lower mean distance covered per stroke (t = −7·068, 

P < 0·001, n = 178, 156) compared to periods of solitary swimming 

(black bars). 

( T = 19949·00, P < 0·001, n = 178, 156) and reduced distance 

per stroke (Fig. 4). For a given speed, mothers swimming in 

echelon increased tailbeat frequency by 17%, which resulted 

in a 13% decrease in distance covered per stroke compared to 

solitary swimming. 

Discussion 

Infant carrying provides a solution for mothers who must 

locomote in their environment while accompanied by their 

young offspring. Echelon swimming in cetacean mother– 

infant dyads is a type of ‘infant carrying’ that improves calf 

swim performance (Noren et al. 

2008), but it appears to come 

with a maternal cost. Average and maximum swim speeds 

were significantly slower for mothers swimming in echelon 

with their calves compared to periods of solitary swimming. 

For example, the mean maximum swim speed of the mothers 

swimming in echelon only represented 76% of the mean 

maximum performance of these mothers swimming solitarily. 

The maximum speed was assumed to represent the animal’s 

extreme performance, which is the method used to qualify 

physiological capacity (Weibel et al. 

1987), thus this result 

implies that the presence of a calf is a detriment to maternal 

swim performance. 

An alternate hypothesis for the decreased performance of 

dolphin mothers swimming in echelon is that the mother can 

only travel as fast as the infant can actively swim because the 

infant must occasionally stroke during the echelon swim 

behaviour. However, 0–1 month-old calves are capable of 


independent swim speeds of 0·58–4·20 m s (Noren et al. 

2006) and this performance is increased when the calf is in 

echelon (Noren et al. 

2008) because it receives up to 60% of 

the thrust from its mother (Weihs 2004). Thus, it is unlikely 

that the swimming ability of an entrained calf constrains 

maternal echelon swim performance. Studies of chimpanzees 

( Pan troglodytes) 

also suggest that infant carrying decreases 

maternal travel speed (Wrangham 2000; Williams, Hsien-Yang 

& Pusey 2002). 


22, 

284–288

In addition to decreased performance, dolphin mothers 

swimming in echelon were required to increase effort compared 

to periods of solitary swimming. For a given speed, 

mothers swimming in echelon significantly increased tailbeat 

frequency with the result that distance covered per stroke 

significantly decreased by 13% compared to solitary 

swimming (Fig. 4). Interestingly, the proportion of decreased 

distance per stroke in ‘infant carrying’ dolphin mothers is 

strikingly similar to the 17% decrease in distance per leap 

measured empirically for marmosets ( Callithrix jacchus) 

carrying weights equivalent to their newborn twin offspring 

(Schradin & Anzenberger 2001). Furthermore, although 

female wallabies carrying a load (approximating the mass of 

a fully developed offspring) did not alter stride frequency, 

they increased the time the foot applied force on the ground, 

which likely increased the stored elastic strain energy to levels 

necessary to transport the additional load (Baudinette & 

Biewener 1998). Regardless of habitat (aquatic vs. arboreal) 

or forces to overcome (hydrodynamic drag vs. gravity) in these 

systems maternal effort must change to support an increased load. 

The increase in maternal effort for dolphin mothers 

swimming in echelon compared to periods of solitary swimming 

may be associated with changes in water flow patterns and 

drag. The presence of the calf may disrupt the boundary flow 

around the mother causing it to separate, which would 

increase turbulent flow. In addition, the entrained calf could 

increase the surface area of the mother, which effectively 

increases the drag of the swimmer (Webb 1975). More power 

is required to overcome increased turbulent flow and drag 

(Webb 1975). As a greater proportion of maternal power 

output is utilized to accommodate increased turbulent flow 

and drag, there is less energy available to propel the animal 

forward. As a result, locomotor performance decreases 

because power output per stroke is limited by mechanical 

constraints (Fish & Hui 1991) and total work is limited by the 

animal’s metabolic scope (Weibel et al. 

1987). These relationships 

may explain the observed decrease in swim speed and 

distance covered per stroke for mothers swimming in echelon 

position. Although Weihs (2006) suggested that the gain in 

forward forces by the following body (calf) is larger than the 

added cost to the leading body (mother), a more detailed 

theoretical examination of the drag and flow patterns for the 

leading body in echelon position is warranted to validate the 

hypotheses for the proposed decreased maternal performance 

observed in the present study. 

Given that infant carrying mothers must forage and evade 

predators, one of many constraints on newborn offspring 

mass may be its impact on maternal locomotor performance. 

As a result, newborn dolphins and marmosets represent a 

similar proportion of maternal mass, 15% (mass data from a 

mother–calf pair in this study) and 17% (Tardif, Harrison & 

Simek 1993), respectively. Ultimately as an infant ages and 

increases in size, maternal costs associated with infant 

carrying theoretically increase in aquatic (Weihs 2004, 2006) 

and arboreal (Schradin & Anzenberger 2001) environments. 

Optimal theory predicts that maternal carrying costs should 

not outweigh the sum of the costs of independent locomotion 


22, 


Infant carrying in dolphins 

287 

by the mother and her offspring (Kramer 1998). Therefore, 

the transition to offspring locomotor independence may 

represent a parent–offspring conflict (Trivers 1974) as energy 

expenditure to carry an infant may limit the mother’s available 

energy to invest in future offspring (Kramer 1998). As 

cetacean and primate offspring increase in size, there is an 

increase in the active prevention and/or avoidance of infant 

carrying by mothers in both groups (Altmann 1980; Taber & 

Thomas 1982; Mann & Smuts 1999), such that with age there 

is a decrease in the time cetacean infants swim in echelon 

(Taber & Thomas 1982; Mann & Smuts 1999; Noren & 

Edwards 2007) and primate infants are carried (Altmann & 

Samuels 1992; Salvage et al. 

1996; Pontzer & Wrangham 

2006). Examination of human infant carrying behaviour also 

suggests that by a certain mass and age, mothers encourage 

their infants to walk independently (Kramer 1998). 

In summary, this study provides the first empirical evidence 

of the maternal consequences of ‘infant carrying’ in an aquatic 

environment. Although infant carrying provides a solution 

for mothers that must manoeuvre within their environment 

while accompanied by their underdeveloped offspring, this 

behaviour is associated with maternal costs regardless of environment, 

as evident in arboreal (Schradin & Anzenberger 2001) 

and aquatic (present study) regimes. The decreased locomotor 

performance and increased locomotor effort associated with 

infant carrying undoubtedly impacts maternal energy budgets, 

foraging efficiency and predator evasion. Given the prevalence 

of infant carrying behaviour across diverse taxa and habitats 

and the consequences of this behaviour, it is surprising that 

the energetics of infant carrying have largely been ignored. 

Future investigations are warranted, particularly in a volant 

environment, which remains unexplored. 


I thank Dolphin Quest, particularly J. Sweeney and R. Stone, for providing the 

experimental facilities and animals and for funding portions of data collection 

and analyses. I also thank Southwest Fisheries Science Center (SWFSC), 

particularly S. Reilly and E. Edwards, for funding portions of data collection. 

In addition, I thank the staff at Dolphin Quest Hawaii (particularly G. Biedenbach 

and C. Buczyna), T. Williams of the University of California Santa Cruz for the 

use of her Peak Motus system, and J. Redfern of SWFSC for assistance with 

data management. 

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Received 12 June 2007; accepted 27 September 2007 

Handling Editor: Francisco Bozinovic 


22, 

284–288

MARINE MAMMAL SCIENCE, 23(3): 629–649 (July 2007) 

C○ 2007 by the Society for Marine Mammalogy 

DOI: 10.1111/j.1748-7692.2007.00133.x 

SIMULATED VESSEL APPROACHES ELICIT 

DIFFERENTIAL RESPONSES FROM MANATEES 

JENNIFER L. MIKSIS-OLDS 1 

PERCY L. DONAGHAY 

Graduate School of Oceanography, 

University of Rhode Island, 

Narragansett, Rhode Island 02882, U.S.A. 

E-mail: jmiksis@gso.uri.edu 

JAMES H. MILLER 

Department of Ocean Engineering 

and 

Graduate School of Oceanography, 

University of Rhode Island, 

Narragansett, Rhode Island 02882, U.S.A. 

PETER L. TYACK 

Woods Hole Oceanographic Institution, 

Woods Hole, Massachusetts 02543, U.S.A. 

JOHN E. REYNOLDS, III 

Mote Marine Laboratory, 

1600 Ken Thompson Parkway, 

Sarasota, Florida 34236, U.S.A. 

ABSTRACT 

One of the most pressing concerns associated with conservation of the endangered 

Florida manatee is mortality and serious injury due to collisions with watercraft. 

Watercraft collisions are the leading identified cause of manatee mortality, averaging 

25% and reaching 31% of deaths each year. The successful establishment and 

management of protected areas depend upon the acquisition of data assessing how 

manatees use different habitats, and identification of environmental characteristics 

influencing manatee behavior and habitat selection. Acoustic playback experiments 

were conducted to assess the behavioral responses of manatees to watercraft approaches. 

Playback stimuli made from prerecorded watercraft approaches were constructed 

to simulate a vessel approach to approximately 10 m in sea grass habitats. 

Stimulus categories were (1) silent control, (2) approach with outboard at idle speed, 

(3) vessel approach at planning speed, and (4) fast personal watercraft approach. 

Analyses of swim speed, changes in behavioral state, and respiration rate indicate 

1 Present address of corresponding author: Jennifer L. Miksis-Olds, The Pennsylvania State University, 

Applied Research Laboratory, P. O. Box 30, State College, Pennsylvania 16804, U.S.A. 

629

630 MARINE MAMMAL SCIENCE, VOL. 23, NO. 3, 2007 

that the animals responded differentially to the playback categories. The most pronounced 

responses, relative to the controls, were elicited by personal watercraft. 

Quantitative documentation of response during playbacks provides data that may 

be used as the basis for future models to predict the impact of specific human 

activities on manatees and other marine mammal populations. 

Key words: manatee, Trichechus manatus latirostris, disturbance, avoidance, playback 

experiment, watercraft approaches. 

A pressing question regarding the conservation of Florida manatees (Trichechus 

manatus latirostris) ishow to minimize both the lethal and nonlethal impacts on 

manatees in areas where watercraft operate. The lethal impacts of watercraft account 

for an average of 25% to more than 30% of identified manatee deaths each year 

(Ackerman et al. 1995, Reynolds 1999). The nonlethal impacts of boating on the 

physical health of manatees, as well as an indirect impact on food availability and 

communication, are controversial topics for which available data are inadequate. 

Identifying specific environments or behaviors that put manatees at a greater risk 

for boat collisions and quantifying manatee reactions to varying speeds and motor 

types of approaching vessels are necessary steps toward achieving the overall goal 

of minimizing the negative, lethal, and nonlethal impacts of boats and associated 

noise. 

Manatees most commonly encounter relatively small boats: outboard or inboard/outboard 

leisure boats, personal watercraft (PWC), and fishing trawlers 

(Gorzelany 2004). PWC means a vessel

MIKSIS-OLDS ET AL.: SIMULATED VESSEL APPROACHES 631 

Specifically, swimming speed increased and animals moved toward deeper channel 

waters in response to boat approaches. The distance from the manatees to the boat, 

water depth at the boat, and water depth at the manatees each had a significant effect 

on swimming speed, whereas the type of boat or boat speed did not have a significant 

effect. 

Accurate detection of an approaching boat is only part of the problem for a manatee. 

In order to swim out of the direct path of the boat, the manatee must accurately 

localize the boat and respond appropriately. The physical characteristics of sound 

propagation in shallow water are complicated, and this can make it difficult to locate 

a sound source. From an acoustic standpoint, shallow water refers to areas where sound 

is propagated to distances at least several times the water depth, under conditions 

where both the surface and sediment boundaries have an effect on transmission (Urick 

1983). Compared to deep-water environments, there is greater attenuation of sound 

in shallow water environments (Medwin and Clay 1998). Higher frequencies have 

shorter wavelengths and are therefore more directional than lower frequencies with 

respect to a sound source of a given size. High levels of sound reverberation in shallow 

water also make localization difficult for even those species that possess extremely 

accurate localization ability. For example, bottlenose dolphins (Tursiops truncatus), 

which have excellent acoustic localization capabilities, have been hit by boats in shallow 

water (Wells and Scott 1997, Buckstaff 2004). These observations suggest that 

successful localization of approaching boats is necessary, but not a sufficient component, 

for dolphins to safely avoid approaching watercraft. Localizing approaching 

boats may also be an important component for manatees to avoid collision. 

Manatees that do manage to avoid collisions with watercraft still need to cope 

with other effects of boats. Boats that produce noise over the same frequencies as 

manatee vocalizations (Nowacek et al. 2003) can potentially mask communication 

signals. Motor noise can potentially mask communication signals. For example, if 

boat noise interferes with communication, females may lose contact with their calves 

or other members of a group, which could affect survival of the calves (Bengtson and 

Fitzgerald 1985). Manatees also are displaced from critical habitats with chronic boat 

disturbance (Provancha and Provancha 1988, Buckingham et al. 1999). Heavy vessel 

traffic may also cause manatees to expend more energy than they normally would 

(Reynolds 1999). For example, manatees significantly increase swim speed and move 

from shallow habitats to deeper channels during boat approaches (Nowacek et al. 

2001a). Based on these findings, as well as observations of behavioral responses to 

opportunistic vessel approaches prior to the initiation of this study, three categories of 

response (slow swim, fast swim, and rolling dive) were defined prior to the initiation 

of the study. The magnitude and diversity of manatee responses to vessel traffic clearly 

indicate the need for playback experiments to demonstrate manatee responses to the 

acoustic component of vessel approaches. 

Stimulus Recordings 

MATERIALS AND METHODS 

All stimulus recordings were made using a single hydrophone suspended from 

a recording vessel anchored in a sea grass habitat adjacent to a boating channel. 

The recording hydrophone was a HTI-99-HF hydrophone with built-in preamplifier 

and had a 2 Hz–125 kHz frequency range and −178 dB re 1V/Pa sensitivity. 

The recording system was a National Instruments PCMCIA DAQ Card-6062E used


Table 1. Characteristics of playback stimuli 

Category Exemplar 

Received level at 

10 m (peak SPL) Speed (mph) Motor size 

Idle 1 150 dB 5 115 hp 

2 151 dB 5 100 hp 

Planing 1 168 dB 35 115 hp 

2 163 dB 35 100 hp 

PWC 1 166 dB 40 1,235 cc 

2 158 dB 25 1,235 cc 

3 157 dB 25 1,235 cc 

4 162 dB 40 1,235 cc 

in conjunction with a Dell Inspiron 8100. The recording system had an overall 

frequency response of 20 Hz–22 kHz with a −178 dB re 1 V/Pa sensitivity at 16bit 

resolution. For each stimulus, the sound was recorded as a vessel approached the 

recording hydrophone at a constant speed from approximately 500–1,000 m away. 

The vessel approached to exactly 10 m away from the recording hydrophone and 

continued away at a constant speed for another 500–1,000 m. This method enabled 

calculation of received levels of the watercraft at 10-m distance (Table 1). The 10-m 

distance was the closest point of approach. Acoustic recordings of vessel approaches 

were made at two boat speeds: idle and full-throttle planing. Multiple exemplars 

from each category were recorded in order to ensure the generality of results and 

reduce pseudoreplication, defined as generalization from a study due to an animal 

responding to or learning from a single exemplar (Kroodsma 1989). Characteristics 

of each exemplar are summarized in Table 1. All vessels recorded possessed a 4-stroke 

motor, which provided an element of standardization across playback categories, 

regardless of engine size or vessel type. Two vessels were recorded for idle approaches. 

One vessel had a 115-hp outboard, and the other vessel had 100 hp. The same vessels 

were used to record two exemplars during a planing approach. Two separate 4-stroke 

PWCs were used to produce two planing approach recordings from each vessel for a 

total of four exemplars. Each PWC was recorded at two planing speeds: 25 mph (40 

km/h) and 40 mph (64 km/h; Table 1). 

The duration of all stimulus exemplars, regardless of stimulus category, was edited 

to 3 min to ensure the same length for each exemplar. This was done to control 

for the amount of time the playback subject was exposed to any sound coming 

from the playback system. Three-minute durations were chosen based on the longest 

audible approach sequence, which was the slow moving idle approach. For the idle 

approaches, 45 s of ambient noise preceded and followed the onset and offset of the 

stimulus signal, resulting in a total exemplar duration of 3 min. For planing and 

PWC approaches, ambient noise preceding and following the stimulus signal was 

appropriately included to produce a final stimulus duration of 3 min. The duration 

of ambient recording added prior to the stimulus onset was equal to that added after 

the signal offset. A silent control of 3 min was also constructed by creating a null 

vector (sound file containing 3 min of silence) at the same sample rate as the other 

stimuli. A silent control was selected to expose the subjects to any extraneous noise 

added by the transmit system that could potentially elicit a reaction. A control of only 

background noise was not included in the playback sessions because ambient noise 

preceded boat noise stimuli in all stimulus categories. If the animals were significantly


Figure 1. Playback categories aligned in time. Top row (A) shows the acoustic envelope 

difference among the categories. The middle row (B) shows the raw time series of a single 

exemplar within each category. The bottom row (C) shows the corresponding spectrograms 

for each exemplar. Spectrograms are plotted on a relative dB scale. Received levels of each 

vessel type are presented in Table 1. 

reacting to the background noise, there would have been a significant reaction to all 

category approaches. There was no significant response to the idle approach, which 

indicated that the animals were not reacting to either the boat noise or the background 

noise. 

Playback Categories 

The exemplars in the playback categories varied in several acoustic parameters. The 

stimulus categories differ not only in their acoustic envelopes, or overall amplitude 

shape, but also in their frequency characteristics (Fig. 1). The idle approaches had 

the longest stimulus duration but the lowest stimulus amplitude (Fig. 1a, b). The 

planing approaches had a more rapid rise time and higher amplitude than the idle 

approaches, but with a shorter acoustic envelope. The planing approaches also had a 

more gradual onset compared to the abrupt offset. The acoustic envelope of the PWC 

approaches was the shortest with the most rise time and approximately equal peak 

amplitude as the planing approaches. 

The differences in frequency parameters were most evident in the spectrograms 

of Figure 1c. The idle approaches lacked a clearly defined broadband peak at the 

closest point of approach, and the U-shaped bands indicated the beta effect of sound 

during the approach and retreat (Tang 2005). The beta effect results in a decrease 

in signal frequency prior to the vessel’s closest point of approach and an increase 

in signal frequency during the retreat. From the perspective of the manatee, the 

beta effect could provide information about the position of the vessel. The planing 

and PWC approaches had a clear broadband peak at the closest point of approach.


This was preceded by a strong tonal, harmonic signal. In the PWC approaches, 

the tonal component of the approach was vastly reduced compared to that of the 

planing approaches, and the broadband peak of the PWC approach was also much 

narrower. Figure 2 further illustrates the difference in frequency spectra among the 

playback categories. Fifteen seconds prior to the closest point of approach, the PWC 

was approximately 10 dB quieter than both the idle and planing signals at 2–3 

kHz (Fig. 2a). The magnitude of the idle and planing approaches was similar up 

to approximately 6 kHz. Above 6 kHz, the planing approach became about 10 dB 

louder than either the idle or PWC signals. Fifteen seconds prior to the closest 

point of approach, the planing approach transmitted the loudest signal in the higher 

frequencies. The planing approach was also clearly the loudest at the peak of approach 

by about 10 dB (Fig. 2b), with the exception of the PWC being the loudest between 

2 and 3 kHz. The idle approach was the quietest at all frequencies during the peak 

of approach. 

To better understand what the manatees detected during the vessel approaches, 

the power spectra of approaches were weighted by the only available manatee hearing 

thresholds as measured by Gerstein et al. (1999) (Fig. 3). Prior to the closest point of 

approach (Fig. 3a), planing signals were most salient above the background noise. The 

idle approach was above both the hearing threshold and noise floor for frequencies of 

approximately 2 kHz, whereas the PWC signature was either at or below detectable 

levels. At the closest point of approach (Fig. 3b), both the planing and PWC signals 

were well above threshold levels for all except the very lowest frequencies. The idle 

approach signal was loudest at approximately 2 kHz at the closest point of approach, 

but this level is 5 dB quieter than the planing and PWC levels over a band of 20 Hz 

to 20 kHz. 

Playback Experiments 

All playbacks were conducted in grass bed habitats that are commonly occupied 

by manatees. Restricting playbacks to one habitat type eliminated a confounding 

variable due to habitat type in the statistical analysis. In addition, playbacks were 

only performed with animals that were initially feeding or resting. The animals 

were relatively stationary during these two behaviors compared to traveling, milling, 

or social behaviors; therefore, changes in movement could be more easily observed 

and quantified. Restricting playbacks to two specific behavioral states also served to 

reduce the number of categories of analysis for statistical purposes, thus increasing 

the degrees of freedom within each category for each test. 

The playback protocol was designed to simulate a boat approaching a manatee to 

10 m. The same positional set-up was used for each playback regardless of which 

stimulus was used. The playback vessel was always positioned between the playback 

subject and the closest boating channel to simulate a boat approaching from deeper 

water and from the direction that a majority of boats would be traveling. Transmitted 

levels were adjusted for animal position so that the subject animal received 

appropriate received levels, as a function of stimulus type and exemplar (Table 1), 

regardless of the manatee’s distance to the playback vessel, which was between 2 

and 25 m from the manatee. Projection from a single, stationary transducer did not, 

however, allow for a directional motion component to the playback recording. If 

the manatees can localize the source accurately, the distance between the manatee 

and the playback vessel could have impacted the behavioral response. Due to the

A 

Power spectrum (dB re 1 Pa 2 /Hz) 

B 

Power spectrum (dB re 1 Pa 2 /Hz) 

130 

120 

110 

100 

90 

80 

70 

60 

50 

40 


Power Spectrum of Vessel Approach 15 s Before Peak 

30 

0 5 10 15 20 25 

100 

90 

80 

70 

60 

50 

40 

Frequency (Hz) 

Idle 

Plane 

PWC 

Power Spectrum for Vessel Approaches at Closest Point of Approach 

130 

Idle 

120 

Plane 

PWC 

110 

30 

0 5 10 15 20 25 

Frequency (Hz) 

Figure 2. Power spectra of vessel approach stimuli: (a) the comparison of 2-s clips measured 

15 s before the closest point of approach; (b) the comparison of 2-s clips taken at the closest 

point of approach.


A 

Weighted Spectrum (dB) 

B 

Weighted Spectrum (dB) 

130 

120 

110 

100 

90 

80 

70 

60 

50 

40 

Weighted Spectrum for Vessel Approaches 15 s Before Peak 

30 

0 5 10 15 20 25 30 30 

90 

80 

70 

60 

50 

40 

Frequency (kHz) 

Idle 

Plane 

PWC 

Noise 

Hearing Sensitivity 

Weighted Spectrum for Vessel Approaches at Closet Point of Approach 

130 

130 

120 

Idle 

Plane 

PWC 

120 

110 

Noise 

Hearing Sensitivity 

110 

100 

100 

30 

0 5 10 15 20 25 30 30 

Frequency (kHz) 

Figure 3. Spectra of vessel approaches weighted by the manatee hearing thresholds and 

smoothed in frequency plotted with ambient noise levels: (a) comparison of 2-s clips measured 

15 s before the closest point of approach; (b) comparison of 2-s clips taken at the closest point of 

approach. For illustration purposes the manatee hearing sensitivity values for the frequencies 

measured in this paper are shown by the dashed-dotted line (data taken from Gerstein et al. 

1999). 

130 

120 

110 

100 

90 

80 

70 

60 

50 

40 

90 

80 

70 

60 

50 

40 

Hearing Sensitivity (dB re 1 µPa) 

Hearing Sensitivity (dB re 1 µPa)


logistical constraints of the study design, this impact could not be addressed. Additional 

tests with stimuli simulating a rapid change in either direction or speed during 

the approach would provide valuable information that this study design was unable to 

offer. 

During playback experiments, the focal animal (occurring as a single animal or 

in a pair) was observed for a minimum of 20 min before and after the exposure of 

the playback stimuli. Primary observers were blind to the stimulus presentation, as 

the transducer and observer were on opposite sides of the boat and the background 

noise in the boat masked the in-air component of the playback stimulus, which was 

audible at the amplifier. During this time the subject was either identified from 

previously catalogued animals or photographed for later identification. Playbacks 

were only conducted if no other animals were detected within visual range during 

the 20-min pre-exposure period. Pre- and poststimulus observation included 4-min 

interval sampling of focal animal course, heading, distance to boat, and behavioral 

state. Ventilation and vocalization rates were recorded continuously. Vocalization 

rates were not analyzed, however, because the transducer was on the same vessel as 

the recording hydrophone, and the playback saturated the hydrophone recording rendering 

the manatee vocalizations inaudible. Saturated vocalization recordings during 

the playback sessions did not allow for uninterrupted vocalization rate analysis. If 

the animals left the area during the pre-exposure period or during exposure to the 

playback stimuli, they were not followed. 

Five minutes prior to the playback of any stimulus, the research vessel was anchored 

within 25 m of the focal animal and the sound source was deployed. An Aiwa model 

XP-V516C compact disc player connected to a Rockwood Detonator AMP-400 CRX 

amplifier delivered sound to a Lubell 9162 transducer, which projected the playback 

stimuli. This system was capable of producing a source level of approximately 190 dB 

re 1 Pa at 1 m in the frequency range of 240 Hz to 20 kHz. Response due to multiple 

boat interactions was avoided by only performing a playback when no other vessel 

had entered a 1-km radius for a 15-min period prior to the start of playback session. 

Each playback session consisted of four playback stimulus presentations presented 

5 min apart. The 5-min stimulus presentation was chosen based on the knowledge 

that bottlenose dolphins in Sarasota Bay encounter a passing vessel every 6 min 

(Buckstaff 2004). Manatees would experience a similar or shorter interval between 

boat encounters depending upon the number of recreational vessels in the area at any 

particular time. One stimulus from each of the four categories (control, idle, plane, 

PWC) was presented in random order. If the focal animal moved outside of a 25-m 

radius before the presentation of the last stimulus, the research vessel re-anchored 

closer to the animal, and the remaining playback stimuli were presented followed by 

a 20-min poststimulus observation period. In an effort to reduce pseudoreplication, 

no manatee was a playback subject more than twice, and no animal ever received the 

same exemplar more than once (Table 2). 

During the playback session, observations included point sampling of focal animal 

course, heading, distance to boat, ventilation, and behavior at the time of each 

surfacing. Visually observed responses to the playback stimuli generally fell into four 

categories: (1) investigate boat, (2) slow swim, (3) rolling dive, and (4) fast swim. Animals 

investigating the boat swam directly to the boat and interacted with it in some 

way. Slow swims were characterized by the animals changing position relative to the 

playback vessel without any visible wake or fluke prints. Rolling dives were identified 

by the arching of the manatee’s back and entire fluke leaving the water prior to a 

dive. Fast swims were characterized by a visible wake and strong fluke prints, often


Table 2. Summary of playback subjects, stimulus sequence, and response. In the “age” and “group composition” categories, A indicates adult, SA 

indicates subadult, C indicates calf 

Number Group Stimulus 1 Stimulus 2 Stimulus 3 Stimulus 4 

Session Date ID Age in Group composition Response Response Response Response 

1 4 June 2004 Snuff A 2 A, A C Idle2 PWC4 — 

(SB047) None None FS, LA — 

2 10 June 2004 Phish LA A 1 Plane2 C Idle2 PWC2 

SS None SS RD 

3 15 June 2004 Phish A 1 PWC2 Plane1 Idle2 C 

SS None None None 

4 21 June 2004 DU723 A 2 A, C Plane2 Idle2 C PWC1 

SS None None FS 

5 23 June 2004 623BB A 2 A, A C Idle1 Plane1 PWC3 

None SS FS FS, LA 

6 25 June 2004 625A A 2 A, C PWC4 Idle2 Plane2 C 

FS SS SS None 

7 28 June 2004 628A A 2 A, C PWC1 C Plane1 Idle1 

FS SS RD None 

8 1 July 2004 DU723 A 2 A, C C Idle1 PWC2 Plane1 

None SS FS SS 

9 6 July 2004 706AA SA 1 PWC4 Idle1 C Plane1 

RD None None None 

10 21 July 2004 721A A 2 A, C Idle1 Plane2 C PWC1 

None None None FS, LA

Table 2. Continued. 


11 22 July 2004 Clyde A 2 A, A C PWC4 Plane2 Idle2 

None SS None None 

12 23 July 2004 723B A 2 A, C Plane2 C PWC3 Idle1 

RD None RD RD 

13 23 July 2004 723A A 2 A, C PWC2 C Plane2 — 

RD None SS, LA — 

14 26 July 2004 726D A 2 A, C Plane1 Idle2 PWC1 C 

FS SS FS None 

15 26 July 2004 Phish LA A 2 A, A C Idle1 PWC4 Plane1 

None None FS SS, LA 

16 27 July 2004 Splotch A 2 A, A PWC2 Idle1 C Plane1 

FS None None None 

17 28 July 2004 727AA SA 1 C Idle2 — — 

SS None — — 

18 3 August 2004 803BB A 2 A, SA Plane2 C Idle1 PWC3 

RD None RD SS, LA 

19 4 August 2004 804C SA 2 SA, SA C PWC4 Idle2 Plane1 

None FS None None 

20 5 August 2004 805BB A 2 A, A Idle1 Plane1 PWC1 C 

None FS FS SS 

21 19 August 2004 823F SA 1 Idle2 PWC2 Plane1 C 

None SS None SS


accompanied by a mud cloud stirred up from the bottom. Two retreating behaviors 

were also observed in relation to the playback vessel: (1) retreat to deep water and 

(2) pass by boat on the way to deep water. Direct retreats were characterized by the 

animal increasing distance from the playback vessel in the direction of deeper water. 

Passing by the boat on the way to deep water was a separate classification because 

the animal had to initially approach the playback vessel before retreating to deeper 

water. Passing by the boat on the way to deep water differed from the “investigate 

boat” response because the passing by the boat did not include any direct contact or 

interaction with the playback vessel by the manatee. 

In addition to behavioral responses, a respiratory response to the playback stimuli 

was also calculated. An index of ventilation variability (index of variability) was 

calculated from the time series of visually observed surface breaths recorded continuously 

throughout the playback experiments. The poststimulus index of variability 

was calculated by adding the absolute values of the difference in time between breaths 

for the three consecutive breaths following the stimulus onset (poststimulus index 

of variability =|t 0 − t 1| +|t 1 − t 2| +|t 2 − t 3|). Higher values of poststimulus 

variability indicated a larger variability in ventilation. Traditional measures of ventilation 

rate and its associated variance were not utilized in this analysis because long 

submersions followed by quick successive breaths cancelled each other and masked 

the true breathing pattern. Inclusion of absolute values preserved the level of variability 

between breaths. Prestimulus index of variability was calculated in a similar 

manner. The index was calculated from a time series of triads consisting of three consecutive 

breaths preceding the first stimulus. The triad values were then averaged to 

produce a prestimulus index of variability (prestimulus index of variability ={(|p 0 

− p 1|+|p 1 − p 2|+|p 2 − p 3|)}/n). Multiple, consecutive triads were used in the 

prestimulus index in order to establish the most accurate baseline index of variability. 

The poststimulus index only contained a single triad because this was the minimum 

number of surfacings observed between stimulus presentations during the playback 

session. 

Statistical Analysis 

The first level of analysis compared the frequency of animals either responding 

or not responding to each playback category and the control condition. Statistical 

significance was based on the binomial distribution. Differences in the frequency of 

behavioral responses between categories were investigated with a R × C G-test for 

independence. Based on behavioral observations to opportunistic vessel approaches, 

the three categories of response (slow swim, fast swim, and rolling dive) were defined 

prior to the initiation of the playback study. A priori conditions were met, which 

justified the use of the R × C G-test for independence used to assess the frequency 

of behavioral responses to the playback stimuli. Differences in the deviation between 

prestimulus and poststimulus index of variability across playback categories were 

tested with a single-factor analysis of variance (ANOVA). 

RESULTS 

Twenty-one playback sessions were conducted with 19 different subjects encountered 

either as single animals or in pairs (Table 2). A total of eighty stimuli were 

played: 21 Control, 10 Idle1, 10 Idle2, 11 Planing1, 8 Planing2, 6 PWC1, 5 PWC2, 

3 PWC3, and 6 PWC4. Seventeen out of 21 animals (81%) showed no locomotor


Figure 4. Proportion of responses elicited by playback treatments. 

response to the silent control (Table 2 and Figure 4). The difference between response 

or no response for all stimuli vs. the silent control was significant at the 95% significance 

level based on a binomial distribution (P < 0.001). This indicated that the 

manatees were not significantly reacting to the exposure of the broadcasting system 

provided by the control stimulus. Manatees showed a marked locomotor response 

to the playback stimuli compared to the silent control. Thirteen of twenty animals 

(65%) showed no response to the idle approach, whereas 35% showed some type 

of locomotor response (i.e., slow swim, approach boat, fast swim, etc.) (Figure 4). 

This 35% response rate was not significant at the 95% significance level. During 

the planing approaches there was a significant locomotor response rate of 63% (P = 

0.002). Of the twelve animals that showed a locomotor response to the planing approach, 

two abandoned the area. All animals showed a locomotor response to the 

PWC approach (P < 0.001). Four of the twenty animals that responded (20%) left 

the area. 

An analysis of response orientation and heading of those animals that did show 

a locomotor response to the playback stimuli revealed a striking pattern (Fig. 4). 

Of the four animals that did respond to the control, all four investigated the boat. 

Seven animals of twenty responded to the idle approach. Of the seven, four (57%) 

retreated directly to deep water, two (29%) passed by the playback vessel on the way 

to deeper water, and one animal (14%) retreated from the playback vessel to shallow 

water. During the planing and PWC approaches, the number of animals retreating 

directly to deep water increased, whereas the number of animals passing by the boat 

decreased. In general, manatees tended to respond to all approaches by retreating to 

deep water. The frequency of animals retreating directly to deep water increased in 

response to an increase in speed of the approaching vessel. 

Behavioral analysis of the retreating animals showed a graded response in behavior 

associated with playback category (Fig. 5). No animals retreated during the controls, 

so this category was not included in the analysis. The frequency of animals retreating 

with a slow swim decreased from 71% in response to the idle approach to 37% for the


Figure 5. Behavioral response of retreating manatees to the playback categories. There 

is no response for the controls because no animals retreated during control presentations. ∗ 

shows the significant decrease in the slow swim response associated with playback category 

(0.01 

playback category (0.01 

planing approach to finally 16% in response to the PWC approach (Fig. 5a). Analysis 

of frequency using a R × C G-test for independence revealed that the frequency of 

the slow swim response was dependent on playback category (0.01 

Sokal and Rohlf 1995). Similarly, the increase seen in the frequency of fast swim 

response was dependent upon playback category (0.01 

responded to the idle approach with a fast swim, whereas 37% and 68% responded 

to the planing and PWC approaches, respectively (Fig. 5b). There was slight decrease 

in the frequency of rolling dive responses to the PWC approaches, but this decrease 

was not a significant pattern. 

An ANOVA of the poststimulus index of variability showed a significant overall 

effect of stimulus type (F3,82 = 2.72, P = 0.04; Fig. 6). Post hoc multiple comparisons 

indicated an increase in variability between the prestimulus and both planing 

Figure 6. Mean deviation from prestimulus/control variability for each playback category. 

The asterisk ( ∗ ) indicates categories that differed significantly from the prestimulus/control 

values. Error bars represent standard error.


and PWC responses. Post hoc multiple comparisons were performed for all other 

category comparisons, but no other comparisons were significant. This suggests that 

the manatees responded to the planing and PWC approaches in a similar manner 

with an increase in ventilation variability. 

DISCUSSION 

The most pronounced responses to the playback stimuli, relative to the controls, 

were elicited by the PWC. Significant behavioral and physiological responses were also 

seen in response to planing boat approaches, indicating that rapid vessel approaches do 

affect manatee behavior. Approaches by fast-moving vessels resulted in the disruption 

of feeding activity, an increase in energy expenditure inferred from swim speed, and 

in some cases a short-term avoidance of the feeding area. Avoidance reactions to 

approaching vessels are not unique to manatees, as disturbance responses to motorized 

vehicles have been documented in both marine and terrestrial species. In the marine 

environment, avoidance to motorized watercraft had been reported in manatees, 

cetaceans, and pinnipeds (manatees: Provancha and Provancha [1988], Buckingham 

et al. [1999], Nowacek et al. [2004a]; cetaceans: bottlenose dolphins, Janik and 

Thompson [1996], Nowacek et al. [2001b], Hastie et al. [2003], Buckstaff [2004]; 

killer whales, Orcinus orca, Kruse [1991], Williams et al. [2002a, b]; Hector’s dolphins, 

Cephalorhynchus hectori, Bejder et al. [1999]; beluga whales, Delphinapterus leucas, Finley 

et al. [1990]; pinnipeds: walruses, Odobenus rosmarus, Fay et al. [1984]; and harbor 

seals, Phoca vitulina, Reijnders [1981]). Documented disturbance reactions include 

increases in vocalization rate, increases in swim speed, longer dive durations, decreased 

interanimal distance, increased breathing synchrony, and displacement from haulout 

sites. Terrestrial animals (bighorn sheep, Ovis canadensis canadensis, MacArthur 

et al. [1979]; white-tailed deer, Odocoileus virginianus, Richens and Lavigne [1978]; 

caribou, Rangifer tarandus, Murphy et al. [1993]; and penguins, Pygoscelis adelia, Culik 

et al. [1990]) were also found to avoid road vehicles, snowmobiles, and aircraft. 

The manatees studied here showed the ability to discriminate and differentially 

react to the two different engine types and speeds simulated in the playback experiments. 

Nowacek et al. (2001a, 2004a) reported a generalized response by manatees 

to approaching boats involving turning toward or into deep water without specific 

regard to boat type, boat speed, distance from the manatee, the kind of habitat the 

boat was operating in, or the kind of habitat occupied by the manatee. Increases in 

swim speed were most prevalent in shallow water grassbeds when boats approached 

to between 0 and9m(Nowacek et al. 2004a). This study also showed that manatees 

reacted to simulated vessel approaches to within 10 m with an increase in swim 

speed and directed movement toward the closest deep water. The findings here differed 

from the previous study, however, because boat type and boat speed in this 

study appear to have a significant effect on swimming speed. This effect may not 

have been detected by Nowacek et al. (2004a) due to differences in study design and 

categorization of visible responses. This study differentiated between responses based 

on two different changes in swim speeds and the presence of rolling dives, which 

indicate deeper dives. Results presented here show that the manatees responded to 

slower idle approaches with a greater number of slow swim responses and a larger 

number of retreat paths that intersected with the playback vessel. In contrast, responses 

to fast approaching outboard motorboats or PWCs elicited a significantly 

greater frequency of response for fast swim speeds and retreat paths that avoided


the playback vessel. Because playback experiments only introduce the frequency and 

amplitude components of vessel signals (other potential components include visual 

information above and below water, and changes in the bearing of the acoustic signal), 

the frequency and amplitude information available to the animal prior to the closest 

point of approach can be used to explain how the animals may be discriminating and 

ultimately reacting to the different playback categories. 

Fifteen seconds prior to the closest point of approach, the planing approaches were 

approximately 10 dB louder than the idle and PWC approaches for frequencies from 

6to22kHz. Similarly, the idle approach was approximately 12 dB louder than both 

the planing and PWC approaches at 2 kHz. Therefore, the slower rise times of the 

idle and planing approaches provide more information to the animals 15 s prior to 

arrival compared to the PWC approach. It is possible the manatees can extract the 

necessary information from these acoustic cues relating to speed, direction, and boat 

type in order to execute the most appropriate and energetically favorable response. 

The most desirable responses are those that enable manatees to avoid collisions with 

watercraft. The playbacks provided an opportunity to observe responses to specific 

acoustic components of vessels approaching at a constant speed under controlled 

circumstances. Responses indicated that manatees are able to detect approaching 

vessels and execute appropriate responses to avoid vessel collisions by retreating to 

deep water where they can swim beneath the boat. Furthermore, manatees are able to 

discriminate between vessel types and speeds, which appeared to influence the degree 

and direction of response. Manatees tended not to respond to idle approaches. When 

animals did respond, most did so at a slow speed. By contrast, responses to PWC and 

planning approaches elicited a greater proportion of fast swims. Slower responses to 

slowly approaching vessels and quicker responses to faster-moving vessels would be 

appropriate in real-life situations, provided the vessels did not change speed. Manatee 

response is in marked contrast to that of right whales, which tend not to respond 

to approaching ships even though they do respond to alert signals (Nowacek et al. 

2004b). Right whales responded to an alert signal during controlled exposures by 

swimming strongly to the surface, which is a response that is likely to increase rather 

than decrease the risk of collision. 

The most energetically favorable response for a manatee to any vessel approach 

would be to minimize locomotor costs by not moving at all. However, this would 

not always be the most appropriate response in terms of avoiding vessel collisions. If 

a change in location is necessary, a response at swim speeds at or near the minimum 

cost of transport would be most efficient. It is often found that birds and mammals 

swim underwater at or near the speed of minimum cost of transportation (Williams et 

al. 1993, Ropert-Coudert et al. 2001, Lavvorn et al. 2004). Manatees generally cruise 

at speeds of 2–6 mph (3–10 km/h), although they have been recorded at speeds of 

15 mph (24 km/h) for short bursts (Hartman 1979). Speeds of 2–6 mph would have 

been classified into the slow swim response in this study, so it appears that manatees 

responding to idle and many planing approaches acquire enough prior information to 

execute an energetically efficient response. The PWC acoustic signatures 15 s prior 

to arrival do not provide as much acoustic information compared to the idle and 

planing approaches. 

The short rise time signal associated with PWC approaches does not differ greatly 

from ambient noise levels until 5 s before the peak, so it is possible that the 

manatees do not perceive these approaches in enough time to execute an energetically 

favorable response. Consequently, faster, less efficient responses are necessary to


retreat from a possible PWC collision. An alternative explanation is that the sharp 

rise time associated with the PWC approach elicits a startle response that causes 

manatees to retreat from the sound source without evoking a higher level of cognitive 

analysis. Avoidance responses to the short rise time signals have also been 

observed in sharks. Myrberg et al. (1978) reported that a silky shark (Carcharhinus 

falciformis) withdrew 10 m from a speaker broadcasting a 150–600-Hz sound 

with a sudden onset and a peak sound pressure level of 154 dB re 1 Pa. These 

sharks also avoided a pulsed attractive sound when its sound level was abruptly increased 

by >20 dB. Finally, through prior encounters with PWCs, manatees may 

have learned to associate the PWC acoustic signal with vessels that are less predictable 

and more likely to approach them in shallow areas, thus requiring a more extreme 

response. 

Regardless of the specific acoustic characteristic of the fast vessel approaches that 

elicit fast swim responses, these signals cause manatees to increase their swim speed. 

Swim speed, as well as breathing rates and heart rate, have been used to estimate the 

energies of free-ranging marine mammals (Sumich 1983, Kshatriya and Blake 1988, 

Williams et al. 1992, Hind and Gurney 1997). Assuming that manatees respond at 

maximum speeds and that the maximum aerobic energy used during locomotion can 

reach 4–11 times resting levels in marine mammals (Elsner 1986, Williams et al. 

1993), consistent responses to vessel approaches potentially affect the energy budget of 

manatees in a significant way. Responses detected in this study are consistent with an 

energy cost, and future work quantifying energy expenditures will determine whether 

multiple reactions could have a long-term effect at the individual or population 

level. 

Most playback experiments measure movement, visual, or vocal responses to the 

sound played. Behaviors most typically measured are orientation or movement relative 

to the sound source, vocalizations made in response to the playback, and previously 

defined behaviors or displays such as aggressive or sexual displays. Less frequently 

used, but possibly more objective, responses are changes in heart rate (birds: Davis 

[1986], Diehl [1992]; humans: Brown et al. [1976]; chimpanzees, Pan troglodytes: 

Berntson and Boysen [1989]; bottlenose dolphins: Miksis et al. [2001]) and hormone 

levels (Dufty 1982). Neither quantitative swim speed nor fluke rate or amplitude 

was measurable in this study. More accurate measurements of both swimming characteristics 

and physiological responses during playback responses are necessary in 

order to determine the degree to which repeated exposure to vessel approaches are 

affecting the manatee energy budget or stress levels. Technological advances in tag 

construction and measurement sensors may soon allow for the recording of these 

critical parameters (Johnson and Tyack 2003). 

In summary, the playback technique presented here permits the investigation of 

numerous questions associated with manatee disturbance, threshold level, etc. without 

the risk of injury associated with the unpredictable behavior of wild animals 

during directed vessel approaches. This methodology has identified that vessel approaches, 

especially by PWCs and fast approaching watercraft, are a cause of manatee 

disturbance. This may be of regulatory concern, as harassment is prohibited in the 

Unites States by the Marine Mammal Protection Act. Manatees were also shown to 

hear and respond to boats approaching at idle speeds. Much more information is 

needed to determine how to minimize this disturbance in order to meet the criteria 

for species downlisting as outlined in the Florida Manatee Recovery Plan (U.S. Fish 

and Wildlife Service 2003). For example, the measured responses in this study were


only made during feeding and resting behaviors in grass bed habitats. Behavioral 

state and habitat type may have significant impacts on the motivation to react, and 

responses in other behavioral contexts (e.g., actively socializing) and habitats should 

be investigated. 


The success of this project would not have been possible without the help of numerous 

people. The interns and staff in the Manatee Research Program at Mote Marine Laboratory were 

critical to the field efforts. Special thanks are extended to Doug Nowacek for his input on initial 

project design. Thanks are also extended to Gretchen Hurst, Joe Gaspard, and Marie Chapla 

for their help with stimulus recordings. All playbacks were conducted under the guidelines 

of U.S. Fish and Wildlife permit MA071799-0 issued to Jennifer Miksis and comply with all 

current laws of the country. This project was funded by a National Defense for Science and 

Engineering Graduate (NDSEG) Fellowship, P.E.O. Scholar Award, and American Association 

for University Women (AAUW) Dissertation Writing Fellowship awarded to Jennifer Miksis. 

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Received: 9 May 2006 

Accepted: 5 February 2007

MARINE MAMMAL SCIENCE, 15(1): 102-122 (January 1999) 

0 1999 by the Society for Marine Mammalogy 

BEHAVIORAL SAMPLING METHODS FOR 

CETACEANS: A REVIEW AND CRITIQUE 

JANET MANN 

Department of Psychology and Department of Biology 

Georgetown University 

Washington, DC 20057, U.S.A. 

E-mail: mannj2@gunet.georgetown.edu 

ABSTRACT 

Behavioral scientists have developed methods for sampling behavior in or- 

der to reduce observational biases and to facilitate comparisons between stud- 

ies. A review of 74 cetacean behavioral field studies published from 1989 to 

1995 in Marine Mammal Science and The Canadian Journal of Zoology suggests 

that cetacean researchers have not made optimal use of available methodology. 

The survey revealed that a large proportion of studies did not use reliable 

sampling methods. Ad libitum sampling was used most often (59%). When 

anecdotal studies were excluded, 45% of 53 behavioral studies used ad libitum 

as the predominant method. Other sampling methods were continuous, one- 

zero, incident, point, sequence, or scan sampling. Recommendations for sam- 

pling methods are made, depending on identifiability of animals, group sizes, 

dive durations, and change in group membership. 

Key words: methods, sampling, observations, behavior, vocalization, Ceracea, 

ethology, quantitative. 

Researchers studying the behavior of cetaceans at sea face several unusual 

methodological challenges. Many cetaceans swim rapidly, range over long dis- 

tances on a daily basis, and have seasonal migrations of thousands of kilome- 

ters. Cetaceans are difficult to follow because they disappear during dives and 

do not leave long-lasting traces, such as tracks, scats, or dens. 

To meet these challenges, cetacean researchers have developed photoiden- 

tification methods and some clever technical solutions. For example, individ- 

uals of many species can be identified by natural markings, allowing research- 

ers to link sightings separated by years and thousands of kilometers (Ham- 

mond et al. 1990). Individual animals can be followed in more detail by 

tagging them with radio, acoustic, or satellite tags. Diving behavior can be 

monitored using time-depth recorders. Hydrophones and underwater video 

cameras can provide continuous data on the behavior and communication sig- 

nals of animals for shorter periods of time. 

In spite of these impressive technical advances, methods for sampling ce- 

102

MANN: BEHAVIORAL SAMPLING METHODS 103 

tacean behavior have received less attention. In this paper, I review quantitative 

observational methods typically used in cetacean studies and offer specific sam- 

pling suggestions. 

Altmann (1974) points out that most field observations of behavior involve 

sampling decisions, whether those decisions are explicit or not. 

“Sampling decisions are made wbenever the stua’ent of social behavior cannot continuously 

observe and record all of the behavior of all of the members of a social group. . , . We 

suspect that the investigator ofen chooses a sampling procedure without being aware that 

he is making a choice. Of course, he does not thereby escape fiom the consequences of that 

choice.” (Altmann 1974:229). 

The lack of an explicit protocol for sampling was termed ad libitum sam- 

pling by Altmann (1974), and she pointed out that it typically entails scoring 

“as much as one can” or whatever is most readily observable of the behavior 

of a group (Altmann 1974:235-236). These kinds of observations may be 

necessary as one learns to identify behaviors, as one plans a study, or as one 

observes rare but significant events. However, ad libitum observations suffer 

from a variety of potential biases. Different individuals may be more or less 

visible. Some behaviors may be more salient and more readily recorded than 

others. Individual animals may alter their behavior depending on how visible 

they are to other animals (and to observers). The same observer may concen- 

trate on different behaviors during different observation periods, and different 

observers may notice or attend to entirely different behaviors during the same 

observation period. Such biases indicate that ad libitum data are not appropriate 

for estimating rates of behaviors or for comparing rates across subjects or across 

studies. The selection and appropriate use of sampling methods that yield 

unbiased estimates of behavior are critical to the scientific validity of any study. 

In this paper, first I review the methods employed in the majority of recent 

cetacean field studies, including sampling method and protocols, and discuss 

the general advantages and pitfalls of each sampling method. Second, I rec- 

ommend specific sampling methods for cetaceans, depending on identifiability 

of animals, group sizes, dive durations, and change in group membership. 

Literature Survey 

To evaluate what methods are currently used by cetologists, I surveyed 

papers on cetacean behavior published from 1989 through 1995 (see Appendix 

1 for details). To limit the survey, I selected two peer-reviewed journals that 

together published the majority of studies in wild cetacean behavior, The Ca- 

nadian Journal of Zoology (CJZ, 31% of studies) and Marine Mammal Science 

(MMS, 29% of studies). 

Seventy-four studies were reviewed, 38 in CJZ and 36 in MMS. The fol- 

lowing information was noted: species, age and sex classes, number of animals, 

number of observation or recording hours, group-size minima and maxima, 

whether animals were individually identified, types of behaviors recorded (in- 

cluding vocalizations), definition of group and definition of behaviors, and

104 MARINE MAMMAL SCIENCE, VOL. 15. NO. 1. 1999 

methods of observation and sampling. In many cases, essential information in 

these categories was not provided (Appendix 1). 

CRITIQUE OF METHODS 

For every behavioral study, two basic kinds of sampling decisions must be 

made. One choice concerns which subject(s) one watches and for how long; 

the other concerns the details of how behavior is recorded (Martin and Bateson 

1986). I will discriminate these as “follow protocol” and the “sampling meth- 

od.” “Follow protocol” refers to how long an observation extends and to wheth- 

er researchers follow a group or an individual animal. “Sampling method” 

refers to the procedures used to sample the behavior of individuals or groups. 

Such a distinction is necessary because the sources of error or bias differ ac- 

cording to each protocol and according to each method. For example, in the 

ethological literature the term “focal-animal sampling” is used to refer to data 

collection that involves sampling of behavior of one individual for a set period 

of time. However, there are really two separate components, the follow protocol 

(following an individual) and a sampling method (which could be continuous 

sampling, point sampling, etc.). To state only that one’s method is “focal- 

animal sampling” would be insufficient. For example, a researcher could collect 

data on a focal individual systematically at regular intervals or opportunisti- 

cally (ad libitum ) by irregularly noting behaviors of interest. 

In the following sections, the prevalence and the costs and benefits of dif- 

ferent follow protocols and sampling methods are discussed. Table 1 is a guide, 

illustrating how different techniques (follow protocol and sampling method) 

are likely or unlikely to be effective, depending on the characteristics of the 

animals under study. My use of the term “identifiable” in Table 1 refers to 

cases when observers can identify known individuals (such as in a longitudinal 

study) or can discriminate between animals sufficiently to keep track of the 

same animal. When I refer to “group,” both for group size and group mem- 

bership, this concerns the number of animals close enough together to be 

potentially confused with each other. 

Follow Protocol 

For the studies surveyed, five different follow protocols can be defined: 

survey, group-follow, individual-follow, tracking, and anecdote. Three studies used 

more than one protocol (e.g., group-follows and surveys). Two studies did not 

provide enough information to allow classification by protocol. 

Survey refers to encountering groups or individual animals and staying with 

those animals for brief periods to census, for example, the number of animals, 

identifications, location, and behavior. If observers typically monitor groups 

for 30 min or less, then their protocol is identified here as “survey.” Surveys 

comprised 16% (n = 12) of the studies reviewed. Surveys provide a “snapshot” 

of animal life and are very useful for tracking patterns of association and for 

analyzing demographic, reproductive, and ecological factors. Surveys are par-

MA”: BEHAVIORAL SAMPLING METHODS 105 

Table 1. Recommended uses for different sampling methods depending on subject 

characteristics. 

Group 

Rapidly Group membership Dive time 

identifiable? size rate of change 

Method yes no*


Appropriate sampling techniques applicable during group-follows are dis- 

cussed below (see Table 1). 

If observers monitor an individual regardless of whether the animal is in a 

group or not, their protocol is classified as indiuidaal-follow. Only 12% of the 

studies reviewed used this protocol. The indiuidad-follow is roughly equivalent 

to focal-animal sampling. The critical feature of this method is to focus on 

one animal and systematically record behavior that is defined a priori. When 

sampling individual behavior, researchers may still collect ad libitam data on 

other animals or scan the group at regular intervals to determine group mem- 

bership. However, with few exceptions, data collection on non-focal animals 

should not compromise focal data. 

The individual-follow enables the observer to focus on the individual ani- 

mal’s “perspective.” What is the day in the life of that animal like? Who do 

they approach, avoid, stay close to, interact with, mate with, and fight with? 

Observing the continuous stream of individual behavior in different contexts 

is central to the understanding of the dynamics of social relationships. Time- 

budget data for individual animals are more appropriate for most studies than 

group-activity data because individuals of varying age and sex have different 

behavioral and ecological strategies. Both methodological and theoretical ar- 

guments support focusing on the individual as the unit of analysis. Selection 

operates at the level of the individual (Williams 1966), and this perspective 

is critical to understanding the behavioral and reproductive strategies of ce- 

taceans. Group-living cetaceans may rely on each other for survival and repro- 

duction, but the costs and benefits of group living are unlikely to be shared 

equally among all group members. Measures of such variation are particularly 

relevant to the study of how natural and sexual selection has shaped the evo- 

lution of social systems and behavior patterns in a species. 

The success of systematic sampling with the individual-follow depends on 

how rapidly animals can be identified or discriminated from other group mem- 

bers when they surface (Table 1). Several factors influence this, including the 

size and stability of groups and the duration of dives or “out-of-sight’’ periods. 

The optimal situation for individual-follows is that of a small stable group 

where individuals can be identified as soon as they come into view. If indi- 

viduals are not readily identifiable upon surfacing, individual-follows may still 

be used if the animals are solitary much of the time (e.g., humpback whales). 

Group size is also a factor. No matter how identifiable an animal is, if there 

are hundreds of animals, it will be hard to keep track of a focal animal (Table 

1). Brief focal samples, spanning 5 min or less (one or two surfacing bouts), 

may. be appropriate under such conditions. Individual-follows might be facil- 

itated by focusing on a readily identifiable member (i.e., based on size, marks, 

tags, or radiotracking), although the potential biases inherent to such selection 

must be considered. 

Although sampling decisions depend on the observation conditions, long 

individual focal-follows are highly recommended where possible. Rogosa and 

Ghandour (1991) have argued (mathematically) that short samples are one of 

the biggest sources of unreliability in sampling uncommon behaviors. Long


individual follows may also be practical, given the search-time costs of sam- 

pling different individuals on the same day. If the researcher is likely to lose 

track of the focal animal in certain behavioral contexts (e.g., foraging), then 

scans or other sampling techniques may be applied to prorate or correct for 

such biases. Individual follows often enable the observer to identify the sources 

of sampling bias (e.g., conditions that prove difficult for monitoring individual 

behavior). If the study design requires following individuals for long periods 

of time, but individuals are not rapidly identifiable, then visual, radio, or 

acoustic tags may be necessary. 

Tracking refers to studies that electronically monitor individuals’ locations 

or behavior (through hydrophones, transponder tags, or other devices). Track- 

ing is particularly valuable if researchers need to continuously record the be- 

havior of an animal over long periods. Six studies (8%) reviewed here tracked 

small numbers of animals using radio and transponder tags to record diving 

and vocal behavior. This approach can be relatively expensive, and the attach- 

ment process or device may affect behavior. Sample sizes tend to be small in 

tracking studies. 

An anecdote is a descriptive report of a single event or series of events, such 

as birth or predation. Twenty-eight percent (n = 21) of the studies analyzed 

here were classified as anecdotes. Anecdotes are a valuable means of describing 

rarely observed events. 

The survey and group-follow may be considered “group-protocols”-where 

groups are monitored unless animals are alone. The individual-follow is an 

“individual-protocol”-where a specific individual is monitored regardless of 

whether or not it is a member of a group. Tracking can involve groups or 

individuals. The merits of different protocols must be weighed against their 

impact or influence on the animal’s behavior. Few data are available on whether 

or how tagging, equipment noise (e.g., engine, tag, depth sounder), and pro- 

longed vs. brief follows directly affect the behavior of cetaceans. Indirect effects 

may also occur by alteration aQ the behavior of cetacean prey or predators. By 

combining different approachies, or directly testing for the effects of these 

approaches, observers can find ways to minimize their impact on behavior. 

Sampling Methods 

Given that a researcher has, chosen a protocol for following the animals, a 

number of sampling methods may be used. These include ad libitum, contin- 

uous, fical-group, one-zero, point, scan, predominant activity, sequence, and all-event1 

incident sampling (defined below). The success of each sampling method de- 

pends, in part, on whether a researcher is focusing on events (brief behaviors, 

measured in frequency) or states (long behaviors of measurable duration). Al- 

though the distinction is convenient, events and states are on a continuum 

(ie., all events have durations and all states have frequencies). 

Ad libitum sampling-Ad libitum samples are “typical field notes” (Altmann 

1974). The observer writes down what seems of interest. Ad libitum sampling 

does not involve systematic constraints on what is recorded and when it is


recorded. The initial phases of behavioral study often involve some ad libitzlm 

sampling in order to delineate and define behaviors and research questions. 

Most observers continue to collect some ad libitum data throughout the course 

of their study. In the survey of studies, the sampling method was classified as 

ad libitum only if it was the predominant method used. Ad libitum sampling 

was the most common technique used (59% of studies). Ad libitum sampling 

is useful for certain kinds of comparisons, but not for estimating rates of 

behavior or for comparing behavior patterns of different age or sex classes 

(Altmann 1974). As Altmann points out, some animals may be more notice- 

able, either because of their behavior (or activity level), size, or level of habit- 

uation. Ad libitum sampling may be applied during individual focal-follows 

(e.g., prey captures by focal animal) or group-follows (e.g., displays). Ad libitum 

data are valuable for looking at the direction of interactions or at what happens 

within a dyad if the direction of the interaction is unlikely to be influenced 

by the probability of seeing it. For example, ad libitum data are commonly 

used in ethology to assess dominance relationships, where one animal “wins,” 

and the other “loses” an agonistic interaction (e.g., see Samuels and Gifford 

1997). Rates of agonistic interactions cannot be acquired through ad libitum 

sampling, because the likelihood of seeing an interaction may be affected by 

the rank, size, sex, or other characteristics of the animals (e.g., conflicts between 

adult males are more likely to escalate and thus be observed than conflicts 

between adult females). However, given that two animals are fighting, the 

outcome of the fight is unlikely to influence or be influenced by the probability 

of seeing the interaction. Ad libitum sampling is effective for examining di- 

rected displays, in which both signaller(s) and recipient(s) can be determined. 

Sociomatrices are an excellent means of illustrating some patterns of interac- 

tion with ad libitum data. A sociomatrix has all potential interactants listed 

on the top and along the side, with one axis indicating actor or “winner” and 

the other as recipient or “loser.” Frequencies are tallied within each cell of 

interactants. When dominance hierarchies are linear, for example, then most 

entries will fall on one side of the diagonal. Sociomatrices can be applied to 

other behaviors sampled ad libitum. Mann and Smuts (in press) recorded 1,3 1 1 

rubbing events between nine wild Tursiops newborns and their mothers during 

focal individual-follows (189 h). Rubbing rate could not be determined, nor 

whether some infants rubbed more than others. But rubbings were extremely 

asymmetrical, with infants initiating and performing 99% of the rubbing on 

their mothers. 

Ad libitum data are a valuable part of any field study but should not be 

represented as rates, proportions, frequencies, or other unbiased estimates of 

behavior. The use of ad libitum data for anecdotes is perfectly appropriate. Rare 

events such as predation, a birth, or a lethal fight, can provide critical infor- 

mation and insights, and ad libitum sampling is likely to be the only way such 

events are recorded. 

Continuous sampling-Alternate names: event sampling, frequency sampling, 

focal-animal sampling. Continuous sampling is a systematic record of fre- 

quencies or durations for a specified set of behaviors. Researchers occasionally


use the term “focal-animal sampling,” to indicate continuous sampling of 

behavior during an individual-follow. Measuring the exact times (and dura- 

tions for behavioral states) of every occurrence of a behavior is very demanding 

for the observer. Scoring event frequencies within time blocks can simplify 

data collection. The reliability of continuous data can be easily compromised 

if the observer tries to record too many behaviors at once, especially when the 

animals are active. Thus, Altimann (1974) recommends that this method be 

used for one or two animals at most. 

Continuous data on associa.tions, diving behavior (with transponder tags), 

other behaviors, or vocalizations were collected in 14% (n = 10) of the studies 

surveyed. In four of these studies researchers observed animals directly. Two 

studies used tags to track individuals. The remaining four collected continuous 

data on small groups of animals using videotape or multiple observers. 

Continuous sampling of behavior is relatively simple for activities at the 

surface (during surfacing bouts). Surfacing-bout durations, breath frequency, 

dive types, surface-display rates, and synchronous surfacings of the focal animal 

and others may be recorded on a continuous basis for many dolphin and whale 

species. Even deep-diving animals, such as sperm whales, may have prolonged 

bouts of socializing at the surface (Whitehead and Weilgart 1991). If the 

activities are brief, or difficult to time, then they can be scored as events 

(frequencies), rather than states (onset to offset). Records of behavior sequences 

are typically intact in continuous sampling. As Table 1 indicates, continuous 

sampling is most likely to succeed when animals are rapidly identifiable, live 

in small groups, and dive for short periods. Under these sampling conditions, 

observers can keep track of a specific individual for long periods of time. 

Continuous data are the richest source of information on social behavior and 

relationships, because such dlata include information on details, sequences, 

actors and recipients, rates and durations of behavior for individual animals. 

While it is simple to record vocalizations continuously using a tape recorder, 

for these data to qualify as continuous data for an individual follow, the ob- 

server must be able to identify which vocalization comes from the focal in- 

dividual. Use of tags that can record or transmit acoustic data is one technique 

for achieving this (e.g,, Tyack 1985, Tyack and Recchia 1991). Another tech- 

nique involves passive acoustic localization (e.g. Clark 1980, Freitag and Tyack 

1993, Frankel et al. 1995). Fusion of these acoustic and visual data remains a 

challenge to anyone interested in cetacean communication. As with behavioral 

studies, the study of cetacean vocalizations still hinges upon such basic infor- 

mation as the species, sex, or age class of the animal producing the call. The 

study of how these sounds are used in social communication will require 

increased application of methods to identify which animal produces which 

sound during interactions wit:hin and between groups. 

Focal group sampling-Alternate names: focal subgroup sampling, group 

sampling, predominant group activity sampling. Focal-group sampling is a 

continuous assessment of group activity. Group activity may be scored at in- 

tervals (e.g., indicate predominant group activity every 5 min) or continuously 

(e.g., the group rested from 1122-1147). This method is widely used in ce-


tacean research when observers follow groups, and Altmann (1974) has been 

cited in support of it (e.g., Shane 1990). Altmann (1974) used the term “focal 

sub-group sampling” to refer to continuous sampling with more than one 

individual. However, Altmann described focal sub-group sampling as appro- 

priate only under a very restricted set of conditions “in which all individuals 

in the sample group are continuously visible throughout the sample period 

. . . if one is working with observational conditions that are less than perfect, 

focal-animal sampling should be done on just one focal individual at a time, 

or at most, a pair (e.g., mother and young infant)” (Altmann 1974:243-244). 

Twenty-seven percent of the studies surveyed here (45% of ad libitum studies) 

used “focal group sampling.” These studies scored “group behavior.” Dozens 

of animals, not pairs, were sampled using focal-group sampling. I chose to 

classify these studies as ad libitum because none of the conditions necessary for 

unbiased focal-group-sampling were met. That is, observers could not have 

continuously observed all animals equally in a group regardless of activity. 

Some observers appeared to visually assess group activity, perhaps by infor- 

mally scanning the group. However, this method is not explicit enough in 

how subjects were sampled and does not differ in any substantial way from 

ad libitum sampling. 

A few studies identified their method as predominant group-activity sam- 

pling. This should not be confused with predominant activity sampling (de- 

fined below). Predominant group-activity sampling is essentially the same as 

“focal group sampling” and was coded as ad libitum in the survey. During 

predominant group-activity sampling, the observer defines group activity 

based on an assessment of what most (>50%) of the group is engaged in over 

an interval, focusing on the proportion of individuals estimated to be engaging 

in a behavior, not the proportion of time an individual engages in a behavior for 

that interval. An estimate of predominant group activity can be achieved by 

explicitly scan sampling over 50% of the individuals in the group, rather than 

by “watching the group.” 

Altmann (1974) prescribed a restricted set of conditions for focal sub-group 

sampling because of the many biases inherent to watching groups. First and 

foremost, the observer’s attention is naturally drawn to animals that are most 

visible, most active, or most interesting. No observer can possibly continuously 

track and record all behavior of all individuals simultaneously under all con- 

ditions; it is difficult enough to record the behavior of one animal. Group 

activity may be determined if all members of a small group are cohesive and 

engaging in the same behavior, such as resting closely at the surface, but it 

may be difficult to determine if some animals are engaging in other activities. 

The accuracy of focal-group sampling is dependent upon group size, cohe- 

siveness, and activities of the animals, thus potentially introducing biases into 

data collection. Some behaviors, such as socializing, may be particularly ob- 

vious to observers, and even though most of the animals are resting, one might 

score the more visible behaviors as group activity. While using group-sam- 

pling, observers are often making implicit assumptions about the relative im-


portance of behaviors of different age and sex classes. If two mothers are hunt- 

ing, but their calves are traveling, should one call it hunting or traveling? 

With video, continuous sampling of groups is possible because observers 

can rewind the tape and code the behavior of different individuals separately 

(thus making the process equivalent to conducting multiple continuous focal- 

animal samples simultaneously). However, simultaneous behaviors of different 

individuals within the same group are likely to depend upon one another, 

which must be taken into account for statistical analyses. Focal-group sam- 

pling is not only used during the group-follow protocol, it is also used during 

surveys to identify “group activity.” However, this too is subject to the same 

criticisms. 

One study (Fragaszy et a/. 1992) has compared focal-group sampling with 

focal-individual point sampling and scan sampling (see definitions below). 

This study, although on primates, is particularly relevant for cetacean studies 

because, like cetaceans, capuchins and squirrel monkeys move in and out of 

view and are difficult to follow for continuous periods of time. Fragaszy et al. 

(1992) compared foraging time budgets of squirrel monkeys using both focal- 

group sampling and focal-animal point sampling methods and concluded that 

focal-group sampling overestimated foraging considerably. They came to this 

conclusion by correlating individual-focal point sampling rates with focal- 

group sampling rates. The focal-group sampling error rate (computed by JM) 

ranged between 39% and 63%. They also compared scan sampling of capuchin 

monkey groups to focal-animal point sampling. Scan sampling fared much 

better. When time budgets for scan sampling and focal-animal point sampling 

for foraging among capuchins were compared, the error rate was only 0.8% 

(computed by JM). For other, less frequent behavioral states, the error rates 

for scan sampling ranged from 10% to 26%. Focal-group sampling error rates 

for other behavioral states were not compared. However, error rates are lowest 

for more prevalent behaviors, and foraging was the most common state. Thus, 

error rates are likely to increase for other states. Such error rates should give 

pause to anyone considering group-sampling. 

One-zero sumpling-Alternate names: time-sampling, Hansen frequencies, in- 

terval sampling, partial interval sampling, method of repeated short samples, 

and modified frequencies. One-zero sampling entails scoring whether or not a 

behavior occurs during an interval (e.g., 30 sec), rather than scoring how fre- 

quently or how long the behavior occurred. For example, an observer may 

score whether or not an animal vocalized during 30 seconds, or whether or 

not it rubbed, rather than the frequency of vocalization events or the duration 

of rubbing (a state). Nine percent of the studies surveyed employed one-zero 

sampling. With few exceptions, this technique is not recommended, because 

one-zero scores do not represent frequency or duration and are prone to very 

high rates of sampling error (see Mann et al. 1991). Although one-zero sam- 

pling has no recommended uses (Altmann 1974), there are some natural types 

of one-zero data (categorical variables) that are not represented by the flow of 

continuous behavior but may occur over very long intervals. For example, if 

group fissions and fusions are rare, then whether or not an animal joins a


group during a day or field season is a significant piece of information and 

may be more biologically meaningful than the absolute rate. However, one 

must already know something about the rates and durations of behaviors of 

interest before employing one-zero sampling. 

Researchers sometimes use one-zero events to define states. That is, one- 

zero data may assist in the development of an ethogram but not be part of 

the sampling method. For example, if two animals are seen in contact during 

an interval, this may “define” socializing regardless of the duration or fre- 

quency of contact. Or, one might define foraging based on whether or not the 

animal flukes-up at the dive. It is important then to distinguish between the 

use of one-zero (categorical) information to help define behaviors that are pre- 

sumed to be continuous and treating one-zero scores as state behaviors them- 

selves. 

Point sampling-Alternate names: instantaneous sampling, on-the-dot sam- 

pling, time sampling. Point sampling entails scoring activity as a “snapshot” 

at a given moment (e.g., every 30 sec). The observer may score states, such as 

distance to others, activity, or other information on a point-sampling basis. 

Five percent of the studies surveyed used point sampling. It is a reliable 

method that is widely applied in ethological studies but has been rarely used 

for cetaceans. One possible explanation is that the “point” often happens when 

the animal is submerged. The few studies reviewed here that used point sam- 

pling did so by electronically tracking the animal. For direct observations, 

point sampling can still be applied with two basic strategies. (1) The animal’s 

behavior is sampled at the first surfacing after the interval point. Two factors 

may lead to sampling biases. One ends up sampling surface behavior rather 

than the behavior occurring underwater at the point. By examining the rela- 

tionships between surface and subsurface activities, these biases may be min- 

imized. Another bias is that the behavior is not sampled at regular intervals, 

but at intervals determined in part by the subject’s surfacing and diving be- 

havior. If the observer sampled at 1-min intervals, and animals tended to 

remain close to the surface during socializing and dive deeply for longer pe- 

riods during foraging, then the observer could successfully sample socializing 

but would miss several sampling intervals during foraging. Social behavior 

would be overrepresented in relation to foraging. This problem can be alle- 

viated by establishing a point interval greater than the typical long dives of 

the subject. (2) The second strategy is to use point sampling for behavioral 

states if one can assume that the state continues when the focal animal moves in and 

out of view. Observers often infer behavioral state based on surfacing pattern, 

proximity of other individuals, and other cues (e.g., flukeprints or bubbles at 

the surface). The observer may apply a convention such as scoring a behavioral 

state at the “point” if the animal engaged in the behavior prior to diving or 

disappearing from view and was engaged in the same behavior upon surfacing. 

This convention may be applied if the “out-of-sight” periods tend to be much 

shorter than the bout duration of the behavioral state. Another convention is 

to score the behavior as that last observed, or, alternatively, first seen upon 

surfacing. Such conventions must be explicitly defined, justified, and the po-


tential biases considered. As Table 1 suggests, point sampling can be applied 

under many conditions but becomes problematic if dive times or out-of-sight 

periods are long and group sizes are large (making it difficult to keep track 

of an individual animal). 

Point sampling can be a very useful method to determine time budgets or 

diurnal patterns of behavior. This method is also a useful supplement to other 

focal-individual sampling methods. For example, the observer may record an 

animal’s speed at 5-min intervals, or note a focal animal’s nearest neighbor 

based on who surfaces closest to the focal animal at the first surfacing after 

each 10-min interval. Although point sampling is typically recommended for 

behaviors of appreciable duration, activity can be more difficult to score on a 

point-sampling basis. In reality, even with the animal in full view, it may take 

several seconds or more to “decide” what an animal is doing. It is important 

that the observer decide as quickly as possible, so shelhe does not inadvertently 

wait until the animal does something that is easier or more interesting to 

score. Brief behaviors or events are difficult to observe accurately with point 

sampling because such behaviors are often missed at the “point.” 

Scan sampling-Scan sampling entails taking a “point” or “instantaneous” 

sample of an individual’s behavior or location before moving to the next animal 

and doing the same. Scans are conducted either at regular intervals (e.g., sample 

each animal at 10-sec intervals), or as quickly as possible (ie., search for the 

next animal as soon as the last was sampled). Both point and scan samples are 

good techniques for measuring states, but brief events are likely to be missed. 

Three percent of the cetacean field studies reviewed here used scan sampling. 

Scan sampling is very valuable for sampling behavior when focal-individual 

observations are not possible or desirable, or if the researcher wishes to keep 

track of group activities. An explicit scan-sampling technique should also be 

considered for surveys of groups, rather than using ad libitam sampling to 

identify “group activity.” Observers sometimes use a random scan-sampling 

schedule, or just scan from one side of a group to the other. Alternatively, if 

group sizes tend to be large and the animals move rapidly, but age or sex 

classes are distinctive in size or markings, then the researcher may scan age 

and sex classes separately (e.g., scan large males, then females with dependent 

calves, then immature animals). This would leave some agehex classes unsam- 

pled but would enable the observer to scan a group of fast-moving animals 

more effectively. 

Scan sampling and point sampling share practical difficulties: the time it 

takes to decide the animal’s activity and out-of-sight or diving periods. One 

may employ the same strategies for scan sampling as for point sampling, but 

with scan sampling the observer samples each individual only once per session. 

In some cases, the observer may need to watch each individual for 3 min or 

more (approximating a short individual-follow) but uses the midpoint (e.g., 

minute 2) to define the behavioral state. Thus, one data point is taken for 

each animal in succession, although each observation period is longer than for 

a typical scan. The same conventions used for point-sampling out-of-sight 

periods can be adapted to scan sampling.

114 MARINE MAMMAL SCIENCE. VOL. 15. NO. 1. 1999 

Potential uses for scan sampling are varied (see Table 1). First, an observer 

may scan a group at fixed intervals (e.g., every 10 min) to assess which is still 

present, which is close to a focal animal, etc. Second, an observer may scan a 

group to rapidly estimate group activity by identifying each animal’s activity 

as it surfaces. This is only possible for groups where one can keep track of 

each individual within the group during surfacing and depends in part on the 

degree of interindividual overlap in surfacing bouts. The observer may be able 

to scan rapidly enough to minimize the likelihood of resampling the same 

individual or scan from the front to the back of a group if direction changes 

are infrequent. If the scan procedure inadvertently allows for repeat sampling 

within a session, then the resampling of highly identifiable individuals would 

alert the observer to this problem. Third, an observer might use it to assess 

nearest neighbors for each animal. Fourth, one could record both activity and 

nearest neighbor for each group member. If group scans are conducted during 

individual-follows, then it is important that the scans can be completed very 

quickly to prevent the observer from being distracted from the focal individ- 

ual. With scan sampling, cetacean researchers can broaden their dataset to look 

at coordination of group activities and refined measures of association for a 

number of animals of different age and sex classes. 

Predominant activity sampling-Predominant Activity Sampling (PAS), de- 

veloped by Hutt and Hutt (1970), refers to scoring individual behavior as the 

predominant activity over some interval (e.g., 30 sec), only if that behavior 

occupied 50% or more of that interval (>15 sec). This method is only useful 

for measuring states. No studies in the survey used PAS. It is an empirically 

valid technique for estimating the proportion of time during which behavioral 

states occur (Tyler 1979). Very brief behaviors or displays (events) will not be 

represented in PAS data unless the observer uses very short intervals. It is 

important that the interval length is brief enough to capture the briefest states 

of interest. 

PAS is useful for sampling animals that go in and out of view for brief 

periods. In a sample of Ti~rsiops calves, some types of data have been collected 

using both focal individual point samples and focal PAS simultaneously (J. 

Mann, unpublished data). Thus calf activity budgets could be compared based 

on sampling type. For example, “calf position swimming” (when the calf is 

in contact under the mother) was measured using both point sampling (in- 

stantaneous measures of swim position at first surface after each 2.5-min in- 

terval) and PAS (calculated from the continuous data on observed onsets and 

terminations of calf position swimming). I compared the percent time swim- 

ming in calf position for 19 calves in my longitudinal sample. Each calf was 

observed during focal-individual follows for 10-15 h per yr for one or more 

years. The sum of observation hours for all calves across all years was 750. 

Each infant had a PAS and point sampling percentage for each year, for a total 

of 40 calf-years (an average of two years or samples per calf). The PAS per- 

centages and point sampling percentages were correlated by treating each in- 

fant observation year as independent. This yielded a significant value (Spear- 

man’s rho = 0.97, n = 40, P < 0.0001). The mean percent error rate for PAS


was 3.2%. Several methodologists (e,g., Tyler 1979) have demonstrated the 

validity of PAS and point sampling using statistical models, but no one has 

contrasted these methods using actual observational data. 

Incident sampling-Alternate names: all-event sampling, all-occurence sam- 

pling, all-animals sampling. Incident sampling entails scoring all behavioral 

events of a specific type in a group. This method is not applicable for most 

behavioral states. The observability of the events is key to the success of this 

method. The behaviors themselves must be obvious enough to alert the ob- 

server (e.g., breaching). In addition, the observer must be able to record all 

the events regardless of how many animals are present. Thus, for incident 

sampling to be successful, the behavior must be sufficiently infrequent to allow 

complete recording for the group. As Altmann points out, this is a form of 

continuous sampling (referred to as focal animal sampling in her paper) of a 

group for a restricted set of behaviors. However, with continuous sampling, 

the individual animals are identified. During incident sampling, distinctions 

between subjects may or may not be made. Observers should still make every 

effort to determine whether the same or different animals are exhibiting the 

behavior(s). Two areas can be problematic. First, animals may tend to repeat 

displays, thus becoming overrepresented in the dataset. Second, if group com- 

position changes often (Table 1) it may be difficult to calculate event rate as 

a function of group size or structure. 

In the survey, 16% of the studies used incident sampling. Studies that 

identified their method as “focal-group-sampling” were sometimes coded as 

using incident sampling if they scored a very restricted set of obvious behav- 

iors. For example, breaches and lobtails are so visible that observers are likely 

to detect each occurrence within a group. Similarly, if observers could deter- 

mine how many animals were within acoustic range, then incident sampling 

could apply to studies of vocalizations. 

Incident or all-event sampling is valuable for cetacean researchers who wish 

to focus on specific dramatic or easily recognized events that involve few an- 

imals. For example, observers could use this method to compare successful and 

unsuccessful killer whale hunting attempts via beaching. Dramatic surface 

percussive displays, such as breaching or lobtailing, can also be observed re- 

liably in groups (Waters and Whitehead 1990). Incident sampling requires 

that the observer systematically record every event. Incident sampling may be 

adopted with a group protocol, but the observer should still be able to dis- 

tinguish which animal (or agehex class member) is engaging in the behavior 

to avoid misattributing the behavior pattern equally to all individuals. 

Sequence sampling-In sequence sampling, the observer focuses on sequences 

of behavior or on particular interactions, rather than individuals, and system- 

atically records all relevant behaviors that occur during the event(s), main- 

taining the sequences of behaviors in the record (Altmann 1974). Parameters 

defining how an interaction begins and terminates must be specified in se- 

quence sampling. For example, observers may score sequences of behaviors 

among surface-active groups of humpback whales by defining the beginning 

of the sequence as “male humpback whale challenges principal escort by ap-


proaching within 50 m” and terminating the sequence when either the chal- 

lenger or the principal escort separates more than 50 m from the female for 

30 min. It is distinct from incident sampling because during sequence sam- 

pling multiple events may occur in a group, but the observer focuses on the 

start of the first event seen and records that particular event or interaction to 

completion (even if other group members engage in similar behaviors at the 

same time). Only one of the studies surveyed used sequence sampling. 

Sequence sampling is recommended for very observable behaviors but can 

be applied under a broad range of field conditions (see Table 1). The researcher 

must be able to determine when the sequence begins and ends and be able to 

discriminate between, although not necessarily identify, the interactants. The 

individual animals may be hard to identify if they communicate over long 

ranges and move in and out of the observer’s view. For example, if the re- 

searcher wants to know whether breaching animals attract or repel others, s/ 

he can use sequence sampling to test whether animals are likely to approach 

or leave the animal who breached (e.g., within 10 min of the first breach). 

Sequence sampling is excellent for determining the conditional probabilities 

of behavior sequences. 

RECOMMENDATIONS 

Although tightly focused and informative studies peppered the literature, 

the survey of CJZ and MMS revealed two shortcomings in studies of cetacean 

behavior. First, a large proportion of studies used ad libitum sampling, which 

is replete with bias. Second, there was little consistency in reporting behavioral 

data, sampling methods, hours of observation, behavioral and group defini- 

tions, and number of subjects. This information is critical to evaluation of the 

claims of any study. Furthermore, the comparability of results and hopes of 

replication are lost if this information is not provided. Information about 

equipment (cameras, film, boat, motor, tape recorders, etc. ) was frequently 

reported, but basic methodological information regarding subjects and pro- 

tocol was sometimes lacking. 

To allow evaluation of statistical power, it is important to indicate the 

number of animals observed and how long each animal was observed. Re- 

searchers usually reported the number of animals identified in the population 

but not the number of animals observed. Sample sizes can be determined only 

when animals are observed individually. Similarly, only a few studies treated 

each subject, rather than each observation, as independent. As Milinski (1997) 

points out, this is a form of pseudoreplication, one of the “deadly sins” in the 

study of behavior. 

Group size and definition of group are needed, as well as a statement of 

protocol used if group composition changed. I recommend proximity-based 

measures, because this method is quantifiable and does not rely on behavioral 

sampling to determine group membership. “Coordinated-behavior” definitions 

make implicit assumptions about proximity, because observers cannot assess 

the activities of animals who are kilometers away. Furthermore, individuals at

MANN: BEHAVIORAL SAMPLING METHODS 117 

close range may be engaged in more than one activity that is shared with 

those farther away. An explicit definition of group, and a rationale for the 

definition in terms of the study goals, is essential. 

Specific details of how behaviors were defined and how behaviors were sam- 

pled should be included, using either standardized terms from the ethological 

literature or descriptions. Only a few studies of those reviewed used standard 

sampling terms described by Altmann (1974) and others. All studies of ce- 

tacean behavior should provide the basic methodological information described 

in this review. Following are more specific recommendations regarding the 

uses of different sampling protocols and techniques, with special consideration 

of how to reconcile unbiased observations under ideal conditions with the 

imperfect conditions that cetacean biologists face. Additional detailed discus- 

sion of methods and statistical comparisons of different observational methods 

are available elsewhere (see Altmann 1974, Dunbar 1976, Tyler 1979, Martin 

and Bateson 1986, Mann et al. 1991, Rogosa and Ghandour 1991). 

Follow Protocol 

Sampling biases in group-follows and surveys can be minimized by using 

scan sampling, incident sampling, or sequence sampling methods. Monitoring 

groups (surveys and group follows) is valuable when the goal is to gain a 

“snapshot” of group life through surveys (e.g., habitat use by foraging com- 

pared to resting groups) when observation conditions do not permit tracking 

of individuals (but tracking of groups is possible), when research questions 

focus on the synchrony or coordination of group members, or when the study 

focuses on sequences of very observable behaviors. To identify the predominant 

group activity during a survey, observers can scan-sample >50% of the group 

members. This may be possible for large groups of dolphins or whales that 

are visible at the surface for long enough to be scanned. If group sizes are in 

the hundreds or thousands, then a protocol for random scan sampling of a 

subset of the group may be developed. Sampling biases, such as number of 

scans per individual as a function of group size, must be taken into account 

during data reduction. Researchers may track a group and record all occur- 

rences of certain very obvious behaviors, thus using incident sampling. Se- 

quence sampling may also be applied if observers are interested in sequences 

of behavior during specific types of interactions, such as cooperative hunting 

in killer whales. Focal-group sampling is not recommended, because this 

method does not explicitly or systematically sample individuals or behaviors 

in groups. 

Focal-individual sampling methods with the application of continuous, 

point, and/or predominant-activity sampling, are critical tools for insuring 

reliable estimates of behavior. The individual is the natural unit of analysis 

for behavior. Data can be pooled by individual, and data from different indi- 

viduals can often be treated as independent (Machlis et ul. 1985). When ob- 

servers cannot identify or discriminate which individual produces a behavior 

(e.g,, during scan- or all-event sampling), this makes it difficult to identify

118 MARINE MAMMAL SCIENCE. VOL. 15. NO. 1. 1999 

independent units for statistical analysis. This can present problems with the 

group-follow protocol. 

General Sampling Problems: Deep Divers, Large Groups, and Cowespondence 

Between Surface and Subsurface Behavior 

The correspondence between surface (observable) and subsurface (often 

unobservable) behavior is unknown for most studies of cetaceans, but such 

information could help in assessing the biases in relying on surface behavior 

alone. For example, some animals forage at depth and not during surfacing 

bouts. One option is to define the surfacing breaks between foraging dives as 

part of the continuous state of “foraging.” Other behaviors may not change at 

the surface (e.g., socializing, resting, traveling). Although it is still valuable 

to record surface behavior even though no correspondence to subsurface be- 

havior is implied, such sampling decisions should be indicated clearly in the 

methods section of the article. 

All ethologists face difficult decisions when their subjects disappear from 

view. These “out-of-sight’’ periods may be treated differently, depending on 

the animal under study. Nesting or burrowing animals may be most likely to 

disappear from view when feeding their young or engaging in sexual behavior. 

Some cetaceans may disappear for long periods when foraging. Deleting the 

time that animals are “out of sight” is desirable when animal visibility is not 

determined by or biased by animal activity. Other strategies for using “out- 

of-sight’’ periods are needed for cetaceans, because some of their activities co- 

vary with diving periods (when animals are most likely to be out of view). 

Cetaceans may rest, travel, socialize, or engage in other diverse behaviors at 

or near the surface. Certain types of social behavior may occur at depth, but 

certainly not all of them do. If the out-of-sight periods tend to be short relative 

to the bout lengths of the behavior, then ethologists might designate the 

activity for the out-of-sight period as either the last activity seen before the 

subject disappeared or the first activity seen when the animal reappears. Al- 

ternatively, the observer may consider a state continuous only if the last ac- 

tivity seen and the first activity seen after a brief out-of-sight period are the 

same. This strategy is not effective if some behaviors, such as foraging or 

hunting, consistently occur out of an observer’s view. In such circumstances, 

cetacean observers may detect foraging using other cues, including bubble 

patterns at the surface, echolocation clicks, or intermittent sightings of fish 

catches or chases. Sometimes there are signs at surfacing of what the animal 

was doing on the preceding dive. For example, bottom-feeding whales may 

surface with mud streaming from the mouth (Wiirsig et al. 1985). Thus, 

observers may use fleeting observations of events to define states or indirect 

cues (rapid surfacing, changing direction) to define “unobservable” states. One 

may also tag an individual to track behaviors at depth for comparison with 

cues visible at the surface. By combining these techniques, observers can de- 

velop behavioral definitions and systematic protocols to capture the range of 

cetacean behaviors.


Sampling from large groups of hundreds or thousands (e.g., Scott and Per- 

ryman 1991) can prove to be difficult. However, Ostman (1994) has success- 

fully completed short focal follows on Stenella longirostris in Hawaii, suggesting 

that it is possible to stay with individuals long enough to get a 5-min sample 

using an underwater observation booth built into a vessel. Scan sampling of 

large groups of unidentified animals is another possible approach. In such 

circumstances, researchers would need to scan a subset, possibly by randomly 

selecting subgroups or particular agehex classes. Videotaping for later scoring 

or photogrammetric analysis (.g., Scott and Perryman 1991) can provide data 

on association and behavior. 

Although observation conditions for studying cetaceans are rarely ideal, 

proximity between animals, synchrony in surfacing, and basic activities can 

be recorded systematically under most sampling conditions. Cetacean behav- 

ioral research could benefit greatly from a wider use of quantitative sampling 

techniques. If applied carefully, such partial but systematic observations can 

help elucidate cetacean social and behavioral ecology. 


This paper was prepared while I was a fellow at the Center for Advanced Study in 

the Behavioral Sciences in Stanford, California, with support from the National Science 

Foundation (#SBR-9022 192). Helpful comments on the manuscript were provided by 

Robin Baird, Vincent Janik, Edward Miller, Amy Samuels, three anonymous reviewers, 

William F. Perrin, Douglas Wartzok, and especially Peter L. Tyack. I was also sup- 

ported by the Helen V. Brach Foundation, The Eppley Foundation for Research, and 

Georgetown University. I thank Jeanne Altmann for igniting my interest in observa- 

tional methods in 1980. 


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Received: 10 July 1995 

Accepted: 14 January 1998


APPENDIX 1 

I conducted a search of the Science Citation Index (Institute for Scientific Infor- 

mation, Inc., 1996) using all 39 cetacean genera for keywords. The search yielded 846 

studies. To determine whether the study focused on cetacean behavior in the wild, each 

title was examined for keywords: behavior, acoustics, observations, field, captive, wild, 

and a description of the geographic location. The 846 studies were classified according 

to 14 subjects (e.g., molecular, neurophysiological, conservation, behavior); many stud- 

ies received more than one classification. Of the total, 125 studies (14.8%) in 28 

journals focused on cetacean behavior (n = 106) or vocalizations (n = 19) in the wild. 

Studies that appeared to focus strictly on population assessment (e.g., aerial counts) 

were not classified as behavioral studies. CJZ and MMS published 60% of the studies. 

The next most popular journal for cetacean behavior studies was the Journal ofMam- 

malogy, which published only 5% (n = 6). Thus, CJZ and MMS clearly represent the 

majority of relevant peer-reviewed publications in the Science Citation Index (SCI) and 

were chosen for in-depth analysis for this reason. Based on a comparison of Impact 

Factors (Impact Factor = the average number of times a paper in a journal is cited in 

the Science Citation Index within two years of publication), MMS and CJZ represent 

mid-level quality in research. Approximately an equal number of cetacean studies 

ranked above (n = 21) and below (n = 22) MMS and CJZ, with six studies (published 

in the Journal of Mammalogy) ranking the same as CJZ and one study ranking below 

CJZ but above MMS. 

Because the SCI search may have missed studies that did not use genera for key- 

words, I surveyed all issues of CJZ and MMS for all studies of free-ranging cetacean 

behavior and vocalizations published during 1989-1995. The SCI search by genera 

did not miss any studies, but one CJZ study I classified as a “behavior study” from 

the title was excluded from the review because the article’s content did not include 

behavior or vocalizations. 

The basic unit of analysis was one published article. Of 144 authors, 21 (14.6%) 

published more than one study. Of these, 14 published two studies, six published 

between three and five studies and one researcher authored or co-authored nine studies 

(using five different sampling methods). 

Species studied-Twenty-four cetacean species were studied in the 74 papers I re- 

viewed. Studies of humpback whales (Megaptera novaeangliae) were the most common 

(24%), followed by those of sperm whales (Physeter macrocephalus, 16%), and killer 

whales (Orcinus orca, 16%). Bottlenose dolphins (TurJiops truncatus) were represented in 

9% of the studies. Bowhead (Balaena mysticetus) and gray whales (Eschrictius robustus) 

were each represented in 5% of the studies. Narwhals (Monodon monoceros), Bryde’s 

whales (Balaenoptera edeni) and belugas (Delphinapterus leucas) were each represented in 

4% of the studies. Seven studies included more than one species. Of the 15 remaining 

species, only one or two studies were published on each. 

Age and sex classes sampled-Twenty studies focused on animals of a particular age 

or sex class. Otherwise, observers either did not know the ages or sexes of animals, or 

they observed animals of all ages and both sexes. No studies made quantitative com- 

parisons between age or sex classes. 

Number of animals sampled-The range of animals sampled was one to >1,000. 

Typically, researchers reported the number of animals that they surveyed or identified 

but not how many animals were observed or sampled. In 45% of the studies, the 

number of animals identified and/or sampled could not be determined. When groups 

of animals were sampled (e.g., in surveys or group-follows), 59% of the time (n=44 

studies) I could not distinguish between how many animals were individually identified 

and how many were actually observed. 

Individual identifiation-In 66% (n = 49) of the studies, researchers could identify 

individual animals. In 34% (n = 25), individual animals were not identified, although 

in about half of those (48%, n = 12), physical features of the species and reference to


other studies indicated that individual identification was possible. In all studies that 

could identify individuals, rates of individual behavior or vocalizations were not re- 

ported unless the study involved only one or two animals (n = 3 studies). 

Observationirecording hours-Twenty-eight studies (38%) did not report how much 

time was spent observing or recording behavior. Some of these studies reported the 

hours spent at sea, but this information is only useful (as an indicator of sighting 

effort) when observation hours are also presented. Sixty-two percent of the studies 

reported the number of surveys conducted or the number of hours spent observing 

animals. Only four studies treated each subject, rather than each observation, as in- 

dependent for behavioral analysis. 

Group definitions and group size-Definition of “group” is essential to assess the va- 

lidity of behavioral sampling from groups. I indicated whether or not “group” was 

defined, and if it was defined, I noted the definition. Group-size definition was not 

relevant in nineteen studies (e.g., only one animal was studied). For 55 studies (surveys, 

group-follows, anecdotes), groups of animals were observed. In 42 of these (76%), 

researchers did not define “group.” If group was defined (n = 13), proximity-based 

measures (e.g., within 10 m) or coordinated behavior (all visible animals engaged in 

the same activity) were the two most common definitions of group. 

Group-size means or ranges (minimum and maximum group size) were reported in 

38 studies. Seventeen studies did not report group size information. 

Types of behavior and vocalizations recordd-Behaviors recorded in each study were 

classified as breathing (14%), diving (30%), resting (24%), surface displays (8%), so- 

cializing (30%), feeding or foraging (43%), traveling (27%), or “other.” Association 

(proportion of time animals together) was recorded in 22% of the studies and vocali- 

zations were recorded in 38%. “Other” included births (1%) or other unusual events 

(16%). Over half of the studies (57%) provided definitions for one or more of the 

behaviors recorded. Studies were classified according to the behaviors that researchers 

recorded, not which data were analyzed. If an ethogram was given, this was noted. No 

studies reported measures of inter-observer or intra-observer reliability. 

Sound recording was used either to find or track whales or to describe the vocal 

repertoire of a species, group, or individual. Of the 29 papers that recorded dolphin 

or whale vocalizations, 28% identified species-specific repertoires or group-specific rep- 

ertoires. In one study, species-typical vocalizations were monitored to test for the pres- 

ence of the species. Identification of individual repertoires within groups was limited 

to anecdotes, but one study used passive acoustic localization to identify which animal 

was likely to be vocalizing. Fourteen percent of the studies that recorded cetacean 

vocalizations calculated vocalization rates for groups of animals but not for individuals. 

Solitary individuals were acoustically recorded for portions of one study. 

All 74 studies were classified according to sampling method: ad libitum, continuous, 

focal-group, one-zero, point, scan, predominant activity, sequence, and incident sampling. If a 

study used more than one sampling method (six studies), both were scored. The results 

of these classifications are reported in the main text.

Aquatic Mammals 2008, 34(1), 35-43, DOI 10.1578/AM.34.1.2008.35 

Distribution and Habitat Use of Antillean Manatees 

(Trichechus manatus manatus) in the Drowned Cayes Area of 

Belize, Central America 

Katherine S. LaCommare, 1 Caryn Self-Sullivan, 2, 3 and Solange Brault 1 

1 University of Massachusetts, Boston, Department of Biology, 100 Morrissey Boulevard, Boston, MA 02125, USA; 

E-mail: kslacommare1@hotmail.com 

2 Texas A&M University, Department of Wildlife and Fisheries, College Station, TX 77845, USA 

3 Sirenian International, Inc., 200 Stonewall Drive, Fredericksburg, VA 22401, USA 

Abstract 

Belize, Central America, has long been recognized 

as a stronghold for Antillean manatees (Trichechus 

manatus manatus) in the Caribbean (O’Shea & 

Salisbury, 1991). The Drowned Cayes area, in 

particular, has been noted as an important habitat 

(Bengston & Magor, 1979; O’Shea & Salisbury, 

1991; Auil, 1998, 2004; Morales-Vela et al., 2000). 

It is critical to evaluate habitat use and the relative 

importance of different habitat types within these 

cayes because this area is increasingly impacted 

by human activities (Auil, 1998). The two research 

objectives for this paper are (1) to document 

manatee distribution within the Drowned Cayes, 

Swallow Caye, and Gallows Reef, and (2) to examine 

habitat use patterns in order to identify habitat 

characteristics influencing the probability of sighting 

a manatee. Binary logistic regression was used 

to examine whether the probability of sighting a 

manatee varied in relation to several habitat variables. 

The probability of sighting a manatee across 

all points was 0.31 per scan (n = 795). Habitat 

category, seagrass category, and habitat category 

interaction with resting hole were the most important 

variables explaining the probability of sighting 

a manatee. The Drowned Cayes area clearly constitutes 

a manatee habitat area. Seagrass flats and 

cove habitats with resting holes were especially 

important habitat characteristics. 

Key Words: distribution, habitat use, Antillean 

manatee, Trichechus manatus manatus, Belize 

Introduction 

The Antillean subspecies of the West Indian manatee 

(Trichechus manatus manatus) is found in 

19 countries throughout the Caribbean, Central 

America, and South America (Lefebvre et al., 

2001). It is listed as vulnerable to extinction by 

the International Union for the Conservation of 

Nature and Natural Resources (IUCN) (2004) 

because of its greatly reduced numbers, continued 

exploitation, and population fragmentation. 

However, Belize, Central America, has long been 

recognized as a stronghold for Antillean manatees 

in the Caribbean (O’Shea & Salisbury, 1991). In 

the 1960s, Charnock-Wilson (1968, 1970) conducted 

interviews and personal observations and 

reported that manatees were abundant in the country. 

From the late 1970s to the early 2000s, aerial 

surveys continued to document that Belize has a 

relatively large number of manatees in comparison 

to neighboring countries (Bengston & Magor, 

1979; O’Shea & Salisbury, 1991; Auil, 1998, 

2004; Morales-Vela et al., 2000). 

The Drowned Cayes, Swallow Caye, and 

Gallows Reef, in particular, are recognized as 

important manatee areas within Belize. Charnock- 

Wilson (1968) described manatees using drowned 

cayes or mangrove islands, in a general sense, 

stating that it was common to spot manatees 

around drowned cayes, their channels, lagoons, 

and surrounding seagrass beds. Subsequent aerial 

surveys have documented high concentrations of 

manatees in the cayes near Belize City, of which 

the Drowned Cayes, Swallow Caye, and Gallows 

Reef are a part (Bengston & Magor, 1979; O’Shea 

& Salisbury, 1991; Auil, 1998, 2004; Morales- 

Vela et al., 2000). Boat surveys that have been 

conducted since 1999 further corroborated 

that this area is consistently used by manatees 

(LaCommare et al., 2003). 

This important manatee area may become 

increasingly threatened by tourism and human 

population growth (Auil, 1998); growth in tourism 

by cruise ships has been particularly dramatic. 

Between 1998 and 2006, the number of tourists 

entering Belize via cruise ships increased from 

14,183 visitors per year to 851,436 visitors per 

year (Belize Tourism Board, 2007). During that 

same period, there was an 18% increase in the 

population of Belize City (Brinkhoff, 2005). Due

36 LaCommare et al. 

to the Drowned Cayes’ proximity to Belize City, 

and because these islands lie between the mainland, 

the reef, and developed cayes, manatees could be 

particularly prone to threats from these sources. As 

tourism increases, a corresponding increase in boat 

traffic as well as land development is expected. 

Boats pass through the Drowned Cayes when traveling 

from Belize City to the northern cayes, outer 

cayes, and the reef, causing a risk of watercraft collisions 

with manatees. Watercraft collisions are the 

leading source of human-caused manatee mortality 

in Belize (Auil & Valentine, 2004). The proximity 

of these islands to the barrier reef may result in 

increased land development that could result in the 

loss of mangrove habitat. In the last five years, new 

resort development and expansion have occurred. 

And finally, development in Belize City and along 

the Belize River is likely to cause increases in runoff, 

which may decrease the productivity, biomass, 

and percent bottom cover of seagrass (Hemminga 

& Duarte, 2000; Duarte, 2002)—a principal food 

source for manatees (Ledder, 1986; Provancha & 

Hall, 1991; Mignucci-Giannoni, 1998; Lefebvre 

et al., 2000; U.S. Fish and Wildlife Service, 2001). 

Because the Drowned Cayes area is an important 

manatee area within the country and because the 

islands are increasingly affected by human activities, 

it is critical to improve our understanding of 

how manatees utilize this area. Evaluating animal 

habitat use and the relative importance of habitat 

types informs habitat management and conservation 

(Garshelis, 2000). The two research objectives 

for this paper are (1) to document manatee distribution 

within the Drowned Cayes, Swallow Caye, 

and Gallows Reef, and (2) to examine habitat use 

patterns in order to identify habitat characteristics 

influencing the probability of sighting a manatee. 


Study Area 

The Drowned Cayes and Swallow Caye are mangrove 

islands along the central coast of Belize, 

10 to 15 km east of Belize City and 5 km west of 

the Belize Barrier Reef (Figure 1). The Drowned 

Cayes are a string of mostly uninhabited islands 

that are 14 km long by 4 km at their widest 

point and are almost entirely comprised of red 

(Rhizophora mangle) ) and black (Avicennia ( ger- 

minans) mangrove stands. There is very little dry 

land, and the islands are interspersed with broad 

channels, narrow inlets, shallow lagoons, and protected 

coves. The entire complex is surrounded by 

seagrass beds; seagrass also grows in varying densities 

on the bottoms of the channels, lagoons, and 

coves. Turtle grass (Thalassia testudinum) is the 

predominant species with shoal (Halodule wrightii) 

and manatee grass (Syringodium filiforme) also 

very common. Water depth is less than 1 m in 

some places and is never greater than 6 m within 

the study area; the tidal range is less than 0.3 m. In 

2002, the northern portion of the Drowned Cayes 

and Swallow Caye were designated as the Swallow 

Caye Wildlife Sanctuary. 

The islands are in a marine environment. In 

open water areas, salinities range from 35 to 40 

ppt (mean salinity is 37 ppt), making the environment 

slightly hypersaline. Within the mangrove 

island complex, salinities have greater fluctuations 

as a result of larger run-off, evaporation, and tidal 

influences. Therefore, within the channels, coves, 

and lagoons of the mangrove islands, salinities 

can range from 30 to 42 ppt. 

Survey Design 

A point sampling survey design was devised for a 

small boat platform to quantify manatee distribution 

and habitat use. Fifty-four permanent points 

were established in all habitat types throughout 

the study area (Figure 2). Habitat types are 

defined in Table 1. These points were randomly 

sampled during January, February, March, June, 

July, and August from 2001 to 2004. Surveys were 

also conducted in June, July, and August 2005. 

Using a mix of experienced observers and volunteers, 

three to 13 observers searched for manatees 

at each point for 30 min. These searches are 

referred to as point scans. As the boat came within 

100 m of each point, observers started scanning 

for manatees in a 360º circle around the boat. The 

boat was then anchored in position using a pole. 

For each scan, the number of manatees and habitat 

characteristics were recorded. The latter consisted 

of habitat category, presence of a resting 

hole, presence and type of seagrass, temperature, 

salinity, and sea state (Table 2). 

Data Analysis 

Manatee Distribution—Manatee distribution was 

mapped within the Drowned Cayes area by calculating 

the probability of sighting a manatee for each 

point. Since most of the scans had no manatees and 

because location sample sizes were unequal, presence 

or absence of manatees was used to calculate 

the probability of sighting a manatee. Points that 

were visited less than five times were excluded 

from this analysis. This map is a snapshot of the 

overall variation in distribution throughout the 

study area. To provide the most comprehensive 

map of distribution, the largest number of points 

possible was included in the analysis. To do this, 

20-min scans were included in the analysis. To 

create parity between the 20- and 30-min scans, 

presence or absence of the 30-min scans was 

determined based on only the first 20 min of the 

sampling duration. This increased the sample size

Distribution and Habitat Use of Antillean Manatees in Belize 37 

Figure 1. Map of Drowned Cayes and surrounding area (Source: British Admiralty Navigation Chart No. 522, Belize City 

and Approaches, 1989) 

from 613 to 795 scans and increased the number of 

points used in the analysis from 39 to 47. 

Habitat Use—Binary logistic regression was used 

to examine whether the probability of sighting a manatee 

varied in relation to several habitat variables— 

habitat category, presence of a resting hole, presence 

and type of seagrass, temperature, salinity, and sea 

state. Due to the large number of zeros (268 zero 

counts of 430 samples) and unequal sample sizes 

across habitat categories, manatee presence/absence 

was used rather than the number of individual manatees 

sighted during each scan to calculate the probability 

of sighting a manatee. Habitat category was 

determined by placing each point into one of six 

categories based on mangrove shoreline features and 

the depth profile of the particular point. These habitat 

categories were qualitatively assigned and are mutually 

exclusive. It is recognized that not all points fit 

neatly into these designations. A complete description 

of each category is given in Table 1. A resting 

hole is a bottom feature that is a distinct, shallow 

depression in the seafloor. Although they are at least 

3 to 4 m wide by 3 to 4 m long, they can be larger and 

are not necessarily regularly shaped. In some cases, 

they appear to be natural features that are maintained 

by manatee use; in other cases, they may have been 

created by manatee use. Seagrass category connotes 

whether seagrass was present at a particular point 

and, if so, what species of seagrass were found there. 

There were six categories: (1) none, (2) Thalassia


Figure 2. Map of manatee sighting probability throughout the Drowned Cayes study area (n = 795) (Source: Defense 

Mapping Agency Chart, Belize City Harbor, 1996)


Table 1. List and description of habitat categories used in the logistic regression analysis; number of points equals the number 

of points in each habitat category type. Description is the definition of the habitat category type. 

Habitat category 

Table 2. Description and assessment of the model relating the presence/absence of manatees to habitat variables for the 

Drowned Cayes study area (n = 491, Nagelkerke R-Square = 0.22); significant variables were habitat category, seagrass 

category, and habitat category*resting hole interaction term. Backward stepwise procedure and log-likelihood function were 

used to determine the most parsimonious model. Hosmer and Lemeshow Goodness of Fit χ 2 = 3.757, p = .878. 

Variables in the model 

testudinum only, (3) Halodule wrightii only, 

(4) T. testudinum/H. /H. / wrightii mix, (5) Syringodium 

filiforme/T. testudinum mix, and (6) a mix of all 

three. Sea state was based on the Beaufort scale. 

Logistic regression accommodates both continuous 

and categorical predictor variables (Trexler 

& Travis, 1993; Floyd, 2001). Maximum likelihood 

method was used to fit the model to the data, 

and a backward stepwise procedure was used to 

determine the most parsimonious model. The likelihood 

ratio test and the Wald statistic were used 

to determine the significance of the parameters in 

explaining the variation in the dependent variable. 

To determine if the model was an adequate fit to the 

Change in -2 log 

likelihood df 

data and to rule out the undue influence of outliers, 

the Hosmer-Lemeshow test was used and observed 

and expected sighting probabilities were compared 

(Trexler & Travis, 1993). Plots of Cook’s distances 

and Studentized residuals vs predicted probabilities 

were used to examine the influence of outliers and 

bias in the data. All statistical analyses were performed 

using SPSS, Version 13.0 (SPSS, 2004). 

Results 

Significance 

of change 

Dependent variable 

Manatee presence/absence 

Independent variables 

Sea state (Beaufort scale) 0.55 3 NS 

Surface salinity (ppt) 1.76 1 NS 

Water temperature (ºC) 0.11 1 NS 

Habitat category 14.09 5 0.015* 

Resting hole 1.27 1 NS 

Seagrass category 23.21 5 0.0001* 

Habitat category*resting hole 10.46 3 0.015* 

Habitat category*seagrass category 10.84 8 NS 

NS = Not significant, * = significant 

Number 

of points Description 

Lagoon 5 A large open water area totally encompassed within the mangrove islands; the area 

has a uniform and shallow depth (< 3 m). 

Channel 12 An area of deeper water (3 to 6 m) that cuts between the mangrove islands; 

generally, there is mangrove shoreline on two sides. 

Channel edge 8 An area of deeper water that cuts through areas of shallower water; the point 

encompasses two habitat types: (1) channel and (2) seagrass bed. Depth ranges from 

1 to 5 m. The point may be adjacent to mangrove shoreline on one side or may be in 

open water. 

Seagrass bed 11 An area of shallow water, < 3 m, outside of the mangrove islands with a seagrass 

bottom. 

Cove 16 An area of very protected water that is at the end of a channel or off to the side of a 

channel; it is nearly enclosed by mangroves and has shoreline on at least three sides. 

Depth ranges from 0.6 to 4 m. 

Reef 2 This is an open water area on the back reef portion of the Belize Barrier Reef; there 

are no mangrove islands in the vicinity, and depth ranges from 1.5 to 4 m. 

Distribution Within the Drowned Cayes 

Manatees were sighted throughout the study area. 

The probability of sighting a manatee across all


points was 0.31/20-min scan (n = 795). Sighting 

probabilities for each location ranged from 0 to 

0.86/scan. Swallow Caye had the highest probability 

of sightings among its points, and the 

Gallows Reef points had the lowest probability of 

sightings. There does not appear to be a distinct 

spatial pattern of variability in sighting probability 

among the Drowned Cayes points (Figure 2). 

Habitat Use 

The probability of sighting a manatee was lowest 

at the reef (0.17/scan) and highest on seagrass 

flats (0.58/scan) (Figure 3). Habitat category, 

seagrass category, and habitat category interaction 

with resting hole were the most important 

variables explaining the probability of sighting 

a manatee (Table 2). The change in log likelihood 

for each of these three terms was 14.09 with 

p = 0.015, 23.21 with p = 0.0001, and 10.46 with 

p = 0.015, respectively. Within habitat categories, 

seagrass flats and coves with resting holes both 

explained a significant portion of the variation in 

manatee presence (Wald = 4.14 with p = 0.042 

and 4.79 with p = 0.029, respectively) (Figures 

3A & B). There was only one scan point categorized 

as a channel with a resting hole. The low 

sample size of this category type may explain 

why channels with resting holes had an opposite 

trend to other habitat types. Scan points with 

just T. testudinum and S. filiforme present or with 

just H. wrightii present had a significantly lower 

probability of sighting a manatee than other seagrass 

categories (Wald = 6.50 with p = 0.011 and 

6.4 with p = 0.011, respectively) (Figure 4). The 

Hosmer-Lemeshow chi-square goodness of fit 

was 1.486 with a p-value of 0.983, indicating that 

the overall model was a good fit to the data, and 

the Nagelkerke R-Square was 0.221 (Table 2). 

The expected sighting probability for each habitat 

and seagrass category was very similar to the 

observed sighting probability further indicating 

that the model was a good fit to the data (Figures 

3A & 4). Residual plots of change in deviance vs 

predicted probabilities indicated that samples with 

a low predicted probability of a presence were 

poorly fit by the model. In other words, manatees 

tended to be observed more often than predicted 

by the model at places where the probability of 

sighting a manatee was low. 

Discussion 

The Drowned Cayes area clearly constitutes a 

manatee habitat area. Manatees were sighted at 

least once at nearly all of the points that were 

surveyed (47 out of 54 points). There were 

some points that had particularly high sighting 

probabilities (≥ 0.5/20-min scan), and these points 

A. 

B. 

Figure 3. (A) Observed and predicted probability of sighting 

a manatee per 20-min scan by habitat; (B) Observed 

probability of sighting a manatee per 20-min scan by habitat 

with and without the presence of a resting hole; No = 

no resting hole, Yes = resting hole present (2001 to 2005, 

n = 491, ± 1 SE). 

Figure 4. Observed and predicted probability of sighting 

a manatee per 20-min scan by seagrass category (2001 to 

2005, n = 491) 

might be considered “hot spots” within the overall 

mangrove island complex. These points should 

be given particular consideration in management 

plans in terms of tourist activities, development, 

and watercraft traffic.


Based on the logistic regression procedure, 

habitat category was one of the three most important 

variables explaining variation in sighting 

probability across the Drowned Cayes. Variability 

in sighting conditions between habitat types did 

not result in differences in detection probability. 

It is unlikely that there were detection biases as a 

result of habitat types (LaCommare et al., unpub. 

data). Seagrass beds had the highest probability 

of sighting a manatee, and reefs had the lowest. 

Seagrass flats may be a particularly important 

habitat category, indicating the importance of the 

Drowned Cayes as a feeding area. 

However, manatees did utilize all habitat categories. 

Manatees use the entire area and many of 

its components to meet a variety, but probably not 

all, of their physiological and behavioral requirements. 

During the course of this study, manatees 

were observed feeding, socializing, resting, 

nursing calves, and moving from place to place 

(Self-Sullivan & LaCommare, unpub. data). Even 

resources that are used at a low frequency may be 

important components of the manatees’ overall 

habitat. For instance, the reef may be a seasonally 

important travel corridor and stopover site for male 

manatees during the mating season (Self-Sullivan 

et al., 2004). Behavioral and physiological studies 

indicate that manatees probably need regular 

access to freshwater sources to survive (Reynolds 

& Odell, 1991; Ortiz et al., 1998, 1999; Reynolds, 

1999; Deutsch et al., 2000, 2003). Only one source 

of hyposaline water (refractometer measurements 

ranged from 10 to 17 ppt) has been conclusively 

identified (Self-Sullivan & LaCommare, unpub. 

data) within the Drowned Cayes, which may be 

used for osmoregulation. Manatees may also be 

traveling from the Drowned Cayes to freshwater 

sources several kilometers away as they do in 

Florida (Deutsch et al., 2003). Management plans 

should recognize the importance of protecting a 

variety of habitat types. 

Seagrass is clearly an important component of 

the Drowned Cayes habitat. Seagrass category 

was an important variable explaining the probability 

of sighting a manatee. It contributed the 

largest improvement in model fit, and the parameter 

was highly significant. Specifically, sites that 

had a mix of T. testudinum and S. filiforme or sites 

with just H. wrightii present had a significantly 

lower probability of sighting a manatee than the 

other seagrass categories—no seagrass, a mix of 

all three species, just T. testudinum, , or a mix of T. 

testudinum and H. wrightii. 

How this relates to manatee foraging and feeding 

is not clear. The three most common species 

in the study area—T. testudinum, H. wrightii, 

and S. filiforme—are present in the manatee 

diet in both Florida and Puerto Rico (Packard, 

1984; Ledder, 1986; Provancha & Hall, 1991; 

Mignucci-Giannoni, 1998; Lefebvre et al., 2000; 

USFWS, 2001). The relative importance of these 

species in their diet is not fully understood in 

these places. In Indian River Lagoon, Florida, and 

in Puerto Rico, “manatees fed most often on the 

most frequently encountered seagrass” (Lefebvre 

et al., 2000, p. 295). In Indian River Lagoon, this 

was H. wrightii, and in Puerto Rico, this was T. 

testudinum (Lefebvre et al., 2000). However, in 

both locations, it is possible that manatees return 

to specific H. wrightii beds to feed on them 

(Lefebvre et al., 2000). Both T. testudinum and 

H. wrightii appear to be important food resources 

in the Drowned Cayes based on observations of 

feeding manatees, and certain areas appear to be 

more heavily foraged than others (LaCommare 

& Self-Sullivan, unpub. data), perhaps indicating 

foraging preferences. 

While certain types of seagrass sites, as well as 

species, may be particularly important to manatees 

in the Drowned Cayes, fully understanding 

manatee foraging will involve examining the 

extent of feeding behavior in particular places, 

specific physical and biological characteristics of 

important seagrass areas, and the juxtaposition of 

these areas to other important resources. 

Habitat category interacting with resting hole 

was also an important variable explaining variation 

in sighting probability. Cove habitats with 

resting holes were the most significant subcategory. 

Cove habitats are extremely sheltered places 

found at the end of narrow channels or off to the 

side of larger channels. In the Drowned Cayes, 

resting holes are a feature of the bottom topography 

and are associated with resting manatees 

(Self-Sullivan & LaCommare, unpub. data). In 

Florida, manatees often use secluded places for 

feeding, resting, mating, and calving (USFWS, 

2001). This appears to be true in the Drowned 

Cayes as well. The presence of a resting hole was 

a key feature distinguishing which particular cove 

area was utilized (0.25 to 0.49/scan increase in 

sighting probability). It is unclear at this point if 

the resting hole was the reason manatees used the 

site or if the resting hole depression is a result of 

repeated manatee use. 

While the Nagelkerke R-Square for the regression 

model was 0.22, indicating that only 22% of 

the variability in sighting probability was explained 

by the logistic regression model, the model was a 

good fit to the data, and the variability explained 

was the correct variability. The ability to explain 

variation in sighting probability will provide a 

better understanding of habitat use. Building a 

habitat model that includes variables that describe 

the spatial configuration and characteristics of habitat 

is an important follow-up to this analysis and


may even provide insight into habitat selection and 

preferences. Habitat use is dependent on behavior, 

and suitable habitat must include a variety of patch 

types or components so that animals can meet their 

essential behavioral and physiological requirements 

(Mysterud & Ims, 1998). In addition, habitat 

use, selection, and preferences are affected by habitat 

heterogeneity (Johnson, 1980; Li & Reynolds, 

1994; Kie et al., 2002). Heterogeneity can be 

defined in terms of number, proportion, spatial 

arrangement, shape, and contrast between patches 

and patch types (Kie et al., 2002). Analyses examining 

manatee habitat components in these terms 

and with respect to behavior could be important in 

understanding manatee habitat use patterns. 


We thank Earthwatch Institute for substantial 

financial support and Earthwatch Volunteers for 

logistical support and data collection. We thank 

Conservation Action Fund, Henry Greenwalt, 

Project Aware, Virtual Explorers, and Jack Bert 

for additional financial support. Spanish Bay 

Resort provided logistical and in kind support 

from 2001 to 2004. Hugh Parkey Foundation for 

Marine Awareness and Education provided logistical 

and in kind support in 2005. We are grateful 

to the numerous interns and field assistants who 

were vital to data collection and field logistics. We 

are especially thankful for the help and guidance 

of our colleague, friend, and field assistant Gilroy 

Robinson. In addition, we thank the two anonymous 

reviewers for their insightful comments that 

led to the improvement of this manuscript. 


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172 

NOTES 

Caribbean Journal of Science, Vol. 41, No. 1, 172-177, 2005 

Copyright 2005 College of Arts and Sciences 

University of Puerto Rico, Mayagüez 

Bottlenose Dolphins (Tursiops 

truncatus) in the Drowned Cayes, 

Belize: Group Size, Site Fidelity 

and Abundance 

KECIA A. KERR 1 ,R.H.DEFRAN 2 , AND GRE- 

GORY S. CAMPBELL Cetacean Behavior Laboratory 

- Department of Psychology, San Diego 

State University, San Diego, CA 92182-4611, 

USA 

ABSTRACT.—Group size, site fidelity and abundance 

of bottlenose dolphins, Tursiops truncatus, 

ms. submitted June 3, 2004; accepted December 28, 

2004 

1 

Current address: Whale Research Laboratory, Department 

of Geography, University of Victoria, PO 

Box 3050 STN CSC, Victoria, BC, V8W 3P5 Canada 

2 

Corresponding author: rdefran@sunstroke. 

sdsu.edu

were assessed during 392 photo-identification surveys 

conducted during 1997-1999 in the Drowned 

Cayes region, near Belize City, Belize, Central 

America. During this study 2155 dolphins were 

sighted across 736 groups. Mean group size was 2.9 

(SD = 2.32) which is one of the smallest reported for 

bottlenose dolphins. One hundred and fifteen individual 

dolphin were photographically identified, 

with sighting frequencies ranging from one to fifty 

(X ¯ = 8.1, SD = 9.05). Thirty percent of identified dolphins 

were judged to be residents, while 23% were 

photographed only once. Chao’s M th model for 

closed populations was used to derive an abundance 

estimate of 122 dolphins (95% CI = 114 -140). This 

low abundance estimate and a leveling trend in the 

rate of newly identified individuals, indicates that 

the Drowned Cayes dolphin population is both 

small and finite. Group size, abundance, and site 

fidelity comparisons were made with a 4-yr photoidentification 

study conducted at nearby Turneffe 

Atoll. Both the Drowned Cayes and Turneffe Atoll 

studies had similarly small group sizes, low and 

variable levels of site fidelity and low abundance 

estimates, but there was no overlap between individual 

sightings in the two areas. The observed behavioral 

patterns and similarities between the two 

studies raise concerns that increasing pressures on 

Belize’s marine resources may pose a threat to its 

bottlenose dolphins. 

KEYWORDS.—Residency patterns, population dynamics, 

cetaceans, Belize, Caribbean 

A recent 4-yr study at Turneffe Atoll in 

Belize, Central America (Campbell et al. 

2002), was one of the first to document the 

population dynamics of bottlenose dolphins 

(Tursiops truncatus) in a tropical offshore 

atoll containing coral reefs, sea grass 

beds and mangroves, and is one of the few 

published studies on this cetacean species 

in the Caribbean Sea (see also Grigg and 

Markowitz 1997; Rossbach and Herzing 

1999; Rogers et al. 2004). Turneffe bottlenose 

dolphins occurred in small groups 

that were larger when they contained 

calves, and this population had a high proportion 

of individuals sighted only once. 

Further, abundance estimates were low, 

and only a small proportion of these dolphins 

showed evidence of site fidelity 

(Campbell et al. 2002). The habitat characteristics 

of the Drowned Cayes, where the 

current study was conducted, are similar to 

those of Turneffe. Thus, the objectives of 

NOTES 173 

the current study were to examine the generality 

of the Turneffe findings and interpretations, 

identify possible overlap between 

these two dolphin populations, and 

extend the management and conservation 

implications of both studies. 

The Drowned Cayes are located in the 

western Caribbean, south of the Yucatan 

Peninsula, 6 km east of Belize City and 16 

km west of Turneffe Atoll (Fig. 1). The 

study area consisted of a 150 km 2 chain of 

mangrove islands extending from 17°20’N- 

17°34’N, and 88°03’W-88°07’W. Like 

Turneffe Atoll, the Drowned Cayes area is 

characterized by a predominating substrate 

of sandy sea grass beds, but also includes a 

portion of the Belize Barrier Reef. Surface 

water temperature ranged from 25°-33°C 

(X ¯ = 29.2, SD = 1.62), and water depth, measured 

during 216 sightings, ranged from 0.9 

mto11.8m(X ¯ = 4.3 m). All aspects of the 

photo-identification methodology used in 

this study, including: survey methodology, 

criteria for groups and calves, image processing 

and analysis of photographic data 

(i.e., rate of discovery, sighting frequency, 

abundance), were the same as those described 

in Campbell et al. (2002). Briefly 

summarized, boat based surveys lasting 

approximately 4 h were carried out once or 

twice daily, and all portions of the study 

area were covered at least once a month. 

When dolphins were sighted, the survey 

vessel stopped while environmental data 

were recorded and group size was determined. 

Next, an attempt was made to obtain 

high quality dorsal fin photographs for 

each group member. Once photographic 

data were collected, the survey continued 

along a predetermined route to search for 

and photograph additional dolphins. 

During 1246 h expended over a 3-yr period 

(February-December in 1997 and 1998, 

and April-Dec in 1999), 392 surveys were 

completed, and 277 h were spent in direct 

observation of 2155 dolphins sighted across 

736 groups. Group size ranged from one to 

20 dolphins (X ¯ = 2.9, SD = 2.32), but was 

higher for groups with calves (n = 160, X ¯ = 

4.6 [includes calves], SD = 2.68) than without 

calves (n = 576, X ¯ = 2.5, SD = 

1.99)(Mann-Whitney U = 19540.0, Z = 

-11.433, p = < 0.001). Almost a third (31%)


FIG. 1. Drowned Cayes study area (within dashed outline). Insets show the location of the study area from a 

broad regional (top) and western Caribbean (bottom) perspective. 

of all sightings were solitary dolphins and 

99% of all groups contained 10 or fewer 

dolphins. Group sizes for Drowned Cayes 

(X ¯ = 2.9) and Turneffe dolphins (X ¯ = 3.8, SD 

= 3.55, Campbell et al. 2002) are among the 

smallest reported for any population of 

bottlenose dolphins (Connor et al. 2000). 

Group size in bottlenose dolphins, as in 

many other species, is a tradeoff between 

optimizing foraging efficiency and minimizing 

predation risk (Wells and Scott 

1999; Campbell et al. 2002). While there 

have been no studies of prey characteristics 

for Drowned Cayes or Turneffe dolphins to 

date, no observations or images indicated 

evidence of shark bites, suggesting that 

predatory threats from sharks are minimal. 

Low apparent predation at the Drowned 

Cayes suggests, as it did at Turneffe, that 

energy intake is a primary selective pressure 

on group size; and, the small group 

sizes in these areas are optimized for food 

resources that are likely low in density. 

NOTES 

Similarly, in both the Drowned Cayes and 

Turneffe, larger calf-groups may be an adaptation 

that facilitates allomaternal behavior, 

thereby increasing the foraging efficiency 

of nursing mothers who are 

constrained by maternal responsibilities 

(see review in Campbell et al. 2002). 

Across the study period, 115 dolphins 

were photographically identified. The 

slope of the Drowned Cayes discovery 

curve for newly photographed dolphins 

showed a steep rise until the 90 th survey 

when 76 dolphins (66%) had been identified 

(compare with Fig. 2, Campbell et al. 

2002). Few new dolphins were photographed 

until surveys 190-230 (Aug 1999) 

when an additional 23 dolphins (18%) were 

identified. No new dolphins were photographed 

during the remaining 162 surveys. 

Sighting frequencies for identified dolphins 

ranged from 1-50 (X ¯ = 8.1, SD = 9.02), with 

23% (n = 27) of these dolphins identified 

one time, 50% (n = 57) sighted between two

and nine times and 27% (n = 31) sighted 10 

or more times. Evidence for site fidelity 

was evaluated by examining sighting frequencies 

within and between the three 

study years. Dolphins sighted two or more 

times in each of the three study years, or 

four or more times in two successive years, 

were labeled as residents, and comprised 

30% of the identified population. The abundance 

estimate derived by Chao’s closed 

model M th was 122 (95% CI = 114-140) 

(Chao et al. 1992) and was quite similar to 

the number of identified dolphins (n = 115). 

Taken together, the discovery rate for 

new individuals, the high study effort 

(number of surveys) extending over a 3-yr 

period, the high proportion of individuals 

showing low sighting frequencies (vis-à-vis 

the high number of surveys), the small 

number of individuals showing evidence 

for site fidelity (“residents”), and the relatively 

low abundance estimate, suggests 

that, as at Turneffe, a small and finite population 

of dolphins uses this study area. 

These same data indicate that the Drowned 

Cayes area can only support a small number 

of dolphins, probably due to low prey 

item densities (group size interpretation 

suggested above). Some dolphins were 

seen throughout and across years, however, 

indicating that a degree of fidelity to 

the area does exist. 

Photographs of the 115 Drowned Cayes 

dolphins were compared to those of 81 individuals 

photographed during 549 surveys 

at Turneffe Atoll from 1992-1996 

(Campbell et al. 2002). Despite the close 

geographic proximity of the Drowned 

Cayes and Turneffe, the high survey effort 

in both studies, and the presence of a large 

number of individuals in each population 

not considered “residents,” there was no 

overlap documented between these populations. 

While the depth of the channel 

separating Turneffe Atoll from the Belize 

Barrier Reef and the Drowned Cayes (range 

= 274-305 m) may act as a physical barrier 

to regulate movements of dolphins between 

the study areas, the distance between 

Turneffe and the Drowned Cayes 

could be easily traveled by this species 

(Stoddart 1962; Tanaka 1987; Wood 1998; 

Defran et al. 1999). A tentative hypothesis, 


consistent with the existing photo-identification 

data, is that bottlenose dolphins in 

Belize may have overlapping ranges along 

the mainland coastline; however, exploitation 

of the offshore islands, such as the 

Drowned Cayes and Turneffe Atoll, is selective 

among subsets of this population. 

Similar selective partitioning among areas 

of their range were shown for bottlenose 

dolphins (Maze and Würsig 1999) as well 

as humpback (Megaptera novaeangilae) and 

sperm (Physeter macrocephalus) whales 

(Clapham 2000; Whitehead and Weilgart 

2000). To date, no mainland coastal photoidentification 

surveys have been carried out 

in Belize. Such surveys are needed, however, 

in order to clarify the home ranges of 

Drowned Cayes and Turneffee Atoll dolphins, 

as well as to evaluate the selective partitioning 

hypothesis we have proposed. 

Belize is rich in natural resources that 

could be vulnerable to ecologically unsustainable 

growth in tourism, fishing, and development. 

The accessibility of the 

Drowned Cayes to the coastal mainland of 

Belize, including Belize City and the Belize 

River, places an even higher pressure on 

levels of resource extraction, pollution, and 

boat traffic in this region than in other offshore 

locations such as Turneffe Atoll. Although 

fishing pressure in the Drowned 

Cayes, and the rest of Belize, may be considered 

low compared to highly populated 

areas in the Caribbean, the demands on 

fisheries resources are increasing and the 

effects of overfishing are already evident as 

changes in fish community structure (Sedberry 

et al. 1999). Some suggest that reefs in 

the Caribbean have been overfished for 

centuries, and the resulting changes in 

community structure have placed these 

ecosystems in a precarious state that is now 

collapsing (Jackson 1997; Jackson et al. 

2001). While fishing in the study area is 

mainly artisinal, even this type of fishing 

may be unsustainable (Coblentz 1997; Sedberry 

et al. 1999). Shifts in the ecological 

dominance from coral to fleshy algae have 

been found at some reef locations in Belize 

(Aronson and Precht 1997; McClanahan 

and Muthiga 1998). Since the first major 

bleaching event in the history of Belize’s 

coral reefs occurred in 1995, an even more


severe event occurred in 1998 (Aronson et 

al. 2000). Threats, such as overfishing, pollution, 

and the results of climatic change, 

have been shown to detrimentally affect 

marine mammals in a variety of ways (Harvell 

et al. 1999; Allen and Read 2000; Fair 

and Becker 2000; Wilson et al. 2000; Bossart 

et al. 2003). In the aggregate, these factors 

indicate that bottlenose dolphins in Belize 

could play a valuable role as a sentry species 

in this area. For example, shifts in 

bottlenose dolphin occurrence and abundance 

might indicate a further decline in 

prey (and other fish species) abundance. 

Similarly, increases in skin lesions (observed 

on at least two dolphins in the 

Drowned Cayes population, personal observations), 

may provide an early signal of 

compromised immunity to disease (Wilson 

et al. 2000; Bossart et al. 2003). 

Acknowledgments.—We thank the following 

individuals and institutions for their 

contributions to this research: B. Winning, 

Oceanic Society; Oceanic Society volunteers, 

the Belize Fisheries Department, the 

Belize Forestry Department, Coastal Zone 

Management Authority Institute and S. 

Turton in Belize; E. Requeña and staff at 

Spanish Bay Resort, K. Schafer, K. LaCommare, 

A. Sanders, B. Bilgre, S. Barclay, H. 

Petersen, and C. Sullivan for field support; 

B. Bilgre, L. Hinderstein and A. Sanders for 

contributions to the photographic dataset; 

K. Dudzik, B. Hancock, J. Schivone, L. 

Sousa, and A. Toperoff, as well as numerous 

interns, at the Cetacean Behavior Laboratory, 

San Diego State University, for assistance 

with photographic analysis. We 

appreciate the contributions of E. Bardin, 

A. Bradford, B. Hancock, D. Herzing, A. 

Mignucci-Giannoni and one anonymous 

reviewer who graciously offered helpful 

editorial remarks on earlier drafts of this 

manuscript. This research was conducted 

under a marine scientific research permit 

issued to Oceanic Society from the Ministry 

of Natural Resources, the Environment and 

Industry, Government of Belize. 


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Coral Reefs (1997) 16, Suppl.: S23—S32 

Reefs since Columbus 

J. B. C. Jackson 

Center for Tropical Paleoecology and Archeology, Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama 

Accepted: 17 January 1997 

Abstract. History shows that Caribbean coastal ecosystems 

were severely degraded long before ecologists began 

to study them. Large vertebrates such as the green turtle, 

hawksbill turtle, manatee and extinct Caribbean monk 

seal were decimated by about 1800 in the central and 

northern Caribbean, and by 1990 elsewhere. Subsistence 

over-fishing subsequently decimated reef fish populations. 

Local fisheries accounted for a small fraction of the fish 

consumed on Caribbean islands by about the mid nineteenth 

century when human populations were less than 

one fifth their numbers today. Herbivores and predators 

were reduced to very small fishes and sea urchins by the 

1950s when intensive scientific investigations began. These 

small consumers, most notably Diadema antillarum, were 

apparently always very abundant; contrary to speculation 

that their abundance had increased many-fold due to 

overfishing. Studying grazing and predation on reefs 

today is like trying to understand the ecology of the 

Serengeti by studying the termites and the locusts while 

ignoring the elephants and the wildebeeste. Green turtles, 

hawksbill turtles and manatees were almost certainly 

comparably important keystone species on reefs and 

seagrass beds. Small fishes and invertebrates feed very 

differently from turtles and manatees and could and can 

not compensate for their loss, despite their great abundance 

long before overfishing began. Loss of megavertebrates 

dramatically reduced and qualitatively changed 

grazing and excavation of seagrasses, predation on 

sponges, loss of production to adjacent ecosystems, and 

the structure of food chains. Megavertebrates are critical 

for reef conservation and, unlike land, there are no coral 

reef livestock to take their place. 

Introduction 

The status and trends of the world’s coral reefs are highly 

controversial and, until very recently, have attracted far 

less attention than has been lavished on the decline of 

tropical forests. This is partly a function of our greater 

ignorance about coral reefs and their briefer period of 

study. But it is also true that coral reef ecologists have 

been so devoted to dissecting small-scale processes that 

they have not seen the reefs for the corals. 

Ecology is a young science, with little reliable 

descriptive information from before the 1920s (Elton 

1927; Hutchinson 1978) and virtually no time series 

population data extending of back for more than a century. 

The situation is even worse for marine communities 

like coral reefs because of the difficulty of making observations 

underwater. Thus reef ecologists have been 

forced to try to explain patterns of distribution and 

abundance exclusively in terms of the events of the 

past few years using ‘‘real time’’ observations and 

experiments. Their success is manifest in our rapidly 

growing understanding of how environmental variation 

and biological interactions can shape reef communities 

(Connell 1978; Hughes 1989; Knowlton et al. 1990), although 

the importance of events rare on the scale of 

human lifetimes is only beginning to be understood 

(Woodley et al. 1981; Jackson 1991; Knowlton 1992; 

Hughes 1994). 

In the process of these endeavors, however, reef ecologists 

have turned their backs on history and assumed 

that what they were studying was ‘‘normal,’’ despite the 

lack of rigorous baseline data for the condition of coral 

reefs preceding the industrial revolution and the onset of 

worldwide, exponential human population growth. As 

a result, many reef ecologists have concluded that coral 

reefs are healthy in the face of overwhelmingly increasing 

evidence to the contrary. Indeed, the idea for this study 

arose from my feeling like Cassandra in the face of such 

denial during the 1993 Miami Colloquium on Global 

Aspects of Coral Reefs: Health, Hazards and History. Most 

felt at the beginning of the colloquium that the condition 

of coral reefs was on the whole rather good, despite 

Wilkinson’s (1992) plenary paper at the 7th International 

Coral Reef Symposium about widespread devastation 

worldwide. However, by the end of the Colloquium, there 

was a beginning acceptance that the situation was perhaps 

bad in the Caribbean, but only recently, and probably not 

in the pacific.

S24 

The problem is that everyone, scientists included, believes 

that the way things were when they first saw them is 

natural. However, modern reef ecology only began in the 

Caribbean, for example, in the late 1950s (Goreau 1959; 

Randall et al. 1961; Randall 1965) when, enormous changes 

in coral reef ecosystems had already occurred. The same 

problem now extends on an even greater scale to the 

SCUBA diving public, with a whole new generation of 

sport divers who have never seen a ‘‘healthy’’reef, even by 

the standards of the 1960s. Thus there is no public perception 

of the magnitude of our loss. 

Another insidious consequence of this ‘‘shifting baseline 

syndrome’’ (Pauly 1995; Sheppard 1995) is a growing ecomanagement 

culture that accepts the status quo,andfiddles 

with it under the mantle of experimental design and statistical 

rigor, without any clear frame of reference of what it is 

they are trying to manage or conserve. These are the coral 

reef equivalents of European ‘‘hedgerow ecologists’’ arguing 

about the maintenance of diversity in the remnant 

tangle between fields where once there was only forest. 

Let me say from the start that I am not going to make 

some romantic appeal to set back the clock, nor propose 

draconian scenarios that ignore the realities of inexorable 

human population growth and underdevelopment. Instead, 

my goal is to set the stark realities we face in a deeper 

historical perspective than the last few decades in order to 

(1) silence absurd notions of multiuse sustainability and (2) 

help to define better the limited alternatives available. I will 

limit my discussion to the Caribbean, and principally to 

Jamaica, because I know the Caribbean best and Jamaica is 

arguably the worst case today in that region. Jamaica also 

offers the best historical record, which extends back nearly 

350 years, and provides startlingly good but unexploited 

information for ecological assessment. 

I will first work backward from the present to re-examine 

aspects of the classic story relating overfishing, the mass 

mortality of the long-spined sea urchin Diadema antillarum, 

and the collapse of Caribbean coral reefs in Jamaica and 

elsewhere (Lessios et al. 1984; Hay 1984; Hughes 1994). This 

is not to deny the important consequences of overfishing, 

but to show that we have been at least partly wrong about 

the historical role of the sea urchin. I will then work 

forward from 1492 to examine the extraordinarily rapid 

depletion of large consumers on coral reefs and their environs, 

which were once the equivalents of the wildebeeste 

and elephants of the Serengeti plains (Sinclair and Arcese 

1995). For this purpose, I will emphasize the Jamaican 

basedfisheryofthegreenturtleChelonia mydas because the 

data are the best; but the same sort of story applies to 

sharks, rays, groupers, manatees and the extinct Caribbean 

monk seal. I will then depart from the general theme of 

overfishing to briefly consider inputs from the land. These 

have almost certainly been of comparable importance to 

overfishing but the data are less complete. Finally, I will 

return to Jamaica to examine the fishing history there since 

Columbus, which clearly shows that coral reef ecosystems 

had begun to fall apart in the eighteenth century. 

Diadema, damselfish and overfishing 

The conventional story (Hay 1984; Lessios 1988; Hughes 

1994) is that intense overfishing allowed Diadema 

to increase because of reduced predation by fishes, and 

competitive release for algal food that was no longer 

consumed by larger herbivores. This increase in Diadema 

compensated for the loss of herbivorous fishes and kept 

down the growth of seaweeds on reefs. Then when the 

Diadema suddenly died, there were no other consumers 

capable of cropping the seaweeds which soon overgrew 

and killed most of the reef corals at depths down to about 

50 m. 

What are the facts and what is the inference in this 

story? The facts are that (1) overfishing was extreme by 

any standard, (2) Diadema was extremely abundant before 

the mass mortality in 1983, (3) mass mortality of Diadema 

allowed a dramatic increase in seaweeds which overgrew 

and smothered corals. The inference is that (1) decrease in 

large fish allowed a large increase in Diadema, (2) increase 

in people caused the decrease in fish in a roughly proportional 

fashion, and (3) the effects of people were relatively 

recent. Regarding the latter point, for example, Hughes’ 

(1994) graph of human population increase starts in 1850 

and is introduced within a section titled ‘‘Overfishing: 

1960s to Present’’. 

Let us examine some problems with this inference 

before reviewing the historical data. Hay’s (1984) pioneering 

regional study of Diadema versus fish grazing confounds 

‘‘overfished’’ and ‘‘less fished’’ with geography. Hay 

was very careful to avoid terms like ‘‘pristine’’ and ‘‘unfished’’, 

unlike many who have referred to his work subsequently. 

However, all of his ‘‘overfished’’ reefs are on 

islands in the central Caribbean, and all but one of his 

‘‘less fished’’ reefs are on the mainland. Moreover, Levitan’s 

(1992) ingenious study of Diadema nutrition over the 

last century shows an even greater geographic effect. Levitan 

(1991) showed experimentally that the ratio of the size 

of the feeding apparatus to the size of the animal test 

increases in inverse proportion to the food supply. He 

then examined changes in the ratio through time using 

museum specimens, and found a significant but surprisingly 

small increase over the past century when Diadema 

populations were inferred to have exploded due to overfishing. 

In contrast, geographic variation accounted for 

much more (23%) of the total variation observed than 

that due to time. Ordination of coral abundance data 

from reefs around the Caribbean compiled by Liddell and 

Ohlhorst (1988) also shows strong island-mainland differences 

in overall reef community structure (Jackson et al. 

1996). 

So is it possible that Diadema were abundant in the 

Caribbean before Columbus arrived? It turns out that 

Diadema has long attracted commentary because of its 

great abundance and reputation of being dangerous 

(Table 1). Moreover, all of the authors cited except Young 

were professional or amateur naturalists, with extensive 

experience dredging or (in the case of Beebe 1928) diving 

in tropical waters. All were well known for the reliability 

and accuracy of their observations and were not the type 

to mistake an occasional aggregation or hearsay for genuinely 

great abundance. These sources make it clear that 

Diadema was indeed very abundant in the seventeenth 

century when human populations were very small, and 

therefore long before overfishing could have caused their 

increase.

Table 1. Caribbean Diadema lore 

Source Location Quoted text 

Beebe 1928 Haiti Under every bit of coral 2 in great abundance 

Clark 1919 Jamaica and Dry 

Tortugas 

Nutting 1919 Barbados Antigua 

and Bahamas 

On and about the coral reefs, the dreaded poisonous ‘‘black 

sea egg’’ (Centrechinus antillarum) is common and on certain 

areas it is so numerous that a person can scarcely move 

about without touching one. 

No one goes bathing or into the water for any purpose in 

this region without being warned against the danger of being 

wounded by the cruel black spines of this ubiquitous 

sea-urchin. It is found almost everywhere in shallow water, 

both on sandy and rocky bottom. 

The all too familiar black sea-egg Diadema antillarum is 

abundant here, as it is everywhere that I have collected in the 

West Indies (therefore includes his 1895 expedition to the 

Bahamas, not seen) 

Henderson 1914 Cuba We were then upon the inner edge of the main reef upon 

which any further progress would have been difficult on 

account of the rapidly increasing numbers of the long 

black-spined sea urchins, the diademas2 

2the usual presence of the net [dredging] of the diadema 

sea-urchin2 

During the hours of bright sunshine the diademas seek cover 

under the rocks2 In the late afternoon2they issue forth 

en masse in search of food and probably continue their slow 

wanderings throughout the night. In localities where hiding 

places are few, such as upon sandy patches in or near a reef, 

the diademas are always more or less in evidence. 

Field 1891 Jamaica The most strikingly conspicuous of all the creatures about 

the coral reefs. As one approaches the cay, far down in the 

water are seen numerous irregularly shaped black patches of 

varying extent. 

2around and under its branches (elkhorn coral) are 

crowded together great numbers of this large black urchin. 

2what formidable defense against attack they present 

when crowded so closely together. 

Aggasiz 1883 Dry Tortugas 2on somewhat deeper regions (of the reef) we find pockets 

filled with large Diadematidae. 

Young 1847 

(writing of his 

observations 

in 1839) 

Sloane 1725 

(writing of his 

observations 

in 1688) 

Nicaragua and 

Honduras 

There is also strong paleontological evidence that Diadema 

were abundant on Jamaican reefs long before any 

humans arrived there (Gordon and Donovan 1992). Diadematoid 

plates and spines are the most abundant 

echinoid remains in the 125 000 year old Falmouth 

Formation, constituting 90% of all identified echinoid 

fragments. These are almost, certainly of Diadema antillarum 

because the only other Caribbean Pleistocene diadematoid 

is Astropyga magnifica which occurs today in 

S25 

2they were both badly cut by the coral and sea eggs in 

diving for the things that had been upset. 

Numbers of sea eggs were seen in all directions, and we well 

knew the danger of getting amongst them, as they have long 

and sharp pointed spines, which inflict deep and dangerous 

wounds on those who chance to tread on them. 

2the handsome sea-eggs inviting but to betray2 

Jamaica The great, long prickled Sea Egg2set about on every hand 

with prickles, the largest being three or four inches long, with 

membrane round their setting on to the shell2purple deep 

coloured2 

The prickles of this Sea Echinus are very rough and considered 

poisonous. 

I have found them in great numbers on the reef by Gun-Key, 

or, Cayos off the Port Royal Harbour in great numbers. 

deeper water than the backreef environment of the Falmouth 

Formation (Donovan and Gordon 1993). 

In conclusion, Diadema apparently has been the most 

abundant sea urchin on Caribbean reefs for at least 

125 000 years. Its abundance still may have increased 

historically due to overfishing, but we lack the quantitative 

data to tell. However, it now seems unlikely that any 

such increase was as great as that, for example, of 

Echinometra mathaei in response to over-fishing in

S26 

Kenyan lagoons (McClanahan and Muthiga 1988; 

McClanahan et al. 1996). Thus Diadema abundance is at 

best a secondary consequence of the degradation of Caribbean 

reefs, and we need to look for other indicators of 

faunal change in response to human interference. For this 

purpose, let us now turn to changes in the abundance of 

the really large consumers in reef environments, such as 

green turtles. 

How many turtles in 1492? 

Big animals are ecologically important, not only because 

of the amount of plants or animals each individual consumes, 

but also because of the physical and biological 

disturbance they cause, which fundamentally alters their 

environment and affects other species. Perhaps the best 

studied example is the Serengeti ecosystem of east Africa 

(Sinclair 1995a; Sinclair and Arcese 1995). Long distance 

migration (wildebeeste) and growth to very large size 

(elephant, hippopotamus, rhinoceros and buffalo) result in 

virtual escape from predation, so that such herbivores are 

‘‘bottom up’’ regulated by food limitation rather than ‘‘top 

down’’ by predators (Sinclair 1995a). The enormously 

abundant wildebeeste is a keystone species because its 

grazing and migration directly or indirectly affect almost 

everything else. Wildebeeste grazing alters the protein 

content of the grass and stimulates growth of new shoots, 

increasing the available food supply for smaller grazers, 

and possibly also for themselves (McNaughton and Banyikwa 

1995). There is also strong evidence for alternate 

stable states of vegetation (woodland versus grassland), 

maintained by grazing and disturbance by elephants and 

by fire (Dublin 1995; Sinclair 1995b). 

None of these topics have been studied as well on coral 

reefs and surrounding seagrass environments, but what we 

do know strongly suggests similarly important ecosystem 

effects of large species (Heinsohn et al. 1977; Ogden 1980; 

Thayer et al. 1984; Lanyon et al. 1989; Sheppard et al. 

1992). Green turtles crop ‘‘turtlegrass’’ ¹halassia testudinum 

to only a few centimeters above the bottom, and 

cause erosion and pits in the rhizomal mat of turtlegrass 

beds. Manatees and dugongs do much the same, sometimes 

ripping up entire beds of seagrasses and other 

aquatic vegetation, and thereby causing even greater 

physical disturbance. Stingrays excavate pits in seagrass 

beds foraging for mollusks beneath the rhizome mat, 

hawksbill turtles rip up sponges, and large parrotfishes 

occasionally bite to pieces entire coral colonies for unknown 

reasons. 

I have nothing new to add to such observations, except 

the comment that I have not even seen most of these large 

animals underwater for twenty years or more, and some of 

them never at all, despite thousands of hours SCUBA 

diving on and around coral reefs. Instead, I want to dwell 

on the past enormity of the populations of such creatures 

using green turtles as an example. My calculations are 

rough in ways that responsible turtle biologists have shied 

away from, and the data are 15 to 300 years old. Nevertheless, 

it is essential to try, because we have no conception of 

the way things were. Why, after all, are so many hundreds 

of sites around the Caribbean, such as the Dry ¹ortugas, 

named after turtles that almost no living person has 

ever seen? 

Calculations based on old hunting data from the Cayman 

Islands 

Estimates of the size of pre-columbian human populations 

in the Caribbean are controversial and depend on differing 

interpretations of archeological and historical sources 

(Roberts 1989). Nevertheless, populations of Hispaniola, 

Jamaica and Cuba certainly ranged in the hundreds of 

thousands, perhaps even in the millions, and were sustained 

by a highly productive agricultural system supplemented 

by fishing and hunting (Sauer 1966; Rouse 1992). 

These early Americans were reduced by conquest, slavery 

and disease to only a few thousand by 1600. Subsequent 

Spanish colonization was slow, so that there were only 

about five thousand people in Jamaica when the English 

captured the island in 1655 (Long 1774). There was also 

no effective agricultural base, so the English turned immediately 

for food to the vast populations of green turtles 

that nested on Grand Cayman Island (Table 2). These 

abundant turtles were essential to the rapid growth and 

success of Jamaica as England’s most important colony of 

the time, and indeed provided most of the meat consumed 

there until the 1730s (Sloane 1707, 1725; Long 1774; Lewis 

1940; King 1982). 

Thirty years later, the Cayman Islands fishery had 

grown to approximately 40 sloops and 120 to 150 men 

who brought back to Jamaica some 13 000 turtles per year 

between 1688 and 1730. Let us assume that the sex ratio 

and migration interval (time between years that females 

reproduce) were 1: 1 and 2.5 years respectively, just as they 

are today (Bjorndal 1982). Thus, the proportion of the 

adult population (N ) that are nesting females (N )is 

 

given by 

N "N /0.5 (sex ratio)0.4 (migration interval)"5N . 

 

Let us further assume that hunters in 1688 captured only 

1% of the nesting female turtles per year. This is an 

arbitrary but almost certainly conservative guess for the 

purpose of illustration, based on the impression from the 

early descriptions that the beaches all around Grand 

Cayman were literally covered by turtles, so that 13 000 

would have been a very small fraction of the total. Moreover, 

female green turtles require 40—60 years to reach 

reproductive maturity (Bjorndal and Zug 1995), so that 

harvested females could not have been replaced for half 

the century-long duration of the fishery. Despite this, 

however, 13 000 reproductively mature females were harvested 

annually over 42 y, for a total (with the above 

correction) of more than 2.5 million on this basis alone. 

Based on the assumption of an initial catch rate of 1%, the 

estimated total adult population (N ) based on the early 

 

hunting data is 

N "513 000 (number harvested)/0.01 (% N caught) 

 

"6.5 million. 

Further assume that there were five additional precolumbian 

green turtle rookeries roughly equal to Grand Cay-

Table 2. Historical accounts of 

the early great abundance of 

green turtles in the Caribbean 

Andres Bernaldez, 

writing about 

Columbus’ 

2nd voyage in 1494 

Ferdinand Columbus, 

writing about the 4th 

voyage in 1503 

Edward Long (1774), 

writing of the late 

1600s 

not seen, cited in Lewis 1940 

Southeastern 

Cuba 

Cayman 

Islands 

man including Bermuda, Bahamas, Florida Keys, 

Costa Rica, and Isla Aves (now less than a mile long but 

historically much larger). Then the estimated total adult 

population for the entire precolumbian Caribbean is five 

to six times the Grand Cayman estimate, or about 33 to 39 

million. This is about 15 to 20 times the abundance and 

biomass of large ungulates in the Serengeti today (Sinclair 

1995a)! 

Calculations based on carrying capacity 

The following is based on Bjorndal’s (1982) study of green 

turtle nutrition and life history. There is apparently no 

reliable compilation of the total area of seagrasses in the 

wider Caribbean. However, we can assume that roughly 

ten percent of the total shelf area, which is 660 000 km 

excluding south Florida (Munroe 1983), is covered by 

seagrasses for a total of 66 000 km. This is probably 

conservative, since the mapped area of seagrasses for 

south Florida alone is 5500 km (Ziemann 1982). Bjorndal 

(1982) calculated that the carrying capacity of closely 

cropped (2.5 cm) ¹halassia is one 100 kg adult female per 

72 m per year, which rounding up to one turtle per 

100 m, gives 10 000 adult females per km. Assume further 

that the carrying capacity is the same for males as for 

females. Then the estimated total adult population (N ) 

for the entire Caribbean is 

N "10 00066 000"660 million, 

which is about 20 times the estimate based on the old 

hunting data. Of course, sharks and other predators of 

principally juvenile turtles were also very much more 

abundant. However, Sinclair’s (1995a) generalization 

about the predominantly ‘‘bottom up’’ regulation of large, 

migratory herbivores suggests that the abundance of 

large, migrating adult green turtles would have approached 

carrying capacity even in the face of intense 

predation on juveniles. 

Differences in feeding between green turtles and other 

herbivores 

One adult green turtle consumes roughly the same 

amount of turtlegrass as 500 large sea urchins like Dia- 

West of the 

Cayman 

Islands 

S27 

But in those twenty leagues, they saw very many more, for 

the sea was thick with them, and they were of the very 

largest, so numerous that it seemed that the ships would run 

aground on them and were as if bathing in them. 

2in sight of two very small and low islands, full of tortoises, 

as was all the sea about, insomuch that they looked like little 

rocks2 

2it is affirmed, that vessels, which have lost their latitude in 

hazy weather, have steered entirely by the noise which these 

creatures make in swimming, to attain the Cayman isles. 

dema antillarum or ¹ripneustes ventricosus, which works 

out to a potential increase of about 5 sea urchins per m of 

seagrass beds throughout the Caribbean (calculations 

based on data in Thayer et al. 1984). Much more significantly, 

however, there are profound differences in the 

ways turtles versus sea urchins and herbivorous fishes 

graze on turtlegrass, and how well they process what they 

eat, with important consequences for the structure and 

function of the entire turtlegrass ecosystem (Ogden 1980; 

Thayer et al. 1982, 1984; Ogden et al. 1983). Sea urchins 

and fishes tend to feed indiscriminantly on turtlegrass, or 

on the older parts of the blades, whereas green turtles crop 

blades close to their base. They also return repeatedly to 

the same discrete grazing plots which may be maintained 

for a year or more. Moreover, grazing sea urchins and 

fishes feed principally on the cell contents of seagrass 

blades, due to lack of appropriate enzymes or microflora 

to digest cell walls, whereas green turtles rely on microbial 

fermentation in the hindgut to digest cell walls as well as 

their contents (Thayer et al. 1984). 

Repeated grazing of the same plots of turtlegrass by 

green turtles temporarily increases the nutritional quality 

of the blades for the turtles (Thayer et al. 1984). However, 

it also stresses the plants and eventually reduces turtlegrass 

productivity, when turtles presumably move on to 

feed elsewhere. Turtle grazing also results in a roughly 

15-fold decrease in the supply of nitrogen to seagrass roots 

and rhizomes, due to greatly decreased accumulation of 

detritus and digestion of cell walls (Thayer et al. 1984). 

Nitrogen in turtle feces and urine is also released over 

a much wider area with resulting net export to adjacent 

coral reefs and other adjacent ecosystems. 

These differences in the effects of grazing by small and 

large herbivores extend to dugongs and manatees that 

also possess hindgut microflora that digest cell walls 

(Thayer et al. 1984), and were also formerly very abundant 

throughout tropical seas (Dampier 1729, Sheppard et al. 

1992). Similar ecosystem effects almost certainly transpired 

on coral reefs due to the virtual disappearance of 

large predators such as hawksbill turtles, groupers, and 

sharks that were also extremely abundant historically 

(Ibid, King 1982; Limpus 1995). For example, the hawksbill 

turtle, Eretmochelys imbricata, feeds almost exclusively 

on sponges which commonly display large, characteristic 

feeding scars in areas where the turtles are still common 

(Meylan 1985, 1988; van Dam and Diez, in press). Hawksbills 

can rip big sponges apart, and in the process facilitate

S28 

predation by other sponge feeders that cannot penetrate 

the heavy armor of many sponges such as Geodia; unlike 

the much smaller angelfishes that also feed almost exclusively 

on reef sponges (Randall and Hartman 1968). Hawksbills 

feed today mostly on non-toxic astrophorid and 

hadromerid sponges, but this may not have been true in 

the past when, by analogy to green turtles (King 1982; 

Limpus 1995; this study), hawksbills almost certainly 

numbered in the tens of millions. Thus non-toxic sponges 

may have been proportionally rarer before hawksbills 

were intensely harvested. 

Large herbivores and carnivores are ecologically extinct 

on Caribbean coral reefs and seagrass beds, where food 

chains are now dominated by small fishes and invertebrates 

(Hay 1984, 1991; Knowlton et al. 1990). Moreover, 

similar depletion of megavertebrates is almost complete 

throughout the Indo-Pacific (Sheppard et al. 1992; Limpus 

1995). Small consumers cannot fully compensate for 

the loss of megavertebrates because they cannot capture, 

consume or process their prey in the same ways as larger 

species. Many small herbivores are also feeding specialists, 

and live commonly on prey that are chemically defended 

against the much larger consumers that have now disappeared 

(Hay 1991, in press). Thus coral reef ecosystems 

must function in fundamentally different ways than only 

a few centuries ago. Similarly great changes are going on 

right now in east Africa (Sinclair and Arcese 1995). They 

also occurred 10 000 years ago in neotropical forests when 

over 15 genera of large herbivores became extinct (Janzen 

and Martin 1982), before which forests were probably 

more of a mixture of open forest and grassland than the 

dense tropical forest we imagine as more natural (Janzen 

and Wilson 1983). As a result, neotropical herbivorous 

food chains are now dominated by insects and small 

mammals, except where free-ranging livestock may have 

partially redressed the balance. But there are no such 

livestock on coral reefs! 

Effects from the land 

Sedimentation caused by deforestation and poor agricultural 

practice, eutrophication, and oil pollution have 

greatly increased along Caribbean coasts during the 

past few decades (Rodriguez 1981; Lugo et al. 1981), 

causing widespread and dramatic decline of coral reefs 

and associated marine communities throughout the 

region (Cortés and Risk 1985; Rogers 1985, 1990; 

Tomascik and Sander 1985, 1987a, b; Bak 1987; Jackson 

et al. 1989; Guzmán et al. 1991). A common assumption in 

such studies is that most reefs were not seriously affected 

by runoff from the land before the observations began. 

This allows the investigator to designate ‘‘unaffected’’ reefs 

or corals that can be used as a baseline to measure the 

effects of a particular source of pollution, such as an oil 

spill. 

New evidence, however, suggests that great ecological 

changes due to runoff began long before modern ecological 

analyses of Caribbean reefs. For example, Montastrea 

‘‘annularis’’ and Porites spp. were the dominant reef building 

corals around Barbados in the 1960s and 1970s (Lewis 

1960; Macintyre 1968; Stearn et al. 1977). These began to 

decline dramatically in the 1970s and 1980s, due primarily 

to runoff and eutrophication caused by exponential increase 

in populations of residents and tourists (Tomascik 

and Sander 1985, 1987a, b; Bell and Tomascik 1993). 

However, extensive deforestation began in Barbados in 

1627 for sugar plantations, after which the vegetation of 

the island was completely destroyed three times by hurricanes 

(references in Lewis 1984); with untold increases in 

runoff of sediments from the land. Moreover, shallow reefs 

at that time were dominated by the elkhorn coral Acropora 

palmata, which persisted in huge tracts all along the 

southern and western coasts of the island until the 1920s 

(Nutting 1919; Lewis 1984; Bell and Tomascik 1993), and 

the same was true throughout the Late Pleistocene (Mesolella 

1957; Jackson 1992). Degradation of these reefs and 

seagrass beds was clearly visible in aerial photographs 

taken in the 1950s (Lewsey 1978) when elkhorn corals 

were rare (Lewis 1960). 

Similar decline in Acropora palmata and A. cervicornis 

occurred all along the coast of lower Central America in 

the 1970s and 1980s due to disease, deforestation, algal 

overgrowth due to the decline of Diadema, coral bleaching, 

oil spills, and other factors (Cortés and Risk 1985; 

Cortés 1993; Guzmán et al. 1991; Ogden and Ogden 1993). 

Live coral cover along the Caribbean coast of central 

Panama has declined by 50—90% in the past ten years 

(Guzmán and Jackson, unpublished data). However, there 

were hidden signs of danger long before, as measured by 

a steady decline of nearly 50% in the growth rate of the 

massive coral Siderastrea siderea over the past century 

(H. Guzmán, unpublished data). This is all the more 

remarkable because S. siderea generally prospers in turbid 

coastal environments unsuitable to most other Caribbean 

coral species. Guzmán’s work obviously needs to be replicated 

elsewhere, but it strongly suggests that reef environments 

had begun to deteriorate at least 100 years 

before coral cover began to seriously decline. Isotopic 

ratios provide excellent proxy records of climate change, 

but simple growth rates and incidence of injuries are 

measures of coral fitness through time (Jackson 1982). As 

such, they may be among the best available measures of 

coral reef health (Dodge and Vaisnys 1977; Guzmán et al. 

1994; Jackson 1995). 

Fishing and people in Jamaica and San Blas 

The green turtle fishery in the Cayman Islands crashed in 

the latter half of the eighteenth century, and was entirely 

gone by 1800 when the Cayman islanders moved on to do 

the same thing to the turtles of the Moskito Coast (Long 

1774; Lewis 1940; Carr 1956; Neitschmann 1973, 1982; 

King 1982). Fishing on Jamaican reefs was inadequate to 

make up for the loss of turtles. By 1881 locally caught fish 

accounted for only 15% of the total consumed in Jamaica, 

with imported dried and preserved fish from the temperate 

zone making up the balance (Duerden 1901). This was 

probably true by the early 1800s, but there are not enough 

quantitative data. Moreover, extensive trials had clearly 

demonstrated that there was little prospect for improvement 

of local fisheries by trawling or longline fishing which 

are unsuitable for areas of coral reefs (Duerden 1901).

Table 3. Excerpts from Ernest F. 

Thompson’s 1945 report ¹he 

fisheries of Jamaica 

Despite these realities, Duerden’s (1901) official report 

was surprisingly optimistic and, in a still all too familiar 

tone, called for more ‘‘scientific investigations and encouragement’’ 

to improve the marine resources of the Caribbean 

region. Half a century later the fisheries of Jamaica 

had not improved and were clearly unimprovable 

(Thompson 1945, Table 3). Thompson was far ahead of his 

time in recognizing the need for greatly reducing the 

numbers of fishermen, helping them to find alternative 

livelihoods, and focusing instead on the economic opportunities 

of fishing for tourism. But his report was apparently 

ignored and overfishing continued unabated. 

By far the most extensive coral reef fisheries research 

project in the Caribbean was carried out from 1969—1973 

all around Jamaica and in the Pedro Cays (Munroe 1983). 

Overfishing was accepted as an established fact, and it was 

‘‘shown that for most areas of the Jamaican Shelf, the 

fishing intensity is sufficient to ensure that extremely few 

fishes survive for more than a year after recruitment, and 

the proportion of fishes which survive to spawn must be 

extremely small.’’ The report goes on to recommend 

a mesh size for fish traps of 6.60 cm maximum aperture 

that would provide a maximum yield of barely reproductive 

juveniles with a maximum fishing intensity of 1.5 

canoes/km, without any consideration of the possible 

consequences for the health of the entire coral reef ecosystem. 

Of course, it is easy to be unfairly critical with the 

hindsight of the Diadema debacle and the collapse of 

Jamaican reefs (Hughes 1994), although even in the 1970s 

the consequences of not having any pretty reef fishes 

larger than sardines on lost tourist revenues were clear. 

The situation in Jamaica is a story repeated everywhere 

throughout the Caribbean, including the traditional fisheries 

of indigenous peoples commonly romanticized for exhibiting 

wise restraint from overharvesting not observed 

by others. The Comarca Kuna Yala, for example, extends 

some 250 km along the eastern Caribbean coast of Panamá 

and contains extensive coral reefs, seagrass beds 

and mangroves (Porter 1972; Glynn 1973; Clifton 

et al. 1996). The population of Kuna people within the 

Comarca increased from less than 9000 in 1904 to less 

than 24 000 in 1970, when marine biological research 

intensified in the Comarca, and had climbed to 41 000 in 

1989 (Francisco Herrera, personal communication). Kuna 

Locally caught fish represents less than 15% of the protein fish food consumed in Jamaica2 There is 

little prospect of any large increase in this local catch. In fact the probability is that the local areas are 

already overfished (p. 5) 

2the greatest need for Jamaican fishermen is more in the nature of welfare than development (p. 7, 

Thompson’s italics). 

In a great many countries, fishing has proved a very valuable asset as a tourist attraction. Development 

of the tourist potential would require that the present usages of some sections of the community must be 

controlled and restricted (p. 7). 

The fishing situation in Jamaica can be very briefly summarised. There are too many men trying to catch 

too few fish. As there seems little prospect of increasing the number of fish available, the only thing to do, 

if a decent living standard is to be attained, is to reduce the number of fishermen. Thus the chief problem 

for Jamaican fishermen is to organize them, stabilise their economy and assist about four-fifths of them 

to drift back to agriculture from whence they came (p. 83) 

S29 

artesanal fishing has always been a small-scale enterprise, 

and the Comarca is closely guarded against outside exploitation. 

Nevertheless, reefs were severely overfished by 

the 1970s when large fishes were uncommon and branching 

acroporid and poritid corals had been mined extensively 

for landfill. Thus 250 km of coast were already 

insufficient for 24 000 Kuna, ten years before lobster fishing 

for external markets reduced lobster populations to 

critically low levels within only ten years (Chapin 1995; 

Ventocilla et al. 1995). 

So let us now return to Jamaica to consider the history 

of Jamaican fisheries in light of human growth, much as 

Hughes (1994) did, but beginning 350 years before (Fig. 1). 

Depopulation by the Spaniards in the sixteenth century 

left the island almost uninhabited until the British invasion 

in 1655, when marine life may well have been at its 

apogee of the past 10 000 years. In 1688, when Sloane was 

in Jamaica, there were still only 40 000 Jamaicans and 

Diadema was the most abundant sea urchin on coral reefs. 

In 1793, there were 300 000 Jamaicans and breadfruit had 

just been introduced following extensive research by the 

Royal Society and the mutiny on the Bounty, to help stave 

off the starvation of Jamaican slaves. In 1881, there were 

700 000 Jamaicans and local fish accounted for only 15% 

of the fish consumed. In 1945 there were 1 350 000 Jamaicans, 

and the 5 500 000 kg of fish caught locally was still 

only 15% of that consumed. In 1962 there were 1 700 000 

Jamaicans and the fish harvest peaked at 11 000 000 kg. 

This was also when Goreau (1959) published his first 

famous paper about Jamaican coral reefs and the modern 

ecological perspective was born. By 1968, when I began 

my own research in Jamaica, there were 1 900 000 Jamaicans, 

and the harvest of minnow-sized fishes from Jamaican 

coastal waters was back down to 5 500 000 kg. 

Munroe’s fisheries research project was only just beginning. 

It is obvious that any direct relationship between human 

population growth and fishing in Jamaica ended in 

the eighteenth century when human populations were 

only 10% of the present. Throughout this time, Jamaicans 

kept on eating fish courtesy of the now collapsed Grand 

Banks fisheries, and the same was true throughout the 

Caribbean. Thus, the causes of the present ecocatastrophe 

are deep and historical, not just the almost ‘‘current 

events’’ that have passed as history before.

S30 

Fig. 1. Jamaican human population growth since Columbus and the 

depletion of local fisheries resources. Fisheries became inadequate 

some time in the mid nineteenth century when the local population 

was about 15% of that today. Value for 1492 arbitraily set at 100 000 

which is almost certainly much too low (Sauer 1966). Sources for 

population size: 1658—1768 (Long 1774), 1844—1871 (Gardner 1909). 

1901 (Duerden 1901), 1920—2000 (Hughes 1994), 1980 (National 

Geographic Society 1981) 

Concluding remarks 

I hope this brief discussion will put to rest two dangerous 

stupidities, at least within the scientific community. The 

first is the placebo of sustainable use for everyone and the 

second is the fallacy of a ‘‘pristine’’ coral reef. Forty 

thousand Kuna are too many fish eaters for 250 km of 

coastline (Ventocilla et al. 1995), just as a few hundred 

thousand Jamaicans were too many fish eaters for 

Jamaica. The same is true for reefs everywhere else, and 

not just the developing world (Wilkinson 1992). Even the 

Great Barrier Reef cannot be used sustainably at present 

levels, despite the best protection in the world (Bradbury 

et al. 1992), and virtually all other reefs are less sustainable. 

There is nothing new about all this, as described so 

eloquently in Peter Matthiessen’s (1975, 1986) eulogies to 

the turtle fishermen of Grand Cayman or the striped bass 

fishermen of the South Fork of Long Island. However, 

societies desperately need to set goals and priorities that 

reflect the realities of our lost and dying coral reef resources, 

and then follow them. For example, coral reef 

fishes may still provide sustainable luxury food and pleasure 

for tourists, just as Thompson (1945) proposed, and 

captive breeding of aquarium fishes is almost certainly 

a viable enterprise. Deciding on such options to the exclusion 

of others, and then enforcing them, involves extremely 

difficult economic, political and social issues beyond the 

bounds of ecological science. But some such decisions are 

long overdue, and no more research is required to get 

started, because the facts about ‘‘sustainability’’ have been 

clear for more than one hundred years. 

Getting things straight is all the more important because, 

as far as we can tell, almost all the reef species are 

still there almost everywhere. The Caribbean monk seal is 

extinct and manatees are nearly gone, but even green 

turtles still number in the tens of thousands in the Caribbean. 

This means that it is still possible, at least in principle, 

to save Caribbean coral reefs; although continued 

human population growth makes this more and more 

unlikely. For example, all the species of corals encountered 

previously on Panamanian Caribbean reefs are still 

there, even on some of the most devastated reefs, despite 

huge decreases in coral abundance (Guzmán and Jackson, 

unpublished data). Thus the situation is like the East 

African savannas where large animals are more and more 

restricted and diminished, but the great majority of species 

alive during the Pleistocene still survive (Sinclair and 

Arcese 1995). 

For this reason, and by analogy to the Serengeti, really 

large marine protected areas on the scale of hundreds to 

thousands of square kilometers are vital to any hope of 

conserving Caribbean coral reefs and coral reef species. 

Can we restore damaged reefs? Can we control inputs 

from the land and harvesting? Can we manage what we do 

decide to invest in and use? These are the questions that 

really do merit more research on a monumental scale 

(NRC 1995). The people trying to answer them are the 

heros of our discipline and the only chance we have got. 

Acknowledgements. N. Knowlton talked me into writing all this 

depressing stuff down and helped in innumerable other ways. Conversations 

with P. Dayton, L. D’Croz, H. Guzma´ n, J. Lang, J. 

Ogden, R. Robertson, A. Rodaniche, and J. Wulff helped greatly to 

focus my approach. A. Herrera and A. Aguirre tracked down countless 

obscure references which the Smithsonian Libraries obtained 

with their customary efficiency and grace. F. Herrera kindly provided 

data for Kuna populations inside the Comarca which are not 

separated from other mainland Kuna populations in the Government 

of Panama statistics. N. Knowlton, H. Lessios, D. Levitan and 

one other reviewer criticized the manuscript and made many helpful 

suggestions. To all I am very grateful. 

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Social Interactions in Captive Female 

Florida Manatees 

Jennifer Young Harper and Bruce A. Schulte n 

Zoo Biology 24:135–144 (2005) 

Department of Biology, Georgia Southern University, Statesboro, Georgia 

The Florida manatee (Trichechus manatus latirostris) is considered a semi-social 

species with strong bonds developed primarily between mother and offspring. 

Some field studies suggest sociality may be more developed and such social 

relationships may facilitate survival. Seven facilities in Florida house manatees, 

many of which were brought into captivity because of injury or illness sustained in 

the wild. Decisions to release such manatees consider individual history and 

health. We examined social interactions in adult female captive manatees to assess 

level of association and implications for manatee care and release. We 

investigated the degree of contact among 20 manatees in captivity at four 

facilities housing two to nine adult female manatees. We used all contact behavior 

occurrences sampling and continuous recording for 180 continuous minutes per 

day over 3 consecutive days at each facility. Virtually all contacts were nonaggressive. 

The number of contacts between manatees increased as the number of 

manatees per unit volume of water increased. Contacts did not fit a Poisson 

distribution, however, and were not random. When more than two manatees were 

present, manatees only associated with a subset of individuals in the aquarium. 

Relationships maintained in captivity indicate the potentially social nature of 

manatees, and suggest that further research is needed to examine the benefit of 

these relationships to the health and rehabilitation of manatees in captivity and 

conservation in the wild. Zoo Biol 24:135–144, 2005. c 2005 Wiley-Liss, Inc. 

Key words: aggression; association; conservation; ethogram; interaction; social behavior 

INTRODUCTION 

The organization of individuals into social groups is likely to evolve when the 

benefits of group living outweigh the costs [Alexander, 1974; Emlen 1997]. Benefits of 

Dr. Jennifer Young Harper’s present address is Coastal Georgia Community College, 3700 Altama 

Avenue, Brunswick, GA 31520. 

n 

Correspondence to: Bruce A. Schulte, Department of Biology PO Box 8042, Georgia Southern 

University, Statesboro, Georgia, 30460-8042. E-mail: bschulte@georgiasouthern.edu 

Received 2 April 2004; Accepted 8 November 2004 

DOI 10.1002/zoo.20044 

Published online in Wiley InterScience (www.interscience.wiley.com). 

c 2005 Wiley-Liss, Inc.

136 Harper and Schulte 

group living include greater access to resources and protection. Group living has 

ecological costs including an increase in competition for food, space, and mates and 

exposure to parasites, pathogens, and predators. Conflicts and aggression can 

become heightened in crowded areas, especially when there is competition over a 

limited resource. The resolution of conflict can occur when individuals leave a 

particular situation, defend territories, form small closely associated groups, or 

establish dominance hierarchies built upon aggression or affiliation [Maher and 

Lott, 1995, 2000; Pusey and Packer, 1999]. 

Florida manatees (Trichechus manatus latirostris), a subspecies of the West 

Indian manatee, are considered semi-social or asocial animals, because they 

generally do not form organized social structures. Manatees are usually seen 

traveling in warmer coastal waters alone or in mother–calf pairs, with such bonds 

lasting until the calf is approximately 1–2 years old [Reynolds and Odell, 1991]. 

From 1993–1996, Koelsch [1997] observed manatees in Sarasota Bay, Florida and 

noted some strong bonds among adult manatees. In addition, associations were 

stronger within than between the sexes. These non-random association patterns 

along with the social facilitation noted by Reynolds [1981] suggest that manatees 

may be more social than previously thought [Koelsch, 1997]. The current study 

investigated the type and extent of interactions among female manatees held in 

captivity to evaluate the strength of social bonds. 

Manatees in the wild face many problems in their aquatic environment 

including ingestion of foreign materials [Beck and Barros, 1991], exposure to toxins 

such as red tide [Bossart et al., 1998], and collisions with boats [Wright et al., 1995]. 

Injured or sick manatees are taken into captivity for rehabilitation. Once an injured 

animal is out of critical care in a captive facility, it is usually housed with several 

other manatees of the same sex. We know relatively little, however, about how these 

supposed semi-social animals behave in the constant presence of multiple 

conspecifics. The specific objective of this research was to determine if manatees in 

captivity exhibit behaviors that are either aggressive, serve to reduce aggression or 

reflect the establishment of particular associations. Manatees were observed before, 

during, and after feeding periods because conflicts might arise in anticipation of, or 

during consumption of, food (a potentially limited resource). We examined two 

hypotheses on level of interaction: (1) manatees will rarely interact; and (2) manatees 

will interact more under higher density situations (i.e., more manatees per unit 

volume of aquarium space). In addition, we evaluated two hypotheses on the timing 

and type of interactions. Specifically, (3) most interactions will be aggressive and 

occur just before feeding or when food is becoming depleted, and (4) if manatees are 

more social than previously thought, most interactions will be non-aggressive and 

occur outside of feeding periods. 


Study Sites 

This research was conducted from January–March 2001 at four zoos and 

aquariums housing captive manatees, specifically Homosassa Springs Wildlife State 

Park (HSWSP, Homosassa, Florida), Lowry Park Zoo (Tampa, Florida), Sea World 

of Florida (Orlando, Florida), and Walt Disney World’s The Living Seas in Epcot

Captive Female Manatee Social Behavior 137 

(Orlando, Florida). Generally, manatees were housed in human-made enclosures 

approximately 3 m in depth and oval in shape. The exception was HSWSP, which is 

a naturally occurring spring that covers approximately 0.2 ha and reaches depths of 

13.5 m. Manatees (n ¼ 20) at all facilities were viewed from an underwater 

observation area or from above the enclosure. We estimated the volume of water 

for HSWSP from the dimensions of the exhibit. The other three facilities provided us 

with aquarium volumes. Water volumes at each facility are as follows: HSWSP (1.1 

10 7 L [9 manatees]), Sea World (1.4 10 6 L [6 manatees]), Epcot (760,000 L 

[2 manatees]), and Lowry Park Zoo (470,000 L [3 manatees]). 

Behavioral Observations 

Manatees were watched continuously for 180 min over 3 days around 

feeding times. The time duration was selected because there were constraints 

at the facilities that prevented longer observation periods including operating 

hours, interference in observations when visitor numbers were high, and 

logistical issues. Observations were made at the four facilities with 20 individuals 

for a total of 36 hr. No adult males were observed for this study, but three 

juvenile male manatees were observed. One male was at Lowry Park Zoo 

and two were at Sea World. All three males were with females. During the 

3 hr of continuous observations for all interactions, we recorded all aggressive 

and non-aggressive contacts between manatees (sender–receiver) and spatial 

displacement by manatees [Martin and Bateson, 1993]. Aggressive interactions were 

defined as contacts in which the sender’s head touched the receiver with some 

momentum or caused physical movement of the receiver. Displacement was occurred 

when one manatee (sender) caused another manatee (receiver) to move from its 

location without contact because of the presence or movement of the sender. 

Displacements were rare and not considered in the analysis. Other aggressive 

interactions occurred when the sender’s tail hit the receiver with force as it swam 

away. Non-aggressive interactions that might be affiliative in nature included all 

other contacts (head to different body parts, body to different body parts, fin to 

different body parts, and tail to different body parts without force). Incidental 

contacts transpired when an animal brushed against another animal. These contacts 

were not included in the analysis. 

Manatees at all facilities were fed 25–100 heads of romaine lettuce 

depending on the number of manatees in the aquarium (one head weighs 

approximately 488 grams; V. Burke, head keeper at Lowry Park Zoo, 

personal communication). Feeding occurred three to four times a day at regular 

intervals. Three observational periods were defined as pre-feeding, during-feeding, 

and post-feeding. The pre-feeding period occurred during the first 60 min of 

observations before the handlers provisioned any food. The feeding period occurred 

when the manatees were feeding and post-feeding was defined as when 10% or less of 

the food remained (heads and leaves combined). The number of heads of lettuce 

(or leaf equivalents) that remained in the aquarium were counted and recorded every 

5 min. Feeding periods lasted approximately 1 hr. Supplemental foods such as 

carrots, kale, and apples were sometimes provided to manatees by the aquarium 

staff, but not included in the determination of feeding or non-feeding observational 

periods.


Data Analysis 

The total number of contacts for each day and facility was counted. The 

proportion of aggressive or non-aggressive interactions by manatees at each facility 

was calculated by observational period over the 3 consecutive days of observations. 

Similar proportions also were calculated for individual manatees as sender and as 

receiver. Sender-receiver matrices were created for each facility. Non-aggressive 

contacts were used to construct sender-receiver matrices because of the low 

occurrence of aggressive contacts. Animals were ordered in the matrices based on the 

total number of contacts sent. Log-linear G-test analyses were used to examine if 

non-aggressive contacts were more likely before or after feeding at separate facilities 

and to compare the distribution among facilities of non-aggressive contacts before 

and after feeding. Linear regression was used to determine the effect of density on 

total number of contacts. We calculated the coefficient of dispersion (CD) using the 

number of contacts between unique pairs of manatees to determine if contacts fit a 

Poisson distribution, where values greater than one show a clumped distribution, 

whereas values less than one indicate repulsion. For the two facilities (HSWSP and 

SeaWorld) with greater than three manatees, we analyzed the distribution of these 

contacts using a G-test with the Williams correction factor [Sokal and Rohlf, 1995]. 

The distribution is determined by the frequency of manatee pairs with zero to the 

maximum number of observed contacts. To maintain frequencies of at least four 

occurrences per cell (i.e., contacts/manatee pair) some categories were combined. In 

the two analyses, we used three categories. Because the parameter mean in each case 

was estimated from the sample, two degrees of freedom were removed, yielding a 

single degree of freedom for the G-statistic [Sokal and Rohlf, 1995]. Significant 

variation from a Poisson distribution indicated a non-random pattern of contacts. 

Analyses were carried out using JMP, version 3.02 (SAS Institute Inc., Cary, NC), 

and by methods described by Sokal and Rohlf [1995]. 

RESULTS 

Manatees interacted regularly during the non-feeding periods of our study. We 

observed no contacts between manatees while they were feeding. Of the 218 nonaggressive 

encounters, 98 (45%) occurred in the pre-feeding period and 120 (55%) in 

the post-feeding period. The pre-feeding period was always 60 min long whereas the 

post period ranged from 30–75 min (55.773.62 min, mean7SE). The number of 

non-aggressive contacts did not differ in the pre- vs. the post-feeding observational 

period within each facility (all Go1.1, df ¼ 1, P40.05). The distribution of nonaggressive 

contacts also did not differ in the pre- and post-feeding periods among the 

four facilities (G ¼ 2.02, df ¼ 3, P40.05). The number of total contacts per day 

ranged from 10–34 at each of the four facilities (means7SE of contacts/hr: Day 

1 ¼ 6.7572.11, Day 2 ¼ 6.371.48, Day 3 ¼ 5.970.89). 

Of the 228 contacts recorded, only 10 (4.39%) were aggressive. The manatees 

at Lowry Park Zoo accounted for nine of 10 aggressive encounters and seven were 

observed during a single 180-min observation session. These contacts were head-tobody 

contacts mostly by the adult females to a 9-month-old orphaned male. Using 

sender-receiver matrices based upon non-aggressive contacts, we discuss manatee 

interactions at each facility.


Epcot: The Living Seas 

Walt Disney World’s The Living Seas in Epcot housed two female manatees, 

Lydia and Mariah. Forty-three non-aggressive contacts (4.871.3 contacts/hr) 

occurred between these two manatees. Lydia initiated 20 contacts and Mariah 

initiated 23. 

Homosassa Springs Wildlife State Park 

Homosassa Springs Wildlife State Park housed nine female manatees: 

Amanda, Ariel, Betsy, Electra, Holly, Lorelei, Oakley, Rosie, and Willoughby. 

Thirty-one non-aggressive contacts (3.470.1 contacts/hr) occurred between the 

manatees. Eighteen contacts were made between three related individuals (Amanda, 

Ariel and Betsy) termed Group one, consisting of a mother and her two adult 

daughters. The remaining six manatees made 12 contacts to each other with only one 

contact made between the two groups of manatees (Table 1). 

Lowry Park Zoo 

Lowry Park Zoo housed two female manatees, Cinco and BB, and one 

orphaned male calf, Lowry. Eighty-three contacts occurred between these manatees; 

nine were aggressive (10.8%, 1.070.67 contacts/hr) and 74 were non-aggressive 

(89.2%, 8.270.9 contacts/hr). BB initiated five aggressive contacts to Lowry. Both 

Cinco and Lowry made two aggressive contacts (22.2%) toward each other. Lowry 

initiated the most non-aggressive contacts (38). BB and Cinco initiated 20 and 16 

non-aggressive contacts, respectively. For the adult females, BB initiated contact 

with Cinco eight times and Cinco contacted BB nine times. 

Sea World 

Sea World of Florida housed four adult female manatees: Charlotte, Rita, 

Sara, and Stubbie and two orphaned male calves: Brooks and Pistachio. Of the 71 

interactions that occurred, 70 (98.6%, 7.871.0 contacts/hr) were non-aggressive and 

one (1.4%, 0.170.1 contact/hr) was aggressive. The juvenile males initiated more 

contacts than the adult females (52 of 71 or 73%). Brooks made 34 contacts with 

most directed toward Charlotte (15) and Sara (13). These were primarily play 

mounting contacts with the two females. Pistachio initiated four similar contacts 

TABLE 1. Matrix constructed from non-aggressive contacts at Homosassa Springs Wildlife 

State Park with nine adult females 

Amanda a Rosie Betsy a Ariel a Holly Will Oakley Lorelei Electra Total 

Amanda — 0 2 7 0 0 0 1 0 10 

Rosie 0 — 0 0 1 1 2 0 3 7 

Betsy 3 0 — 2 0 0 0 0 0 5 

Ariel 2 0 2 — 0 0 0 0 0 4 

Holly 0 0 0 0 — 1 0 0 1 2 

Will 0 0 0 0 0 — 1 0 0 1 

Oakley 0 0 0 0 0 1 — 0 0 1 

Lorelei 0 0 0 0 0 1 0 — 0 1 

Electra 0 0 0 0 0 0 0 0 — 0 

a Amanda, Betsy and Ariel are related as mother and two adult daughters.


each to Sara, Rita and Stubbie. Excluding the juvenile males from total contacts, 

Charlotte and Sara accounted for 11 of the 13 encounters (Table 2). 

All Facilities 

All manatees, with the exception of one, were involved in some type of 

interaction with other individuals. Density of manatees per unit volume explained 

the majority of variation in contact rates (Fig. 1; r 2 ¼ 0.96). The coefficient of 

TABLE 2. Matrix constructed from non-aggressive manatee contacts at Sea World of Florida 

Brooks a 

Pistachio b 

Charlotte c 

Sara c 

Rita c 

Stubbie c 

Total 

Brooks — 3 15 13 2 2 35 

Pistachio 3 — 1 4 4 4 16 

Charlotte 1 0 — 8 0 0 9 

Sara 2 0 3 — 0 0 5 

Rita 0 0 1 1 — 0 2 

Stubbie 1 0 0 0 0 — 1 

a Juvenile manatee (2 years old). 

b Juvenile manatee (1.5 years old). 

c Adult female manatee. 

Total Number of Contacts 

90 

80 

70 

60 

50 

40 

30 

20 

10 

0 

HSSP 

Epcot 

SeaWorld 

y = 9.9482x + 21.887 

R 2 = 0.96 

0 1 2 3 4 5 6 

Number of Manatees per 1,000,000 L water 

Fig. 1. Number of contacts for each facility (Homosassa Springs Wildlife State Park, Walt 

Disney World’s The Living Seas at Epcot, Sea World of Florida, and Lowry Park Zoo) 

initiated by manatees per million L water within each aquarium. 

LPZ 

7


dispersion (CD) at the three facilities with at least three manatees was always greater 

than one, indicating clumping of the distribution (HSWSP ¼ 3.9, SeaWorld ¼ 6.2, 

Lowry Park Zoo ¼ 1.9). The distribution of contacts was significantly different from 

a Poisson distribution for HSWSP (Gadj ¼ 9.24w 2 0.05[1] ¼ 3.84) and for SeaWorld 

(Gadj ¼ 13.74w 2 0.05[1] ¼ 3.84). We could not perform the analysis for Lowry Park 

Zoo because of the low number of manatees, resulting in single frequencies per cell. 

DISCUSSION 

Manatees in captivity associated and interacted with certain individuals. The 

occurrence of regular, non-aggressive contacts by manatees in captivity and the 

relative rarity of aggressive contacts support the contention that manatees may be 

more social than previously considered [Koelsch, 1997]. Hence, we reject our first 

hypothesis that manatees will rarely interact. The number of non-aggressive contacts 

increased with density (Fig. 1), supporting our second hypothesis. Aggression was 

rare and only occurred at the facilities with the greatest densities (Lowry Park Zoo 

and SeaWorld) but these facilities had one or two juvenile males in with the females. 

Of the ten total aggressive encounters observed, nine were recorded at Lowry Park 

Zoo. These aggressive contacts were directed mainly toward the 9-month-old male 

Lowry by the adult females, possibly to prevent the formation of a mother–calf 

bond. Lowry was born in captivity but his mother Ionia died from her injuries 

during rehabilitation when Lowry was introduced to the two resident adult females, 

BB and Cinco. Because aggression was rare and not related to feeding, we reject our 

third hypothesis and show support for our fourth hypothesis that most interactions 

will be non-aggressive and occur outside of feeding periods. A concurrent study 

showed that time in captivity or differences in facilities did not affect manatee 

activity patterns [Young, 2001]. 

The density-dependent nature of non-aggressive interactions suggests that 

contacts were random and not selective. Interactions were not equally distributed, 

however, among manatees at least at the two facilities with more than three 

manatees. At HSWSP, greater association was apparent within two social 

subgroups. One subgroup consisted of Amanda and her two adult daughters, Ariel 

and Betsy. This observation in captivity fits nicely with field studies, where mother 

and offspring form the most apparent long-term bonds during calf dependency in the 

wild [Hartman, 1979; Bengtson, 1981; Reynolds, 1981]. All three animals were adults 

(Betsy is the youngest, born in captivity in 1990). This long-term close association 

may be common in the wild or an artifact of captivity. These three individuals 

contacted the other subgroup composed of six unrelated manatees only once. In 

contrast, this subgroup exhibited 12 contacts within the group and no contacts to 

Amanda, Ariel, or Betsy. Random interactions would predict more contacts between 

the two subgroups and the analysis supported a clumped distribution of contacts. 

This segregation of manatees is especially interesting at HSWSP, which represented 

the site with the lowest density of manatees. 

At Sea World of Florida, Charlotte and Sara associated regularly with Rita on 

the periphery of this pair. The two young males (Brooks and Pistachio) initiated a 

majority of the contacts, mostly as play mounting contacts with the females. Between 

the females, the overall distribution of contacts was clumped, not random. At Lowry 

Park Zoo, the two adult females, BB and Cinco initiated non-aggressive contacts to


each other in nearly equal number, while never initiating aggressive contacts to one 

another. This contrasted with the relationship to the orphaned, nine-month-old 

male, who received aggressive and non-aggressive contacts. The two adult females at 

Epcot showed a similarly reciprocal level of non-aggressive contact initiation as 

those at Lowry Park Zoo. Such equal initiation of contacts suggests an absence of 

dominance but with only a few animals, statistical analysis is not appropriate. 

In wild manatees, affiliative social interactions have been observed between 

adult females [Koelsch, 1997]. Mothers and calves associate regularly [Hartman, 

1979; Reynolds and Odell, 1991; Koelsch, 1997], but it is uncertain if this 

relationship lasts until adulthood as exhibited by the captive manatees in subgroup 

one at HSWSP. Elephants are the closest living relative of the Sirenia, and they form 

close mother–calf associations that last into adulthood for females [Buss and Smith, 

1966; Eisenberg et al., 1971; Douglas-Hamilton, 1972; Moss 1976; Dublin, 1983]. 

The calf learns basic life skills from its mother and social group members [Lee and 

Moss, 1999], and young males have even been observed play mounting with their 

mothers or other females within their group [Gadgil and Nair, 1983]. Similar play 

behavior toward adult female manatees was observed with juvenile males at Sea 

World. In the wild, juveniles seem to be submissive to adult manatees [Hartman, 

1979], perhaps explaining the prevalence of aggressive contacts initiated by the adult 

females toward the juvenile male, Lowry. The types of associations observed with 

captive manatees are similar to those described by other mammals in captivity 

including elephants [Schulte, 2000], zebras [Schilder, 1992], captive spotted hyenas 

[Glickman et al., 1997], and bonobos [de Waal, 1995]. 

In the case of manatees, understanding relationships in captivity and the wild 

becomes especially important in the rehabilitation and eventual release of manatees. 

Releasing manatees near where they were captured may be beneficial because 

tradition is probably important in manatee survival [Bengtson, 1981]. Manatees may 

learn feeding and resting areas among other information from older conspecifics 

during development. Like elephants [McComb et al., 2001] and cetaceans [Wells 

et al., 1999], manatees may have population level, behavioral diversity related to 

cultural traditions. Associations between individuals beyond weaning may be vital in 

manatee society and enhance survivorship. Such information could be helpful for 

rehabilitation and conservation. To our knowledge, in the instances of simultaneous 

releases of manatees from captivity, associations established in captivity have not 

been maintained (at least five: female and a surrogate calf, two pairs of males, one 

female pair and one mixed sex pair; R. Bonde, Sirenia Project, personal 

communication). The sample size, however, is relatively small. Our data suggest 

that females do establish some particular association groups in captivity, but further 

study is needed to assess to what degree such associations are a result of captivity. In 

terms of captive manatee management, density did not seem to have any negative 

effects on manatee behavior and social aggregation of manatees seems to be a 

normal condition of captive living. 

CONCLUSIONS 

Captive female manatees at different facilities carried out regular non-aggressive 

contacts among conspecifics. Aggressive interactions were rare and not associated 

with feeding periods. The rates of non-aggressive contacts were density dependent

ut not random. Behaviors were not observed in the first 3 months of captivity nor 

were interactions with human handlers documented. Additional studies of captive 

and wild manatees are needed to understand association patterns and the role that 

relatedness and natal range might play in the level and types of interactions. 


We thank Walt Disney World The Living Seas at Epcot Center, Homosassa 

Springs Wildlife State Park, Lowry Park Zoo, Miami Seaquarium, Mote Marine 

Laboratory, Parker Aquarium in Bradenton and Sea World of Florida for granting 

permission to do this research. We also thank the following organizations for helping 

support this research: Georgia Southern University’s Academic Excellence Award, 

the Graduate Student Professional Development Fund at Georgia Southern 

University, and the Jane Smith Turner Foundation and the Eppley Foundation 

(awards to B.A.S.). This research was conducted with IACUC approval by Georgia 

Southern University and approval from each facility participating in the study. 

R. Bonde, J. Koelsch and Drs. R. Chandler, D. Gleason, and L. Leege provided 

valuable comments on the manuscript. R. Bonde has approved of the personal 

communication reference in the discussion. The research was conducted with the 

cooperation of the USGS Sirenia Project (MA791721-2) and we thank their 

personnel for cooperation in this study. 

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Community Structure, Population Control, and Competition 

Nelson G. Hairston; Frederick E. Smith; Lawrence B. Slobodkin 

The American Naturalist, Vol. 94, No. 879. (Nov. - Dec., 1960), pp. 421-425. 

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Tue Nov 6 13:08:48 2007

Vol. XCIV, No. 879 The American Naturalist November-December, 1960 

COMMUNITY STRUCTURE, POPULATION CONTROL, 

AND COMPETITION 

NELSON G. HAIRSTON, FREDERICK E. SMITH, 

AND LARIRENCE B. SLOBODKIN 

Department of Zoology, The University of Michigan, Ann Arbor, Michigan 

The methods whereby natural populations are limited in size have been 

debated with vigor during three decades, particularly during the last few 

years (see papers by Nicholson, Birch, Andrewartha, Milne, Reynoldson, 

and Hutchinson, and ensuing discussions in the Cold Spring Harbor Symposium, 

1957). Few ecologists will deny the importance of the subject, 

since the method of regulation of populations must be known before we can 

understand nature and predict its behavior-. Although discussion of the subject 

has usually been confined to single species populations, it is equally 

important in situations where two or more species are involved. 

The purpose of this note is to demonstrate a pattern of population control 

in many communities which derives easily from a series of general, widely 

accepted observations. The logic used is not easily refuted. Furthermore, 

the pattern reconciles conflicting interpretations by showing that populations 

in different trophic levels are expected to differ in their methods of 

control. 

Our first observation is that the accumulation of fossil fuels occurs at a 

rate that is negligible when compared with the rate of energy fixaeion 

through photosynthesis in the biosphere. Apparent exceptions to this observation, 

such as bogs and ponds, are successionai stages, in which the 

failure of decomposition hastens the termination of the stage. The rate of 

accumulation when compared with that of photosynthesis has also been 

shown to be negligible over geologic time (Hutchinson, 1948). 

If virtually all of the energy fixed in photosynthesis does indeed flow 

through he biosphere, it must follow that all organisms taken together are 

limited by the amount of energy fixed. In particular, the decomposers as a 

group must be food-limited, since by definition they comprise the trophic 

level which degrades organic debris. There is no a priori reason why predators, 

behavior, physiological changes induced by high densities, etc., could 

not limit decomposer populations. In fact, some decomposer populations 

may be limited in such ways. If so, however, others must consume the 

tt 

left-over" food, so that the group as a whole remains food limited; otherwise 

fossil fuel would accumulate rapidly. 

Any population which is not resource-limited must, of course, be limited 

to a level below that set by its resources. 

Our next three observations are interrelated. They apply primarily to terrestrial 

communities. The first of these is that cases of obvious depletion 

of green plants by herbivores are exceptions to the general picture, in which

422 THE AMERICAN NATURALIST 

the plants are abundant and largely intact. Moreover, cases of,obvious 

mass destruction by meteorological catastrophes are exceptional in most 

areas. Taken together, these two observations mean that producers are 

neither herbivore-limited nor catastrophe-limited, and must therefore be 

limited by their own exhaustion of a resource. In many areas, the limiting 

resource is obviously light, but in arid regions water may be the critical 

factor, and there are spectacular cases of limitation through the exhaustion 

of a critical mineral. The final observation in this group is that there are 

temporary exceptions to the general lack of depletion of green plants by 

herbivores. This occurs when herbivores are protected either by man or 

natural events, and it indicates that the herbivores are able to deplete the 

vegetation whenever they become numerous enough, as in the cases of the 

Kaibab deer herd, rodent plagues, and many insect outbreaks. It therefore 

follows that the usual condition is for populations of herbivores not to be 

limited by their food supply. 

The vagaries of weather have been suggested as an adequate method of 

control for herbivore populations. The best factual clues related to this 

argument are to be found in the analysis of the exceptional cases where 

terrestrial herbivores have become numerous enough to deplete the vegeta- 

tion. This often occurs with introduced rather than native species. It is 

most difficult to suppose that a species had been unable to adapt so as to 

escape control by the weather to which it was exposed, and at the same 

time by sheer chance to be able to escape this control from weather to 

which it had not been previously exposed. This assumption is especially 

difficult when mutual invasions by different herbivores between two coun- 

tries may in both cases result in pests. Even more difficult to accept, how- 

ever, is the implication regarding the native herbivores. The assumption 

that the hundreds or thousands of species native to a forest have failed to 

escape from control by the weather despite long exposure and much selec- 

tion, when an invader is able to defoliate without this past history, implies 

that "pre-adaptation" is more likely than ordinary adaptation. This we can- 

not accept. 

The remaining general method of herbivore control is predation (in its 

broadest sense, including parasitism, etc.). It is important to note that 

this hypothesis is not denied by the presence of introduced pests, since it 

is necessary only to suppose that either their natural predators have been 

left behind, or that while the herbivore is abIe to exist in the new climate, 

its enemies are not. There are, furthermore, numerous examples of the di- 

rect effect of predator removal. The history of the Kaibab deer is the best 

known example, although deer across the northern portions of the country 

are in repeated danger of winter starvation as a result of protection and 

predator removal. Several rodent plagues have been attributed to the local 

destruction of predators. More recently, the extensive spraying of forests 

to kill caterpillars has resulted in outbreaks of scale insects. The latter 

are protected from the spray, while their beetle predators and other insect 

enemies are not.

POPULATION CONTROL AND COMPETITION 

Thus, although rigorous proof that herbivores are generally controlled by 

predation is lacking, supporting evidence is available, and the alternate 

hypothesis of control by weather leads to false or untenable implications. 

The foregoing conclusion has an important implication in the mechanism 

of control of the predator populations. The predators and parasites, in con- 

trolling the populations of herbivores, must thereby limit their own re- 

sources, and as a group they must be food-limited. Although the populations 

of some carnivores are obviously limited by territoriality, this kind of in- 

ternal check cannot operate for all carnivores taken together. If it did, the 

herbivores would normally expand to the point of depletion of the vegeta- 

tion, as they do in the absence of their normal predators and parasites. 

There thus exists either direct proof or a great preponderance of factual 

evidence that in terrestrial communities decomposers, producers, and preda- 

tors, as whole trophic levels, are resource-limited in the classical density- 

dependent fashion. Each of these three can and does expand toward the 

limit of the appropriate resource. We may now examine the reasons why this 

is a frequent situation in nature. 

Whatever the resource for which a set of terrestrial plant species com- 

pete, the competition ultimately expresses itself as competition for space. 

A community in which this space is frequently emptied through depletion 

by herbivores would run the continual risk of replacement by another assemblage 

of species in which the herbivores are held down in numbers by 

predation below the level at which they damage the vegetation. That space 

once held by a group of terrestrial plant species is not readily given up is 

shown by the cases where relict stands exist under climates no longer suit- 

able for their return following deliberate or accidental destruction. Hence, 

the community in which herbivores are held down in numbers, and in which 

the producers are resource-limited will be the most persistent. The develop- 

ment of this pattern is less likely where high producer mortalities are in- 

evitable. In lakes, for example, algal populations are prone to crash whether 

grazed or not. In the same environment, grazing depfetion is much more 

common than in communities where the major producers are rooted plants. 

A second general conclusion follows from the resource limitation of the 

species of three uophic levels. This conclusion is that if more than one 

species exists in one of these levels, they may avoid competition only if 

each species is limited by factors completely unutilized by any of the other 

species. It is a fact, of course, that many species occupy each level in 

most communities. It is also a fact that they are not sufficiently segregated 

in their needs to escape competition. Although isolated cases of nonoverlap 

have been described, this has never been observed for an entire 

assemblage. Therefore, interspecific competition for resources exists 

among producers, among carnivores, and arllong decomposers. 

It is satisfying to note the number of observations that fall into line with 

the foregoing deductions. Interspecific competition is a powerful selective 

force, and we should expect to find evidence of its operation. Moreover, 

the evidence should be most conclusive in trophic levels where it is neces- 

423

424 THE AMERICAN NATURALIST 

sarily present. Among decomposers we find the most obvious specific 

mechanisms for reducing populations of competitors. The abundance of 

antibiotic substances attests to the frequency with which these mechanisms 

have been developed in the trophic level in which interspecific competition 

is inevitable. The producer species are the next most likcly to reveal evi- 

dence of competition, and here we find such phenomena as crowding, shad- 

ing, and vegetational zonation. 

Among the carnivores, however, obvious adaptations for interspecific 

competition are less common. Active competition in the form of mutual 

habitat-exclusion has been noted in the cases of flatworms (Beauchamp and 

Ullyott, 1932) and salamanders (Hairston, 1951). The commonest situation 

takes the form of niche diversification as the result of interspecific compe- 

tition. This has been noted in birds (Lack, 1945; MacArthur, 1958), sala- 

manders (Hairston, 1949), and other groups of carnivores. Quite likely, 

host specificity in parasites and parasitoid insects is at least partly due 

to the influence of interspecific competition. 

Of equal significance is the frequent occurrence among herbivores of ap- 

parent exceptions to the influence of density-dependent factors. The grass- 

hoppers described by Birch (1957) and the thrips described by Davidson and 

Andrewartha (1948) are well known examples. Moreover, it is among herbi- 

vores that we find cited examples of coexistence without evidence of com- 

petition for resources, such as the leafhoppers reported by Ross (1957), and 

the psocids described by Broadhead (19>8). It should be pointed out that 

in these latter cases coexistence applies primarily to an identity of food 

and place, and other aspects of the niches of these organisms are not known 

to be identical. 

SUMMARY 

In summary, then, our general conclusions are: (1) Populations of producers, 

carnivores, and decomposers are limited by their respective resources 

in the classical density-dependent fashion. (2) Interspecific com- 

petition must necessarily exist among the members of each of these three 

trophic levels. (3) Herbivores are seldom food-limited, appear most often 

to be predator-limited, and therefore are not likely to compete for common 

resources. 


Andrewartha, H. G., 1957, The use of conceptual models in population ecol- 

ogy. Cold Spring Harbor Symp. Quant. Biol. 22: 219-232. 

Beauchamp, R. S. A., and P. Ullyott, 1937, Competitive relationships be- 

tween certain species of fresh-water triclads. J. Ecology 20: 200- 

208. 

Birch, L. C., 1957, The role of weather in determining the distribution and 

abundance of animals. Cold Spring Harbor Symp. Quant. Biol. 22: 

217-263. 

Broadhead, E., 1958, The psocid fauna of larch trees in northern England. 

J. Anim. Ecol. 27: 217-263.

POPULATION CONTROL AND COMPETITION 

425 

Davidson, J., and H. G. Andrewartha, 1948, The influence of rainfall, evaporation 

and atmospheric temperature on fluctuations in the size of a 

natural population of Thrzps zmagznis (Thysanoptera). j. him. 

Ecol. 17: 200-222. 

Hairston, N. G., 1949, The local distribution and ecology of the Plethodontid 

salamanders of the southern Appalachians. Ecol. hlonog. 

19: 47-73. 

1951, Interspecies competition and its probable influence upon the vertical 

distribution of Appalachian salamanders of the genus Plethodon. 

Ecology 32: 266-274. 

Hutchinson, G. E., 1948, Circular causal systems in ecology. Ann. M.Y. 

Acad. Sci. 50: 221-246. 

1957, Concluding remarks. Cold Spring Harbor Symp. Quant. Biol. 22: 

415-427. 

Lack, D., 1945, The ecology of closely related species with special reference 

to cormorant (Phalacrocorax carbo) and shag (P, arzstotelzs). 

J. Anim, Ecol. 14: 12-16. 

MacArthur, R. H., 1958, Population ecology of some warblers of northeastern 

coniferous forests. Ecology 39: 599-619. 

Milne, A., 1957, Theories of riatural control of insect populations. Cold 

Spring Harbor Symp. Quane. Biol. 22: 253-271. 

Nicholson, A. J., 1957, The self-adjustment of populations to change, Cold 

Spring Harbor Symp. Ouant. Biol. 22: 153-172. 

Reynoldson, T. B., 1957, Population fluctuations in Urceolarza rnzt~a (Peritricha) 

and Enchytraeus nlbzdus (Oligochaeta) and their bearing on 

regulation. Cold Spring Hat bor Symp. Quant. Biol. 22: 313-327. 

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Environmental Conservation 29 (2): 192–206 © 2002 Foundation for Environmental Conservation DOI:10.1017/S0376892902000127 

The future of seagrass meadows 

CARLOS M. DUARTE* 

IMEDEA (CSIC – UiB), C/ Miquel Marqués 21, 07190 Esporles, (Islas Baleares), Spain 

Date submitted: 29 May 2001 Date accepted: 15 February 2002 

SUMMARY 

Seagrasses cover about 0.1–0.2% of the global ocean, and 

develop highly productive ecosystems which fulfil a key 

role in the coastal ecosystem. Widespread seagrass loss 

results from direct human impacts, including mechanical 

damage (by dredging, fishing, and anchoring), 

eutrophication, aquaculture, siltation, effects of coastal 

constructions, and food web alterations; and indirect 

human impacts, including negative effects of climate 

change (erosion by rising sea level, increased storms, 

increased ultraviolet irradiance), as well as from natural 

causes, such as cyclones and floods. The present review 

summarizes such threats and trends and considers 

likely changes to the 2025 time horizon. Present losses 

are expected to accelerate, particularly in South-east 

Asia and the Caribbean, as human pressure on the 

coastal zone grows. Positive human effects include 

increased legislation to protect seagrass, increased 

protection of coastal ecosystems, and enhanced efforts 

to monitor and restore the marine ecosystem. However, 

these positive effects are unlikely to balance the negative 

impacts, which are expected to be particularly prominent 

in developing tropical regions, where the capacity 

to implement conservation policies is limited. 

Uncertainties as to the present loss rate, derived from 

the paucity of coherent monitoring programmes, and 

the present inability to formulate reliable predictions as 

to the future rate of loss, represent a major barrier to the 

formulation of global conservation policies. Three key 

actions are needed to ensure the effective conservation 

of seagrass ecosystems: (1) the development of a 

coherent worldwide monitoring network, (2) the development 

of quantitative models predicting the responses 

of seagrasses to disturbance, and (3) the education of the 

public on the functions of seagrass meadows and the 

impacts of human activity. 

Keywords: seagrass, conservation, status, perspectives, global 

change 

INTRODUCTION 

Seagrasses ecosystems are widely recognized as key ecosystems 

in the coastal zone, with important functions in the 

* Correspondence: Professor Carlos M. Duarte Fax: +34 971 

611761 e-mail: cduarte@uib.es 

marine ecosystem (Hemminga & Duarte 2000). Yet, there is 

growing evidence that seagrass meadows are presently experiencing 

worldwide decline primarily because of human 

disturbance, such as direct physical damage and deterioration 

of water quality (Short & Wyllie-Echeverria 1996; 

Hemminga & Duarte 2000). There is, therefore, concern that 

the functions seagrasses have performed in the marine 

ecosystem will be reduced or, in some places, lost altogether. 

While efforts are being made to conserve seagrass ecosystems, 

these are not guided by a clear forecast of the changes 

expected and the threats to come. There is, therefore, a need 

for a prospective examination of the expected status of 

seagrass ecosystems in the future, which would provide guidance 

for the implementation of effective conservation 

policies. However, such an exercise requires reliable forecasts 

as to the expected progression of the relevant properties 

affecting the future status of seagrass ecosystems. Over the 

time horizon of 2025, there are estimates of human population 

growth and global climate change (Foundation for 

Environmental Conservation 2001), and the goal of this 

review is to provide a forecast of the likely status of seagrass 

ecosystems over that period. However, as Noble laureate Nils 

Bohr once stated, ‘prediction is very difficult, particularly if 

it concerns the future’, particularly given the many gaps in 

the present knowledge on the status of seagrass ecosystems. 

Hence, the future scenario depicted here should be 

considered as an ecological forecast, rather than a prediction, 

driven by the projected trends in the environmental factors 

that shape the seagrass habitat. While such forecasts must 

necessarily entail considerable uncertainty, their formulation 

requires a revision of our understanding of the response of 

seagrass ecosystems to a changing ecosystem that may help 

identify the areas where more robust knowledge is most 

needed. Hence, independently of the reliability of the forecast 

issued here, this review will deliver an identification of 

the research required to increase the reliability of the predictions 

about the response of seagrass ecosystems to a changing 

environment. 

This review differs from previous attempts to forecast the 

future status of seagrass ecosystems in that these focused on 

their response to climate change (e.g. Brouns 1994; Beer & 

Koch 1996; Short & Neckles 1999), whereas the present exercise 

also considers the responses to the pressures derived 

from a growing human population. First, seagrasses and the 

functions they perform in the marine ecosystem are discussed 

together with their response to environmental forcing factors,

including direct and indirect human impacts. Future threats 

and the consequences of seagrass loss are used to identify 

long-term trends and the likely status of seagrass meadows in 

2025. This review concludes by discussing the managerial 

frameworks that must be implemented to anticipate the 

trends forecasted and optimize the conservation status of 

seagrass meadows by year 2025. Indeed, the forecast 

provided here reflects a projection from a ‘business as usual’ 

situation, whereas the adaptive nature of society to change, 

through the development of technologies and practices that 

minimize human impacts on the coastal environment, may 

render the forecasts issued here wrong. The required change 

of attitudes and technological developments may be, 

however, encouraged by the consideration of the future scenarios 

depicted here. 

SEAGRASSES AND THEIR FUNCTIONS IN THE 

ECOSYSTEM 

Seagrasses are angiosperms restricted to growth in marine 

environments. These plants evolved early in the history of 

angiosperms, but, unlike their land counterparts, showed a 

comparative evolutionary stasis (sensu Burt 2001), with their 

species richness being unlikely to exceed one hundred species 

at any one time through their evolutionary history (den 

Hartog 1970; Duarte 2001). All seagrass species are rhizomatous, 

clonal plants, occupying space through the reiteration 

of shoots, with their leaves and roots produced as a result of 

rhizome extension (Marbá & Duarte 1998; Hemminga & 

Duarte 2000). This asexual process appears to be the mechanism 

for seagrass proliferation, although some species such 

as Zostera marina (Olesen 1999) and Enhalus acoroides 

(Duarte et al. 1997a) reproduce a lot sexually, a mode of 

reproduction which is uncommon in some other species like 

Cymodocea serrulata and Posidonia oceanica (Hemminga & 

Duarte 2000). Seagrass species vary about 100-fold in growth 

rate and lifespan, which is inversely related to size (Duarte 

1991a; Marbá & Duarte 1998; Hemminga & Duarte 2000). 

Seagrasses require an underwater irradiance generally in 

excess of 11% of that incident in the water surface for 

growth, a requirement that typically sets their depth limit 

(Duarte 1991b). The upslope limit of seagrasses is imposed 

by their requirement for sufficient immersion in seawater or 

tolerable disturbance by waves and, in northern latitudes, ice 

scour (Hemminga & Duarte 2000). Most seagrass species 

grow subtidally, although species within some genera such as 

Zostera spp., Phyllospadix spp. and Halophila spp. can grow 

intertidally (den Hartog 1970; Hemminga & Duarte 2000). 

Seagrasses can grow in estuarine and brackish waters, but 

require salinity in excess of 5 ‰ to develop (Hemminga & 

Duarte 2000). Although some species such as Phyllospadix 

spp. grow on rocky shores, most grow on sediments, ranging 

from sandy to muddy, with organic contents

194 C.M. Duarte 

well as more recent massive losses such as that in Florida Bay 

(Robblee et al. 1991), which is one of the largest areas of 

seagrass ecosystem worldwide (Fourqurean & Robblee 1999). 

The causes and the possible role of human-derived impacts 

in such losses are still uncertain (cf. Hemming & Duarte 

2000). Strong disturbances, such as damage by hurricanes, 

can also lead to major seagrass losses (Preen et al. 1995; 

Poiner et al. 1989). Smaller-scale, more recurrent disturbances, 

such as that caused by the motion of sand waves in 

and out of seagrass patches (Marbá & Duarte 1995) and that 

caused by large predators, such as dugongs (Nakaoka & Aioi 

1999), represent the main factor structuring some seagrass 

landscapes, which are characteristically patchy (Marbá & 

Duarte 1995). In contrast, some seagrass species have been 

able to form long-lasting meadows, with meadows of the 

long-lived Posidonia oceanica dated to >4000 years old 

(Mateo et al. 1997), and single clones of Zostera marina dated, 

using molecular techniques at 3000 years old (Reusch et al. 

1999). 

In addition to natural variability of the seagrass habitat, 

human intervention is becoming a major source of change to 

seagrass ecosystems, whether by direct physical modification 

of the habitat by the growing human activity in the coastal 

zone (e.g. boating, fishing, construction; Walker et al. 1989), 

or through their impact on the quality of waters and sediments 

to support seagrass growth (Short & Wyllie- 

Echeverria 1996; Hemminga & Duarte 2000), as well as 

changes in the marine food webs linked to the seagrasses 

(Aragones & Marsh 2000; Jackson 2001; Jackson et al. 2001). 

Human impacts 

Humans impact seagrass ecosystems, both through direct 

proximal impacts, affecting seagrass meadows locally, and 

indirect impacts, which may affect seagrass meadows far 

away from the sources of the disturbance (Table 1). Proximal 

impacts include mechanical damage and damage created by 

the construction and maintenance of infrastructures in the 

coastal zone, as well as effects of eutrophication, siltation, 

coastal engineering and aquaculture (Table 1; Fig. 1). 

Indirect impacts include those from global anthropogenic 

changes (Fig. 2), such as global warming, sea-level rise, CO 2 

and ultraviolet (UV) increase, and anthropogenic impacts on 

marine biodiversity, such as the large-scale modification of 

the oceanic food web through fisheries ( Jackson 2001; 

Jackson et al. 2001). Indirect impacts are already becoming 

evident at present (e.g. Beer & Koch 1996). 

The most unambiguous source of human impact to 

seagrass ecosystems is physical disturbance. This susceptibility 

derives from multiple causes, all linked to increasing 

human usage of the coastal zone for transportation, recreation 

and food production. The coastal zone is becoming an 

important focus for services to society, since about 40% of 

the human population presently inhabit the coastal zone 

(Independent World Commission on the Oceans 1998). 

Direct habitat destruction by land reclamation and port 

construction is a major source of disturbance to seagrass 

meadows, due to dredging and landfill activities, as well as 

the reduction in water transparency associated with both 

these activities. The construction of new ports is associated 

with changes in sediment transport patterns, involving both 

increased erosion and sediment accumulation along the adjacent 

coast. These changes can exert significant damage on 

seagrass ecosystems kilometres away, which can be impacted 

by both erosion and burial associated with the changing sedimentary 

dynamics (e.g. Pascualini et al. 1999). The operation 

of the ports also entails substantial stress to the neighbouring 

seagrass meadows, due to reduced transparency and nutrient 

Table 1 Impacts of direct and indirect human forcing on seagrass ecosystems. 

Type Forcing Possible consequences Mechanisms 

Direct impacts Mechanical damage (e.g. trawling, Seagrass loss Mechanical removal and sediment 

dredging, push nets, anchoring, 

dynamite fishing) 

erosion 

Eutrophication Seagrass loss Deterioration of light and sediment conditions 

Salinity changes Seagrass loss, changes in community Osmotic shock 

structure 

Shoreline development Seagrass loss due to burial or erosion Seagrass uprooting 

Land reclamation Seagrass loss Seagrass burial and shading 

Aquaculture Seagrass loss Deterioration of light and sediment conditions 

Siltation Seagrass loss and changes in 

community structure 

Deterioration of light and sediment conditions 

Indirect impacts Seawater temperature rise Altered functions and distributions Increased respiration, growth and flowering, 

increased microbial metabolism 

Increased CO concentration 2 Increased depth limits and Increased photosynthesis, eventual decline of 

production calcifying organisms 

Sea level rise and shoreline erosion Seagrass loss Seagrass uprooting 

Increased wave action and storms Seagrass loss Seagrass uprooting 

Food web alterations Changes in community structure Changes in sediment conditions and 

disturbance regimes

Nutrient inputs 

+ 

+ 

+ 

Phytoplankton 

Epiphytic and 

opportunistic 

algae (+) 

- (shading) 

(Sediment anoxia) 

Grazers 

and contaminant inputs associated with ship traffic and 

servicing, as well as dredging activities associated with port 

and navigation-channel maintenance. Rapid increases in seabased 

transport, as well as recreational boating activities have 

led to a major increase in the number and size of ports worldwide 

(Independent World Commission on the Oceans 1998), 

with a parallel increase in the combined disturbance to 

seagrass meadows. Ship activity also causes disturbance to 

seagrass through anchoring damage, which can be rather 

extensive at popular mooring sites (Walker et al. 1989), as 

well as fisheries operation, particularly shallow trawling 

(Ramos-Esplá et al. 1993; Pascualini et al. 1999) and smallerscale 

activities linked to fisheries, such as clam digging and 

use of push nets over intertidal and shallow areas and, in 

extreme cases, dynamite fishing (Kirkman & Kirkman 2000). 

The exponential growth of aquaculture, the fastest-growing 

food production industry, has also led to impacts on 

seagrasses through shading and physical damage to the 

- 

- 

- 

Sediment resuspension 

- 

Figure 1 Effects of eutrophication derived from increased nutrient 

loading on seagrass ecosystems. Positive and negative indicate the 

sign of the effects. Chained positive and negative effects affect 

seagrasses negatively, whereas chained negative effects affect 

seagrasses positively. 

New habitat 

Sea level rise 

+ 

- Submarine 

erosion 

deep regression 

Increased CO2 

Photosynthesis+ - reduced calcification 

Seawater warming 

Reproduction 

habitat 

expansion + 

-Increased respiration 

Figure 2 Forecasted effects of climate change on seagrass 

ecosystems. All components include positive and negative effects. 

Future of seagrass meadows 195 

seagrass beds, as well as deterioration of water and sediment 

quality leading to seagrass loss (Delgado et al. 1997, 1999; 

Pergent et al. 1999; Cancemi et al. 2000). 

The coastal zone also supports increasing infrastructure, 

such as pipes and cables for transport of gas, water, energy 

and communications, deployment and maintenance of which 

also entail disturbance to adjacent seagrass meadows. The 

development of coastal tourism, the fastest-growing industry 

in the world, has also led to a major transformation of the 

coastal zone in areas with pleasant climates. For instance, 

about two-thirds of the Mediterranean coastline is urbanized 

at the present time, with this fraction exceeding 75% in the 

regions with the most developed tourism industry (UNEP 

[United Nations Environment Programme] 1989), with 

harbours and ports occupying 1250 km of the European 

Mediterranean coastline (European Environmental Agency 

1999). Urbanization of the coastline often involves destruction 

of dunes and sand deposits, promoting beach erosion, a 

major problem for beach tourism. Beach erosion, however, 

does not only affect the emerged beach, and is usually propagated 

to the submarine sand colonized by seagrass, 

eventually causing seagrass loss (Medina et al. 2001). 

Groynes constructed to prevent beach erosion often create 

extensive problems, by altering longshore sediment transport 

patterns, further impacting the seagrass ecosystem. 

Extraction of marine sand for beach replenishment is only 

economically feasible at the shallow depths inhabited by 

seagrasses, which are often impacted by these extraction 

activities (Medina et al. 2001). The threats coastal tourism 

poses to seagrasses are sometimes direct, as in some cases of 

purposeful removal of seagrass from beach areas to ‘improve’ 

beach conditions. Fortunately, there are indications that 

coastal tourism is attempting, at least in some areas, to 

embrace sustainable principles, including the maintenance of 

ecosystem services, such as those provided by seagrasses, and 

could well play a role in the future as an agent pressing for 

seagrass conservation. 

Widespread eutrophication of coastal waters (Vidal et al. 

1999) derived from the excessive nutrient input to the sea, is 

leading to global deterioration in the quality of coastal waters 

(Cloern 2001), which is identified as a major loss factor for 

seagrass meadows worldwide (Duarte 1995; Short & Wyllie- 

Echeverria 1996; Hemminga & Duarte 2000). Human 

activity presently dominates the global nitrogen cycle, with 

anthropogenic fixation of atmospheric nitrogen now 

exceeding natural sources (Vitousek et al. 1997), and anthropogenic 

nitrogen now dominating the reactive nitrogen pools 

in the atmosphere, and therefore rainwater, of industrialized 

and agricultural areas (Nixon et al. 1996). Hence, anthropogenic 

nitrogen dominates the nitrogen inputs to 

watersheds, with the human domination of nitrogen fluxes 

being reflected in a close relationship between nitrate export 

rate and human population in the world’s watersheds (Cole et 

al. 1993). Tertiary water-treatment plants only achieve a 

partial reduction in nitrogen inputs to the sea, for nitrogen 

inputs to the coastal zone are already dominated by direct


atmospheric inputs in heavily industrialized or agricultural 

areas (Paerl 1995). 

Although seagrass meadows are often nutrient limited 

(e.g. Duarte 1990), increased nutrient inputs can only be 

expected to enhance seagrass primary production at very 

moderate levels at best (Borum & Sand-Jensen 1996). 

Whereas seagrasses, through their low nutrient requirements 

for growth and their high capacity for internal nutrient recycling 

(Hemminga & Duarte 2000), are well fitted to cope with 

low nutrient availability, other primary producers, both 

micro- and macroalgal, are more efficient, because of greater 

affinity and higher uptake rates, in using excess nutrient 

inputs (Duarte 1995; Hein et al. 1995). Coastal eutrophication 

promotes phytoplankton biomass, which deteriorates the 

underwater light climate, and the stimulation of the growth 

of epiphytes and opportunistic macroalgae, which further 

shade and suffocate seagrasses (Duarte 1995; den Hartog 

1994; Hemminga & Duarte 2000; Hauxwell et al. 2001). The 

alleviation of nutrient limitation, together with the proliferation 

of phytoplankton and epiphyte biomass as a result of 

increased nutrient inputs imply that coastal eutrophication 

leads to a shift from nutrient limitation to light limitation of 

ecosystem production (Cloern 2001), enhanced through 

competitive interactions between different types of primary 

producers for light (Sand-Jensen & Borum 1991; Duarte 

1995). These effects result in seagrass loss, particularly in the 

deeper portions of the meadows (Sand-Jensen & Borum 

1991; Duarte 1995; Borum 1996). Heavy grazing, which can 

buffer the negative effects of eutrophication, may attenuate 

the effects of overgrowth by phytoplankton, epiphytes and 

macroalgae (cf. Heck et al. 2000; Hemminga & Duarte 2000). 

Eutrophication may, furthermore, have negative effects 

directly derived from the high resulting nutrient concentration, 

for high nitrate and ammonium concentrations may 

be toxic to seagrasses (e.g. Van Katwijk et al. 1997). 

Whereas research on the effects of eutrophication on 

seagrass meadows has focused on the effects of reduced light 

quality (Duarte 1995), the deterioration of the sediment 

conditions may also play a critical role in enhancing the loss 

of seagrasses. Seagrass sediments are typically rich in organic 

materials, due to the enhanced particle deposition and trapping 

under seagrass canopies (Terrados & Duarte 1999; 

Gacia & Duarte 2001) compared to adjacent bare sediments. 

Microbial processes are, therefore, stimulated in the seagrass 

rhizosphere (Hemminga & Duarte 2000), which, if sufficiently 

intense, lead to the depletion of oxygen and the 

development of bacterial communities with anaerobic metabolism, 

which release by-products, such as sulphide and 

methane, that may be toxic to seagrasses (e.g. Carlson et al. 

1994; Terrados et al. 1999). In order to avoid such toxicity 

effects, seagrasses pump a significant fraction of the photosynthetic 

oxygen produced to the roots, which release oxygen 

to maintain an oxidized microlayer at the root surface 

(Pedersen et al. 1998). However, eutrophication reduces 

seagrass primary production both through shading and 

seagrass loss, thereby reducing the oxygen seagrass roots may 

release. This allows anaerobic processes and the resulting 

metabolites to accumulate closer to the root surface, 

increasing the chances of toxic effects to seagrass. At the same 

time, the increased pelagic primary production leads to a 

greater input of organic matter to the sediments, enhancing 

microbial activity and the sediment oxygen deficit, which 

may increase the production of metabolites from anaerobic 

microbial metabolism. Both these processes result in the 

deterioration of the sediment environment to support 

seagrass growth, leading, through its interaction with the 

consequences of reduced light availability, to accelerated 

seagrass loss (Hemminga & Duarte 2000). Eutrophication 

effects on sediments may be more acute where sewage is the 

dominant source of nutrients, for this is discharged along 

with a high organic load, stimulating microbial activity 

( Jorgensen 1996). Aquaculture activities are becoming 

increasingly prominent in the shallow, sheltered coastal 

waters where seagrass meadows abound. Shading and high 

inputs of organic matter from fish cages have been shown to 

lead to seagrass decline below and around fish cages (Delgado 

et al. 1997, 1999; Pergent et al. 1999, Cancemi et al. 2000), 

through processes comparable to those of the eutrophication 

outlined above. 

Increased siltation of coastal waters is also a major human 

impact on seagrass ecosystems, which derives from changes 

in land use leading to increased erosion rates and silt export 

from watersheds. Siltation is a particularly acute problem in 

South-east Asian coastal waters, which receive the highest 

sediment delivery in the world as a result of high soil erosion 

rates derived from extensive deforestation and other changes 

in land use (Miliman & Meade 1993). Siltation severely 

impacts South-east Asian seagrass meadows through 

increased light attenuation (Bach et al. 1998) and burial 

(Duarte et al. 1997b), leading to seagrass loss and, where less 

intense siltation occurs, a decline in seagrass diversity, 

biomass and production (Terrados et al. 1998). 

Large-scale coastal engineering often alters circulation 

and salinity distributions, leading to seagrass loss. Hence, 

seagrass meadows, previously abundant in Dutch coastal 

areas, are now much reduced in surface, partially related to 

shifts of coastal waters from marine to brackish or freshwater 

regimes (e.g. Nienhuis et al. 1996). 

Pollution, other than that from nutrients and organic 

inputs, may be an additional source of human impacts on 

seagrass ecosystems, although, seagrass appears to be rather 

resistant to pollution by organic and heavy metal contaminants 

(Hemminga & Duarte 2000). These substances may 

possibly harm some components of the seagrass ecosystem, 

although such responses have not been examined to a significant 

extent. 

Human activity in the coastal zone has greatly impacted 

biodiversity at regional scales, whether by removing or 

adding species. These changes to marine biodiversity impact 

food webs and competitive interactions between organisms, 

directly and indirectly affecting seagrass beds ( Jackson 2001; 

Jackson et al. 2001). Hunting has led to a major decline in the

abundance of dugongs and sea turtles, which are agents of 

small-scale disturbance influencing the structure and 

dynamics of seagrass ecosystems (e.g. Aragones & Marsh 

2000). Indeed, there is concern that the depletion of dugong 

and sea turtle populations to levels where they can no longer 

exert an impact at the basin scale, may lead to major shifts in 

seagrass community structure, with the decline of the species 

dependent on recurrent small-scale disturbance, such as a 

Halophila spp. (Preen 1995; De Iongh 1996). These concerns 

stem from evidence from the fossil record that extinctions 

within the one diverse syrenid fauna were associated with 

extinctions of seagrass species (Domning 2001). It has been 

suggested recently that the decline in mega-grazers may have 

caused an increase in organic matter deposition in seagrass 

sediments, possibly explaining recent large-scale decline of 

seagrasses in systems such as Florida Bay, USA, and 

Moreton Bay, Australia ( Jackson 2001; Jackson et al. 2001). 

However, the evidence to suggest that the loss of megagrazers 

results or has resulted in a deterioration of habitat 

conditions to support seagrass is meagre at best ( Jackson 

2001; Jackson et al. 2001), so that these suggestions should be 

considered as interesting hypotheses pending confirmation, 

rather than established facts. In addition, high grazing 

pressure in the past, such as implied by this hypothesis, 

stresses the plants and ultimately results in a decline of leaf 

production, which has been ascribed to a depletion in the 

sediment nutrients available for plant growth (Zieman et al. 

1984). 

Global trade has increased the mobility of marine species, 

whether purposely, such as aquarium specimens, or inadvertently, 

such as organisms carried in ballast waters. The 

increased human-mediated transport of species between 

geographically distant locations has increased the incidence 

of invasive species. A case affecting Mediterranean, and 

probably soon Eastern Pacific seagrasses, is the invasion of 

the Mediterranean by the tropical algal species Caulerpa taxifolia, 

which first invaded the French Mediterranean in the 

early 1980s, apparently released from an aquarium, and has 

been reported to have expanded since along the French coast 

to reach the Italian and Spanish (Majorca Island) coasts 

(Meinesz & Hesse 1991). C. taxifolia grows rapidly and 

appears largely to colonize areas devoid of seagrasses, but has 

been reported to compete for space and resources with 

Posidonia oceanica off Monaco (Meinesz & Hesse 1991), being 

able to damage the Posidonia oceanica meadows, particularly 

when these are already under stress (de Villéle & Verlaque 

1995; Jaubert et al. 1999). The species has recently been 

reported on the Californian coast, raising concerns that it 

could also cause problems for the seagrass beds there. The 

Mediterranean Sea has also been invaded by Halophila stipulacea 

(Biliotti & Abdelahad 1990), across the Suez Canal, but 

no damage to the local seagrass meadows has been reported. 

Direct or indirect human intervention locally causes most 

impacts. However, at the regional or global scale, human 

activity also exerts an important impact on seagrass ecosystems. 

These effects are remarkably difficult to separate from 


responses to background natural changes in the highly 

dynamic coastal ecosystem. These impacts involve the effects 

of the realized and predicted climate change (Table 1), and 

result from changes in sea level, water temperature, UV irradiance, 

and CO 2 concentration. 

The mean global sea level has risen about 10–25 cm over 

the 20th century, which should have generated an average 

recession of the global coastline by 10–25 m (Bruun 1962), 

and, therefore, a large-scale erosion of shallow marine sediments. 

There is little doubt that such changes must have 

affected seagrasses, which are very sensitive to sediment 

erosion (e.g. Marbá & Duarte 1995), although there is little 

or no direct observational evidence for these changes. The 

effects on seagrasses of seawater warming of 0.3–0.6 o C over 

the 20th century (Mackenzie 1998) are generally less 

evident than those produced by sea-level changes. 

Temperature affects many processes that determine seagrass 

growth and reproduction, including photosynthesis, respiration, 

nutrient uptake, flowering and seed germination 

(Short & Neckles 1999). Although observations of increased 

flowering frequency of Posidonia oceanica in the 

Mediterranean have been tentatively linked to the seawater 

temperature increase (Francour et al. 1994), there is little 

evidence at present to suggest any impact of increased 

temperature as a result of global warming. The temperature 

increase may further impact seagrass ecosystems through 

effects on other components, such as an increased respiratory 

rate of the associated microbial communities. 

Stimulation of microbial respiration would further enhance 

the problems derived from high organic inputs to seagrass 

sediments (Terrados et al. 1999). Summer UV irradiance 

has greatly increased at high latitudes, and an increase in 

the north-temperate zone is also becoming evident. 

Increased UV levels are expected to impact negatively 

shallow, particularly intertidal, seagrasses (Dawson & 

Dennison 1996). The photosynthetic rates of light-saturated 

seagrass leaves are often limited by the availability of 

dissolved inorganic carbon, and, since the concentration of 

CO 2 in well-mixed, shallow coastal waters is in equilibrium 

with the atmosphere, the increase in atmospheric CO 2 

concentration by 25%, from 290 ppm to 360 ppm, over the 

20th century (Mackenzie 1998), may have led to an increase 

in light-saturated seagrass photosynthesis by as much as 

20% (recalculated from information in Brouns 1994 and 

Beer & Koch 1996). There is, however, little evidence that 

such physiological responses have led to observable changes 

in seagrass ecosystems at present. 

Natural versus anthropogenic influences 

Some cause-effect relationships between local seagrass loss 

and direct human activities, such as increased nutrient and 

organic loading, constructions on the coastline or boating 

activity, can be readily demonstrated. For instance, the 

loss of Zostera marina in a bay on the Atlantic coast of the 

USA has been shown to be closely correlated to housing


development (Short & Burdick 1996). However, the link 

between seagrass losses and indirect human influences is 

more elusive, since the coastal zone is a highly dynamic 

ecosystem, where many conditions vary simultaneously. 

Disturbances such as strong storms, hurricanes and 

typhoons, severely impact seagrass beds, to the point that 

they may be essential components of the dynamics of seagrass 

meadows (Duarte et al. 1997b). The difficulties of discriminating 

between sources of seagrass loss are best illustrated by 

example. A wasting disease decimated Zostera marina 

meadows in the 1930s on both sides of the Atlantic. The 

proximal cause for the loss seems to have been an infection by 

a fungus, Labyrinthula zosterae, although it may have affected 

Zostera marina meadows that were already stressed (den 

Hartog 1987). Hypotheses to account for this widespread loss 

also point to natural changes, such as unusual seawater 

warming, as possible triggers for the decline (den Hartog 

1987). Whether indirect human impacts on global processes 

may have played a role remains untested. The causes for the 

more recent loss of vast areas of seagrass, mostly Thalassia 

testudinum, in Florida Bay (Robblee et al. 1991) continue to be 

debated, and include, among others, increased anthropogenic 

nutrient loading, the effects of climatic changes involving a 

long time interval without hurricanes affecting the area also 

causing unusually low freshwater discharge (Fourqurean & 

Robblee 1999; Zieman et al. 1999), and the effects of the 

increased accumulation of detritus derived from loss of 

mega-grazers ( Jackson 2001; Jackson et al. 2001). Difficulties 

in experimenting at the appropriate scale of whole meadows 

to test these hypotheses have precluded elucidation of 

whether the decline was due to human or natural causes, or a 

combination of both. 

The challenge lies, therefore, in separating local loss 

processes, which would suggest a local, likely humanderived, 

source of disturbance, from indirect effects, both 

natural and anthropogenic, acting at a much larger spatial 

scale. The ability to reconstruct the growth history of the 

long-lived Mediterranean seagrass Posidonia oceanica allowed 

the examination of the coherence of past growth patterns 

along the Spanish Mediterranean coast (Marbá & Duarte 

1997). This examination revealed coherent growth patterns 

in populations 200–300 km along the coast, as well as a 

general tendency towards a decline in vertical growth, which 

indicates a tendency towards sediment erosion (Marbá & 

Duarte 1997). These trends were present even in meadows 

distant from any identifiable human disturbance, and were 

related to decadal changes in climate (Marbá & Duarte 

1997). 

Hence, despite clear signals of anthropogenic effects on 

climate components, the responses of the seagrass ecosystem 

are still unclear, probably due to the still modest size of the 

changes experienced but also, and perhaps to a greater 

extent, to the lack of adequate long-term monitoring systems 

allowing the detection of responses in the seagrass 

ecosystem. 

Future threats 

Future threats to seagrass meadows evolve from the development 

and expansion of those threats already operating. 

Increasing human use of the coastal zone predicates an uncertain 

future for seagrass meadows. Coastal populations, both 

resident and tourist, continue to grow rapidly, with those in 

the Mediterranean doubling at 30-year and 15-year intervals, 

respectively (UNEP 1989). Increased human activity in the 

coastal zone is associated with increased physical disturbance 

of seagrass meadows, through the construction of coastal 

infrastructures, and increased boating and shipping. 

Aquaculture is growing exponentially worldwide (World 

Resources Institute 1998), and parallel depletion of natural 

fish populations should lead to a maintenance, or even acceleration, 

of the expansion of coastal aquaculture, with 

associated potential impacts on seagrass meadows. The 

present trend towards increasing per caput water use, the 

expansion of waterborne sewage systems, and the growing 

use of fertilizers (World Resources Institute 1998) should 

lead to increasing nutrient and sewage discharge to coastal 

waters, and therefore a further expansion of the already widespread 

eutrophication problems. Although sewage treatment 

is also growing, the volume treated is growing much more 

slowly than that of total sewage and nutrient discharge 

(Nixon 1995). Similarly, there are no symptoms that land-use 

changes and deforestation are declining in the developing 

world, so that associated problems, such as siltation of coastal 

waters (see above), are likely to continue to increase in the 

future. 

The extent of indirect human impacts on seagrass ecosystems 

should also increase in the future, due to increasing 

emissions of CO 2 and other greenhouse gases. These activities 

should lead to an increase in the concentration of CO 2 in 

seawater, with a resulting decline in seawater pH (e.g. 

Kleypas et al. 1999), increased water temperature, and sealevel 

rise, together with an increased frequency of storms and 

wave action (Carter 1988; Bijlsma et al. 1996). Whereas an 

increase in the concentration of CO 2 in seawater may have 

positive effects on seagrass photosynthesis, possibly 

enhancing seagrass primary production worldwide, the 

decline in seawater pH should negatively affect calcifying 

organisms (Kleypas et al. 1999), including those present in 

seagrass meadows. The increasing sea level and storm activity 

(Carter 1988; Bijlsma et al. 1996) should be conducive to 

increasing coastal erosion and subsequent loss of seagrass 

meadows. Sea-level rise leads to a recession of the coastline, 

which can be roughly estimated as a horizontal recession rate 

of 100 times the consolidated sea-level rise (applying Bruun’s 

1962 rule of 1 m recession per cm increase in sea level). 

Sea-level rise creates, in the long term, new habitat for 

seagrass growth, which should lead to colonization of the 

inundated land, although the rates of sea-level rise are too 

slow to allow direct observation of the progression of the 

upslope limit of seagrass distribution; however, consideration 

of the sea-level rise of 10–25 cm over the 20th century

suggests the inundation (applying Bruun’s 1962 rule) of 

10–25 m of land, with an equivalent potential upslope 

progression of the vegetation. The downslope limit of the 

seagrass, which is generally set by the water transparency 

(Duarte 1991b), is likely to experience a similar upslope 

regression (i.e. 1–2.5 m horizontally yr -1 ): this assumes the 

transparency to remain constant, so that the bathymetric 

range occupied by seagrasses should not necessarily increase 

with the colonization of new inundated areas upslope. These 

processes introduce a dynamic perspective on the upslope 

and downslope distribution of seagrass meadows, which 

needs be considered in monitoring programmes, which may 

interpret the expected horizontal regression of 1–2.5 m per 

decade at the downslope limit as decline, when it may well 

represent a readjustment of the entire meadow to sea-level 

rise. 

Consequences of seagrass loss 

Seagrass loss leads to a loss of the associated functions and 

services in the coastal zone. The consequences of seagrass 

loss are well documented, through observations of the 

changes in the ecosystem upon large-scale seagrass losses 

(Hemminga & Duarte 2000). Seagrass loss involves a shift in 

the dominance of different primary producers in the coastal 

ecosystem, which can only partially compensate for the loss 

of primary production. For instance, the increased planktonic 

primary production with increasing nutrient inputs 

does not compensate for the lost seagrass production, so that 

there is no clear relationship between increased nutrient 

loading and ecosystem primary production (Borum 1996). 

The loss of the sediment protection offered by the seagrass 

canopy enhances sediment resuspension, leading to a further 

deterioration of light conditions for the remaining seagrass 

plants (Olesen 1996). The extent of resuspension can be so 

severe following large-scale losses, such as that experienced 

during the Zostera marina wasting disease, that the shoreline 

may be altered (Christiansen et al. 1981). The loss of 

seagrasses will also involve the loss of the oxygenation of sediment 

by seagrass roots, promoting anoxic conditions in the 

sediments. Seagrass loss has been shown to result in significant 

loss of coastal biodiversity, leading to a modification of 

food webs and loss of harvestable resources (Young 1978; 

Hemminga & Duarte 2000). In summary, seagrass loss represents 

a major loss of ecological as well as economic value to 

the coastal ecosystems, and is therefore, a major source of 

concern for coastal managers. 

IDENTIFIED LONG-TERM TRENDS 

Whereas records of change in seagrass ecosystems are few, 

the existing reports point to a tendency for widespread 

decline in both temperate and tropical ecosystems. There 

have been reports of large-scale seagrass decline at over 40 

locations (Hemminga & Duarte 2000), 70% of which were 


unambiguously attributable to human-induced disturbance 

(Short & Wyllie-Echeverria 1996), and reports of seagrass 

loss have multiplied by 10 in the last decade, which can only 

partially be accounted for by the increased effort in seagrass 

research and monitoring (Duarte 1999). Whereas some 

recovery has been demonstrated (e.g. Kendrick et al. 1999; 

Preen et al. 1995), most records indicate this to be either nonexistent 

or incomplete, so that the perceived long-term trend 

of seagrass points to a global decline, the extent of which is 

largely unknown. Short and Wyllie-Echevarria (1996) estimated, 

extrapolating from the reports available, the area of 

seagrass meadows globally lost during the 1990s at about 

12 000 km 2 , corresponding to the loss during this period alone 

of about 2% of the area originally covered by seagrasses. 

There is mounting evidence that Posidonia oceanica, which 

was estimated to cover about 50 000 km 2 in the 

Mediterranean (Bethoux & Copin-Montégut 1986), has been 

suffering widespread decline, at least in the north-west 

Mediterranean (Marbá et al. 1996; Pascualini et al. 1999; 

Boudouresque et al. 2000). An analysis of the age structure of 

Posidonia oceanica meadows in the Spanish Mediterranean 

showed a tendency for decline in 57% of the meadows examined 

(Marbá et al. 1996). Whereas some of those meadows 

still persist, some others have already been lost (C.M. 

Duarte, unpublished results 1999). The loss is not evenly 

distributed along the Spanish Mediterranean, but is concentrated 

in approximately 400 km of coastline, where only 

traces of some meadows recorded in the late 1980s remain 

and many have been lost already (C.M. Duarte, unpublished 

results 1999). Whereas local human impacts are often evident 

as causes for the decline of Posidonia oceanica meadows, this 

is not always the case, and, together with significant correlations 

between decadal growth and climate variation (Marbá & 

Duarte 1997), points to climate change effects and possibly 

indirect human impacts on the observed decline. For 

instance, the gradual decline in Zostera marina growing in the 

French coast noticed during the 1980s and 1990s was also 

related to elevated sea-surface temperatures observed since 

the 1980s (Glémarec 1997). These observations suggest that 

seagrass decline and, possibly expansion, may be triggered by 

large-scale climate change (Fig. 2). If so, rapidly changing 

climatic patterns may lead to major changes in seagrass cover 

in the future. 

Along the Danish coast, eelgrass has shown an important 

net reduction in cover over the 20th century, with important 

declines (die-off in the 1930s), rebounds and secondary 

declines, in between (P.B. Christensen, D. Krause-Jensen & 

J. S. Laursen, unpublished data 2000). These observations 

portray eelgrass ecosystems as highly dynamic at time scales 

longer than decadal. If undisturbed, seagrass communities 

can be rather stable, with records of continuous presence of 

specific seagrass beds for several millennia (e.g. Zostera 

marina, Reusch et al. 1999; Posidonia oceanica, Mateo et 

al.1997), and the extent and time scales of fluctuations in 

seagrass meadows may differ greatly across species and 

locations.


POTENTIAL STATUS IN 2025 

The prospective trends in both human forcing and climate 

change for the next 25 years suggest that the status of seagrass 

ecosystems may somewhat improve in some developed countries, 

because legislation is being rapidly implemented to 

protect seagrass meadows. The zero loss policy in the USA 

and Australia (Coles & Fortes 2001) means that any losses 

caused by direct human intervention should be compensated 

by the creation, generally by transplanting, of a similar extent 

of new seagrass meadow. Indeed, the general public is 

becoming increasingly aware of the existence of seagrasses 

and their important services and functions in coastal ecosystems, 

which can only raise the prospect of implementing 

conservation management policies further. Tourism, which 

has often acted in the past as a vector of degradation of coastal 

ecosystems, is shifting towards a more sustainable perspective 

and is becoming, in many countries, an agent promoting 

an improved quality of coastal ecosystems. 

Regrettably, legal protection against seagrass losses is only 

possible where disturbance derives from proximal causes, 

and difficulties of assigning responsibility for more diffuse 

impacts imply that these cannot be corrected through a 

posteriori legal actions. This includes eutrophication-derived 

seagrass loss, for nutrient inputs are mostly diffuse in nature. 

Nutrient reduction plans are being implemented in most 

developed countries, although these seem to have had little 

impact on the extent of coastal eutrophication, which is likely 

to expand in the future, although hopefully at a reduced rate, 

despite efforts to reduce nutrient inputs. Moreover, the 

trends outlined above only encompass a fraction of the 

world’s nations, where losses over the 20th century have 

already been large, and include only a modest fraction of the 

world’s coastline and seagrass beds. 

The bulk of the extant seagrass meadows are found on the 

coastline of developing tropical countries, which are experiencing 

the greatest rate of environmental degradation at 

present, and will continue to do so in the future. The impacts 

on seagrass meadows there will derive from land-use changes, 

particularly deforestation, and the associated siltation of 

coastal waters and growing nutrient and sewage inputs, as 

populations, fertilizer use and sewage implementation 

expand, and the impacts of the rapidly-growing aquaculture 

operations arise. What the loss will be by the year 2025 

remains uncertain, since the total extent of these impacts is as 

yet unknown. However, the geographic extent of these major 

impacts can be readily delimited to the developing world, 

particularly affecting seagrass meadows in South-east Asia, 

East Africa, and, to a lesser extent, the Caribbean. The 

coastal areas of other developing regions, such as South 

America and West Africa, support seagrass meadows that are 

much more limited in extent, so that the local impacts will 

affect smaller areas. 

Oceania is the only region with a major seagrass belt where 

losses are expected to be relatively small, due to the enforcement 

of zero seagrass loss policies and the small population 

(29.5 million) relative to the region’s coastline (30 663 km, i.e. 

968 humans km -1 ) compared at the other extreme to Asia 

(14 197 humans km -1 ; World Resources Institute 1998). Even 

so, the coastal zone near Australian cities has already experienced 

a significant loss (e.g. Cambridge & McComb 1984; 

Clarke & Kirkman 1989), so that seagrasses are considered 

amongst the most stressed of Australian ecosystems 

(Kirkman 1992; Kirkman & Kirkman 2000). 

Seagrass meadows in both developed and developing 

regions will be affected by changes in global processes. The 

predicted sea-level rise of about 0.5 cm yr -1 (Mackenzie 1998) 

implies a further average regression of the global coastline by 

12 m by the year 2025 and therefore important submarine 

erosion, which should impact seagrass meadows globally. 

Quantitative models relating coastline regression to submarine 

erosion and seagrass loss are, however, lacking, so that 

sensible predictions cannot be formulated. The sea-level rise 

may be faster than anticipated due to fast ice melt in polar 

regions, land subsidence, and the release of the fresh water 

retained in reservoirs reaching the end of their operative 

lives. Reservoirs presently hold an amount of water equivalent 

to 7 cm of sea-level rise (Carter 1988), and most of them 

will have exceeded their operative lives by the year 2025. 

This effect may be compensated by construction of new 

reservoirs. Submarine erosion may proceed further than 

expected because of the predicted increased frequency of 

storms and wave energy in the coastal zone with climate 

change (Carter 1988; Bijlsma et al. 1996). For similar reasons 

the consequences of the predicted increase of 0.5 o C in global 

temperature by the year 2025 (Mackenzie 1998) cannot be 

quantitatively formulated, although they are likely to be 

minor compared to other sources of change. Based on the 

calculations in Brouns (1994) and Beer and Koch (1996) the 

elevation of CO 2 concentration to almost 400 ppm by the year 

2025 may further stimulate seagrass photosynthesis by 

10–20%. In addition, Zimmerman et al. (1997) calculated 

that this increased photosynthesis may increase the depth 

limit of seagrasses, which may lead to an expansion in 

seagrass cover. 

The limitations of knowledge are evident from the fact 

that only qualitative predictions on the status of seagrass 

ecosystems by year 2025 are possible, because of (1) undefined 

rates of change in most relevant forcing factors, (2) lack 

of quantitative dose-response models that predict seagrass 

response to changes in environmental factors, and (3) absence 

of a reliable knowledge of the present extent of seagrass 

ecosystems. Even for responses where quantitative predictions 

may be formulated, such as the response of seagrass 

photosynthesis to increasing CO 2 concentrations, the forecasts 

are suspect, for they assume everything else to be held 

constant. The predictions therefore lose reliability when the 

plants respond in an integrative manner to multiple simultaneous 

changes (Chapin et al. 1987), and when these 

responses may be affected by responses of other components 

of the complex communities that comprise the seagrass 

ecosystem. For instance, the positive effect of increased CO 2

concentrations on seagrasses predicted from photosynthetic 

rates may be obscured by similar responses by the epiphytes, 

buffering the seagrass response due to shading. The 

predicted increase in water temperature may enhance 

community respiration, resulting in CO 2 concentrations 

higher than predicted if in equilibrium with the atmosphere 

in some ecosystems. However, enhanced seagrass respiration 

may also partially offset the possible increased photosynthetic 

gains. One of the major effects of climate change on terrestrial 

vegetation is the shift in vegetation ranges with global 

warming. A shift in the range of seagrass species, involving a 

displacement of subtropical and tropical species towards 

higher latitudes, similarly may be expected. This shift should 

not affect a poleward extension of the range of temperate 

species, for there is no evidence for temperature-dependence 

of the latitudinal limit of seagrasses (Hemminga & Duarte 

2000; Duarte et al. 2002). In contrast to terrestrial vegetation, 

quantitative predictions on the possible shifts in seagrass 

ranges with global warming are, however, not possible at the 

moment, since these would be dependent on changes in the 

oceanic currents and fronts that are themselves difficult to 

forecast. The response of seagrass ecosystems to climate 

change integrate partial responses at a number of levels, from 

physiological to organismal and ecosystem levels, which often 

act in opposite directions and interact with one another. The 

complex nature of the responses renders our capacity to reliably 

predict the response of seagrass ecosystems to climate 

change weak. 

Provided the recent trends and anticipated threats identified, 

it is clear that the most likely scenario is one of major 

loss of seagrass ecosystems, although quantitative forecasts 

cannot be issued. In a scenario of present and future loss of 

seagrass ecosystems, the question of the reversibility of 

decline becomes critical, particularly because loss and 

recovery of seagrass may be also associated with loss and 

recovery of important associated fauna and resources. The 

partial recovery of North Atlantic eelgrass populations 

affected by the wasting disease within a couple of decades 

(Short & Wyllie-Echeverria 1996) shows that recovery from 

certain impacts may be possible. However, this is only so 

provided that suitable conditions to support seagrass growth 

are re-established. Yet, the forcing factors identified above as 

likely to cause seagrass decline by year 2025 are forecasted to 

increase even further beyond that date so that global-scale 

seagrass recovery may not even occur within the present 

century. Whereas recovery is possible for species with fast 

growth and/or sexual output, such as Halophila spp. and 

Enhalus acoroides (Hemminga & Duarte 2000), recovery is 

slow in slow-growing species relying largely on clonal expansion, 

like the Mediterranean Posidonia oceanica, where 

colonization is thought to take place over several centuries 

(Duarte 1995). In such species, present and future loss will 

therefore affect many generations to come. Recovery may 

involve a shift in species composition, towards either fastgrowing, 

pioneer species, such as Halophila and Halodule 

spp. (Marbá & Duarte 1998), and/or species with high repro- 


ductive outputs, like Enhalus acoroides in the Indo-Pacific 

region (Duarte et al. 1997a). 

CONCLUSIONS AND MANAGEMENT 

Provided the largely qualitative nature of the possible predictions, 

the future of seagrass ecosystems remains uncertain. 

However, since their present status is already plagued with 

problems, and the future global environmental scenario is 

one of progressive change, the most likely prospect is a 

mounting global seagrass decline throughout the 21st 

century. The main threats to seagrass ecosystems on a large 

scale will continue to derive from human activity, both 

through direct disruption of the coastal zone, changes in land 

use and inputs of silt, nutrients and sewage to the coastal 

zone, as well as diffuse effects of human activity on climate 

(Figs. 1 and 2). Sea-level rise, in particular, is projected to be, 

and may already be (e.g. Marbá & Duarte 1997), a major 

cause of seagrass decline (Hemminga & Duarte 2000). 

Despite this alarm, knowledge of seagrass ecosystems is 

still insufficient to even document their possible present and 

likely future decline. The 600 000 km2 area global cover of 

seagrasses (Charpy-Roubaud & Sournia 1990) is only a best 

guess, derived from the application of a few rules of thumb, 

in contrast with the relatively adequate knowledge on the area 

cover of other key marine ecosystems that can be observed 

more easily from space (e.g. mangroves, coral reefs). 

Knowledge of the present area seagrasses cover globally is 

uncertain, and the situation is probably not much better for 

the bulk of the individual nations with an extended coastline. 

These uncertainties preclude any reliable quantitative forecast 

of future seagrass cover, and only qualitative forecasts 

can be formulated based on established trends and expected 

changes, supported by anecdotal evidence and opportunistic 

observations. 

Remote sensing techniques using optical or acoustic 

methods allow the monitoring of the surface seagrasses 

occupy, allowing the detection of seagrass regression or 

expansion (Kendrick et al. 1999; McKenzie et al. 2001) but 

cannot resolve changes in the internal density of the vegetated 

area. There is therefore a need to improve on the 

capacity to monitor seagrass remotely, such as improvements 

in acoustic techniques and use of hyperespectral imagerybased 

tools to discriminate between seagrass and other 

vegetated sediments. Monitoring programmes, typically 

based on the assessment of cover and shoot density along 

transects and quadrats, generally have an associated error 

greater than 30% about the mean (Heidelbaugh & Nelson 

1996), making it difficult to reliably detect changes; a reliable 

assessment of decline may only be possible for losses already 

amounting to as much as 50–80%. The low power of monitoring 

techniques implies that most monitoring programmes 

can only detect a reliable tendency towards seagrass loss 

when the seagrass meadows monitored have already experienced 

substantial damage. There is, therefore, an urgent need 

to design more effective monitoring approaches, capable of


detecting losses of 10% or less, as well as to develop early 

warning indicators of decline. Repeated census of marked 

shoots in plots may allow such precision for some seagrass 

species (e.g. Short & Duarte 2001). Use of reconstruction 

techniques to assess past seagrass demography (cf. Duarte et 

al. 1994) in monitoring programmes has allowed assessment 

of local tendencies for decline or expansion and the examination 

of the overall demographic balance of very large 

seagrass ecosystems (Peterson & Fourqurean 2001). Yet, 

even an optimistic analysis clearly indicates that monitoring 

efforts cannot possibly encompass but a minimum (< 0.01%) 

fraction of the world’s seagrass extent, although the 

implementation of seagrass monitoring programmes has 

increased over the past decades. The information derived 

from individual monitoring efforts could, however, be used 

to derive knowledge of trends at larger spatial scales than that 

encompassed by the individual monitoring efforts if these 

were networked into a coherent programme. The implementation 

of coordinated monitoring networks at the national, 

regional and global scales would prove instrumental to diagnosis 

of the large-scale status and trends of seagrass 

ecosystems. 

Management practices to address problems affecting 

seagrass ecosystems once detected are also insufficiently 

developed, for management intervention often fails to revert 

an ongoing seagrass decline (e.g. Delgado et al. 1999). The 

easiest impacts to regulate are those pertaining to direct 

mechanical effects on seagrass ecosystems, as well as some 

improvement of seagrass health following regulation of 

anchoring in recreational areas (e.g. Cabrera National Park, 

Spain; N. Marbá, C.M. Duarte, M. Holmer, R. Martínez, G. 

Basterretxea, A. Orfila, A. Jordi & J. Tintoré, personal 

communication 2002). Impacts related to changes in water 

quality are, however, more difficult to alleviate, although 

some successes have been reported, such as the reversal of 

seagrass losses following wastewater treatment on the French 

Society 

- Improved education 

- Improved awareness 

Managerial 

- Monitoring programmes 

- Accurate maps 

- Impact prevention 

- Precautionary principle 

- Networking 

- Restoration 

- Legislation 

Mediterranean coast (Pergent-Martini & Pascualini 2000). 

Empirical (e.g. Duarte 1991b) aswell as mechanistic (e.g. 

Gallegos 1994) models relating water quality to seagrass cover 

have been developed, which can be used to build scenarios of 

the effectiveness of different management strategies to 

improve water quality, and have also led to the development 

of metrics based on seagrass performance to assess water 

quality (Dennison et al. 1993). Direct management intervention 

in the proximal, in addition to the ultimate, causes of 

seagrass decline may be possible, such as intervention on 

sediment processes. For instance, iron additions to carbonate 

sediments may help prevent oxygen consumption by 

sulphide oxidation, possibly alleviating seagrass stress from 

anoxic sediments with high sulphide concentrations (cf. 

Hemminga & Duarte 2000; Chambers et al. 2001). Such 

direct intervention practices, however, must be based on 

robust knowledge of the proximal causes of seagrass decline, 

which requires further research emphasizing experimental 

tests of mechanisms and predictive models. 

Transplanting techniques to restore seagrasses have had 

mixed success (Fonseca 1992; Kirkman 1992), however, 

seagrass transplantation is too costly to be implemented at a 

large scale, which is a particularly critical drawback provided 

the fact that the most important losses are expected in developing 

countries. Hence, even though nationwide mangrove 

afforestation programmes have been implemented in some 

developing countries such as Thailand (Aksornkoae 1993), 

similar initiatives for seagrass meadows are as yet not feasible. 

In addition, seagrass transplantation programmes often 

require damage to a donor population, thereby reducing the 

value of transplantation as a management option. 

The threats and stresses to seagrass ecosystems are so 

diverse that management practices are unlikely to be effective 

unless accompanied by changing public attitudes and awareness 

(Fig. 3). Hence, the mid- to long-term conservation of 

seagrass ecosystems must be based on an adequate education 

Improving seagrass ecosystems 

Scientific 

- Increased knowledge 

- Improved predictive 

capacity 

- Interdisciplinary 

approaches 

- Improved monitoring 

technologies 

- Efficient restoration and 

intervention techniques 

Figure 3 Cooperative elements required to prevent present trend towards seagrass decline and efficiently conserve seagrass ecosystems.

of the public as to the nature of seagrasses, the functions they 

perform in nature, and the services these functions provide to 

society, and on the formulation and dissemination of best 

management practices to conserve seagrass ecosystems, all of 

this based on solid, interdisciplinary understanding of 

seagrass ecology and how to manage the health of seagrass 

ecosystems (Fig. 3). Education campaigns must, therefore, 

occupy a prominent place on the agenda for the conservation 

of seagrass ecosystems (Kirkman & Kirkman 2000), mobilizing 

seagrass scientists, managers and environmental 

educators to convey effectively the importance of seagrass 

ecosystems and the threats to them. Public awareness alone 

cannot be effective unless accompanied by sufficient understanding 

of the causes of stress to seagrass, and how these are 

integrated at the different levels, from physiological to demographic 

and landscape scales, to yield responses to possible 

intervention alternatives. In addition, our capacity to predict 

seagrass recovery from stress must be developed in order to 

allow reliable forecasts to be issued. The future of seagrass 

ecosystems will be largely dictated, therefore, by the social 

and scientific responses to the challenges ahead. 

ACKNOWLEDGEMENTS 

The writing of this paper was supported by the European 

Commission Managing and Monitoring of Seagrass Beds 

project (contract # EVK3-CT-2000-00044). I thank G. 

Kendrick and G. Harris for valuable discussion, J. Borum, 

D.I. Walker, J. Fourqurean and N.V.C. Polunin for valuable 

revisions. 

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OUTLOOK ON EVOLUTION AND SOCIETY 

doi:10.1111/j.1558-5646.2009.00911.x 

IS THE AGE OF THE EARTH ONE OF OUR 

“SOREST TROUBLES?” STUDENTS’ 

PERCEPTIONS ABOUT DEEP TIME AFFECT 

THEIR ACCEPTANCE OF EVOLUTIONARY 

THEORY 

Sehoya Cotner, 1,2 D. Christopher Brooks, 3 and Randy Moore 1 

1 Biology Program, University of Minnesota, Minneapolis, Minnesota 55455 

2 E-mail: harri054@umn.edu 

3 Office of Information Technology, University of Minnesota, Minneapolis, Minnesota 55455 

Received July 20, 2009 

Accepted November 10, 2009 

KEY WORDS: Age of the Earth, evolution education, science education. 

When Charles Darwin was developing his ideas for On the Origin 

of Species, the most widely accepted estimates of Earth’s 

age were those of William Thomson (later Lord Kelvin). Kelvin 

used calculations involving thermodynamics to argue that Earth is 

only 20–100 million years old—an age far too brief to accommodate 

evolution by natural selection. Darwin referred to Thomson’s 

claim as one of his “sorest troubles,” for Darwin understood that 

the history of life on Earth ultimately relies on geology. Darwin 

suspected that Earth was much older than Thomson claimed, but 

Thomson’s enormous stature as a scientist obliged Darwin to reconcile 

his claims with Kelvin’s data. To accommodate Kelvin’s 

timeline, Darwin proposed pangenesis as an explanation of inheritance 

(i.e., every sperm and egg contained “gemmules thrown off 

from each different unit throughout the body”). Darwin’s explanation 

sped evolution while avoiding Lamarck’s quasi-spiritual 

sources of acquired traits. However, Darwin’s explanation of inheritance 

was wrong (see discussion in Moore et al. 2009a). 

The age of Earth remains a divisive topic in the modern 

evolution–creationism controversy. Whereas mainstream science 

has long acknowledged that Earth is approximately 4.5 billion 

years old, a vocal group of citizens and religious activists con- 

858 

tinue to insist that Earth is less than 10,000 years old. Although 

most geocentrists and flat-Earth advocates have capitulated to 

scientific evidence, young-Earth creationists continue to reject 

scientific evidence in favor of religious dictum to claim that Earth 

is less than 10,000 years old. These antiscience claims have been 

surprisingly popular with the public. For example, a Gallup Poll 

in early 2009 reported that “On Darwin’s [200th] Birthday, Only 

4 in 10 Believe in Evolution” (Newport 2009), and Berkman et al. 

(2008) noted that “16% [of biology teachers] believed that human 

beings were created by God in their present form at one time 

within the last 10,000 years.” In another study, 12.5% of students 

were young-Earth creationists (Rutledge and Warden 2000), as are 

10%–14% of biology majors (Moore and Cotner 2009). Answers 

in Genesis’ (AiG) Creation Museum, along with the $27 million in 

donations required to build it, attest to the appeal of young-Earth 

creationism. Indeed, AiG’s income for 2005 exceeded $13 million, 

and that of the Institute for Creation Research (ICR, another 

religious organization based on young-Earth creationism) exceeded 

$7 million. For comparison, the 2005 income of National 

Center for Science Education—the nation’s leading organization 

that defends the teaching of evolution in public schools—was 

C○ 2010 The Author(s). Journal compilation C○ 2010 The Society for the Study of Evolution. 

Evolution 64-3: 858–864

$1.2 million (Moore et al. 2009a). Clearly, Earth’s age remains 

one of the “sorest troubles” for many people today, just as it did 

for Darwin. 

In this study, we examined how college students’ selfdescribed 

religious and political views influence their beliefs 

about Earth’s age and how this may affect their knowledge and 

acceptance of evolution. To our knowledge, this is the first study 

to examine these factors in college students. 

Methods 

POPULATION AND SURVEY INSTRUMENT 

In 2009, we electronically surveyed 400 students enrolled in several 

sections of a nonmajors introductory biology course at the 

University of Minnesota. Because the course is one of a few options 

required of all undergraduates at the University, we assumed 

the survey population is representative of all students (politically, 

religiously, and demographically), except for those enrolled in the 

College of Biological Sciences. The optional survey, which was 

completed before the start of classes, consisted of the 20-item 

Measure of Acceptance of the Theory of Evolution (MATE) developed 

and validated by Rutledge and Sadler (2007), our own 10item 

Knowledge of Evolution Exam (KEE; Moore et al. 2009a), 

and several items intended to gauge students’ religious and political 

preferences. The MATE consists of statements such as “the age 

of the Earth is less than 20,000 years” and “humans are the product 

of evolutionary processes,” to which students noted their level of 

agreement on a five-point Likert scale (from “strongly agree” to 

“strongly disagree”). The KEE questions were modified from an 

internal exam database, were authentic to the nonmajors’ test experience, 

and were designed to evaluate students’ understanding 

of basic tenets of evolutionary theory—for example, how fitness 

is measured, natural selection as a mechanism for evolutionary 

change, etc. (Appendix I). None of the KEE items specifically addresses 

the age of the Earth or evolutionary time. We also asked 

students whether they were politically liberal, conservative, or 

middle-of-the-road, and whether they were not religious (atheist 

or agnostic), or, if religious, were they progressive/liberal, orthodox, 

or middle-of-the-road. Students could ignore questions, and 

their responses had no impact on students’ grades. Response rate 

varied by survey item, with as many as 195 students (almost 50% 

of the targeted group) completing the KEE, and as few as 124 responding 

to some of the MATE items. The survey and subsequent 

data collection were approved by the University of Minnesota’s 

Institutional Review Board. 

DATA ANALYSIS 

We extracted six variables from the survey to explore the factors 

that contribute to holding young-Earth and old-Earth beliefs about 

the origins of the world, on the one hand, and the relation of those 


beliefs to students’ knowledge of evolution and their presidential 

vote. 

The first two variables are self-reported measures of religious 

and political beliefs. The variable measuring students’ religious 

views (MYRELVIEW) is based on the question, “In general, I 

would describe my religious views as conservative, middle-ofthe-road, 

liberal/progressive, or none of the above/I’m not religious.” 

Responses were coded on a four-point scale from conservative 

(1) to not religious (4). Similarly, students’ political views 

(MYPOLVIEW) were determined by the question, “In general, 

I would describe my political views as conservative, middle-ofthe-road, 

or liberal.” MYPOLVIEW consists of a three-point scale 

ranging from conservative (1) to liberal (3). 

We constructed the young-Earth and old-Earth variables from 

MATE items that represent perspectives aligning with those beliefs. 

For the young-Earth variable (YOUNGEARTH), we averaged 

responses to the following two items: “The age of the Earth 

is less than 20,000 years,” and “The theory of evolution cannot be 

correct because it disagrees with the Biblical account of creation.” 

The old-Earth variable (OLDEARTH) was constructed by averaging 

responses to how much students agreed or disagreed with the 

statements that “Organisms existing today are the result of evolutionary 

processes that have occurred over millions of years,” 

and “The age of the earth is at least 4 billion years.” Scales for 

YOUNGEARTH and OLDEARTH range from 1 (Strongly Disagree) 

to 4 (Strongly Agree). Factor analysis confirms that each 

pair of items load onto a single dimension representing young- 

Earth creationist and old-Earth evolutionist beliefs with rotated 

factor loadings of 0.6979 and 0.7787, respectively. 

Students’ recollections of their high school biology courses 

(HSBIO) were captured in responses to an item asking them to 

identify whether or not evolution or creationism was taught in 

their courses. For the purposes of our analysis, HSBIO is coded 

according the following scheme: included neither evolution nor 

creationism = 1; included creationism, but not evolution = 2; 

included both evolution and creationism = 3; and included evolution, 

but not creationism = 4. 

The variable measuring students’ level of evolutionary biology 

knowledge (EVOGRADE) is a summative index of the 

number of questions answered correctly about various facets of 

evolutionary theory. EVOGRADE ranges in value from zero to 10 

with each increment representing a correctly answered question. 

The 2008 presidential candidate supported by each student was 

collected via the self-reported, retrospective response to the statement, 

“In the past presidential election, I voted/would have voted 

for John McCain or Barack Obama.” For analytical purposes, we 

constructed the dichotomous variable VOTE in which support for 

John McCain = 0 and support for Barack Obama = 1. Students 

who voted for other candidates constituted a small minority and 

were excluded from analysis. 

EVOLUTION MARCH 2010 859


Figure 1. Structural equation model demonstrating the nature of the relationships among the variables identified in Table 1. Note that 

“+” and“−” refer to positive and negative relationships, respectively, and asterisks follow the code ∗P < 0.05, ∗∗P< 0.01, ∗∗∗P < 0.001. 

Although our initial goals included the construction of a 

structural equation model (SEM) that employed simultaneous 

equations, the nature of the data is prohibitive (none of our variables 

is either linear or continuous). Therefore, we employed 

several individual models, each of which is best suited to the 

particular dependent variable under consideration. We then developed 

a structural model that demonstrates the nature of the 

relationships between and among our variables (Fig. 1). With 

the exception of models with VOTE as the dependent variable, 

all models are ordered logistical regression. We employed 

logistic regression models when the dichotomous VOTE variable 

was dependent. A Monte Carlo simulation was used to 

transform the ordered logistical regression results into predicted 

probabilities. 

Summary statistics for the variables under consideration are 

reported in Table 1. 

Table 1. Summary statistics. 

Variable N Mean Std. Dev. Min. Max. 

Myrelview 180 2.8111 0.9501 1 4 

Mypolview 173 2.3468 0.7361 1 3 

Youngearth 124 1.4839 0.6806 1 4 

Oldearth 132 3.3674 0.6958 1 4 

Hsbio 194 3.3402 1.0270 1 4 

Evograde 195 5.3026 2.2328 0 10 

Vote 174 0.7816 0.4143 0 1 

860 EVOLUTION MARCH 2010 

Results 

The first set of relationships includes the exogenous variables 

related to students’ religious and political views. These variables 

mutually reinforce one another at statistically significant levels 

(P < 0.001). That is, the more liberal one’s political views, the 

more likely one is to be liberal, agnostic, or atheistic in their 

religious views and vice versa. 

Students’ religious views also served as significant predictors 

of their beliefs about the origins of the world, their knowledge 

of evolutionary theory, and for whom they cast their presidential 

votes. Specifically, the more conservative a student’s religious 

views, the greater the likelihood of endorsing young-Earth beliefs 

(P < 0.05) and the less likely they are to endorse old-Earth 

evolutionist beliefs (P < 0.01). Additionally, more liberal, agnostic, 

or atheistic religious students were significantly more likely 

(P < 0.05) to correctly answer knowledge-based questions about 

theories and facts related to evolution. Finally, students holding 

less conservative religious views were considerably more likely 

to have voted for or supported Barack Obama in the 2008 presidential 

election (P < 0.001). 

The political views held by students contribute significantly 

to their disposition toward evolutionary theory and to their choice 

of presidential candidate. Here, the more liberal a student’s political 

views, the more likely they are to hold old-Earth beliefs about 

the origins of the world (P < 0.05) and to have cast their vote 

for Obama (P < 0.001). However, although more liberal political 

views are negatively related to acceptance of young-Earth views

and positively related to knowledge of evolutionary theory, political 

views fail to predict significantly either of those variables. 

Turning to the intermediate variables measuring the impact 

of beliefs about the origins of life on Earth, we find mutually 

reinforced inverse relationships between young-Earth and old- 

Earth views that are highly significant (P < 0.001). Specifically, 

those who hold young-Earth views are significantly less likely to 

accept an old-Earth rooted in evolutionary theory and vice versa. 

We also find that holding old-Earth beliefs contributes significantly 

to the ability of students to comprehend complex theoretical 

and factual tenets of evolutionary theory (P < 0.05). 

Furthermore, acceptance of old-Earth beliefs also significantly 

increased the probability of voting for or supporting Obama. 

Conversely, holding young-Earth beliefs appears to impact 

negatively, but not significantly, one’s ability to grasp cognitively 

evolutionary theory. And while holding creationist beliefs did 

predict a greater likelihood of voting for John McCain, they did 

not do so in a statistically significant manner. 

Finally, in keeping with previous findings (Moore and Cotner 

2009), the content of students’ high school biology courses 

was a significant predictor of their acceptance of evolutionary theory. 

The content of students’ high school biology course affects 

knowledge of evolution as well: students whose high school biology 

course included only evolutionary theory had approximately 

a 70% chance of answering half of the questions or more correctly 

whereas those with courses teaching only creationism had an approximately 

50% chance of doing so (for discussion, see Moore 

et al. 2009b); those with neither evolution nor creationism had a 

42% chance of scoring 50% or above, suggesting that creationismonly 

education is comparable to no education at all with respect to 

evolutionary biology. In combination, students who recall being 

taught evolution only in high school, and who are religiously and 

politically liberal, were more likely to earn any score above 50% 

on the exam than were their counterparts with more conservative 

educational, religious, and political backgrounds. 

Discussion 

College students have a variety of religious and political views that 

have been shaped collectively by their families, their communities, 

and the institutions with which they have come into contact 

during the course of their lives. These deeply rooted views influence 

students’ receptiveness to theories about life’s origins. 

And because these beliefs about creationism and evolution are 

firmly grounded in, and are expressions of, their worldviews, as 

instructors we are naïve to assume that students in college biology 

courses are necessarily open to scientific inquiry. 

Although student views of evolution are subject to multiple 

influences, our data indicate that their views about Earth’s age 

are a strong predictor of several different factors. But is the age 


of Earth one of our “sorest troubles?” Our research and historical 

and contemporary literature suggest the following: 

(1) Deep time is conceptually difficult to grasp, for the general 

public, science educators, and students throughout the educational 

spectrum. 

Charles Darwin himself had a hard time grasping “deep 

time”—the geologic concept of time, requiring billions of years— 

but knew that it was essential for his proposed evolutionary mechanism. 

Darwin didn’t publish any estimates of Earth’s age, but in 

the first edition of On the Origin of Species he did estimate the 

time needed to erode the Weald (a region in south England stretching 

from Kent to Surrey), “say three hundred million years.” He 

then explained: “I have made these few remarks because it is 

highly important for us to gain some notion, however, imperfect, 

of the lapse of years. During each of these years, over the whole 

world, the land and the water has been peopled by hosts of living 

forms. What infinite number of generations, which the mind 

cannot grasp, must have succeeded each other in the long roll of 

years” (Darwin 1859). 

More recently, attention has focused on the inability of 

scientists (Brush 2001), science educators (Petcovic and Ruhf 

2008), college students (Catley and Novick 2009; Libarkin 2006; 

Truscott et al. 2006), and the general public (Hofstadter 1996) 

to comprehend time in billions of years. Our deficiencies involve 

concepts about both absolute time (time in years; Catley and 

Novick 2009) and relative time (events in an accurate sequence; 

Libarkin 2006). 

(2) Students’ inability to accept an old Earth is a barrier to 

evolution acceptance. 

Not only is an appreciation of deep time foundational to 

our full understanding of life’s origin and diversification (Catley 

and Novick 2009; Hillis 2007), it is a critical concept for understanding 

geology, physics, and astrophysics (see review in Trend 

2002). Creationists themselves acknowledge that “An old age for 

the Earth is the heart of evolution” (Henry 2003), and have, in 

recent years, focused their argument to undermine an ancient 

Earth (Humphreys 1999; Baumgardner 2003; Humphreys et al. 

2004; DeYoung et al. 2005). Investing energy in debunking an 

ancient Earth is only logical if in fact Earth’s age is key to the 

Darwinian revolution, and is, in the words of Ernst Mayr (1972), 

“the snowball that started the whole avalanche.” 

Furthermore, evolution instruction is often independent of 

attempts to teach about deep time (Libarkin et al. 2005), a practice 

that enables students to learn about evolution without fully 

realizing its value as foundational to modern science. For example, 

Libarkin et al. (2005) describe students who can cite Earth’s 

age correctly but fail to comprehend the span of time Earth was 

uninhabitable, or the types of primitive organisms that likely arose 

first. These disconnects may speak to a need to incorporate historical 

arguments (Jensen and Finley 1995) or, more generally, an 



emphasis on the nature of science (Lombrozo et al. 2008) into a 

more multidisciplinary strategy for teaching about evolution and 

the age of Earth. 

(3) Creationists’ explanations for life’s origin are easier to 

teach, learn and internalize than are scientific explanations that 

rely on an understanding of deep time. 

For evidence of creationism’s staying power, one can look to 

the recycled “argument for design” throughout history: In 45 BCE, 

Marcus Tullius Cicero invoked a sundial to claim evidence of a 

creator; in 1691, Anglican clergyman John Ray upgraded to a 

clock; and in 1802, William Paley’s treatise “Natural Theology” 

invoked a watch and its associated watchmaker (“every indication 

of contrivance, every manifestation of design, which existed in 

the watch, exists in the works of nature ...”). Technology–and 

the scientific advancements required to progress from sundials 

to watches—has changed, but the basic argument—evidence of 

design—remains unchanged (Moore et al. 2009a). 

Public-opinion polls provide more contemporary evidence 

of the power of creationists’ claims. In 1982, Philip Abelson 

wrote that scientific creationists “have no substantial body of 

experimental data to back their prejudices. Truth is not on their 

side. In the end, their activities must bring only harm to their 

cause.” At that time, 44% of the American public believed that 

living organisms were created in their present form within the 

last 10,000 years (Gallup 1982). After more than two decades of 

science education reform, that percentage remains unchanged. 

Whether we are constrained by teleology or intentionality 

(Sinatra et al. 2008), humans tend to believe in a universe designed 

for a purpose (Kelemen 2004; Evans 2001). This tendency 

lends a natural authority to supernatural explanations, which, in 

combination with a more intuitive model of Earth’s age (thousands, 

rather than billions, of years; see DeYoung et al. 2005), 

severely jeopardizes a realization of deep time. In asking our students 

to forsake the young, the intended, and the concrete for the 

old, the accidental, and the abstract, we may be fighting our own 

evolutionary history. 

(4) Teaching about time requires teaching for conceptual 

change. 

Learning about deep time is a conceptual change for most 

students, whereby instructors must realize the real barrier that 

Earth’s age presents to student understanding of evolution. In 

addition, and in accordance with studies of teaching for conceptual 

change (e.g., Sinatra et al. 2008), teachers may need to guide 

students to a realization that their understandings of Earth’s age, 

both absolute and relative, are faulty and in need of revision. 

Although several authors have suggested strategies for addressing 

relative time (e.g., James and Clark’s “ticking toilet paper roll” 

[2006]), input on conquering the absolute-time barrier is scarce. 

(5) Failure to accept an ancient Earth has real-world implications. 


We do not doubt that adherence to creationist explanations 

for natural phenomena has far-reaching significance. However, 

in this study, we specifically explored available information on 

voting activity in November 2008, and demonstrate a significant 

link between presidential candidate choice and Earth’s-age 

dimensions. This association is likely bolstered by contemporary 

partisan politics; for example, Republican party platforms 

in several states support some form of teaching creationism (as 

“Creation Science,” “Intelligent Design,” etc.) as a viable alternative 

theory to evolution by natural selection (e.g., Governor Sarah 

Palin’s Alaska: “We support giving Creation Science equal representation 

with other theories of the origin of life. If evolution is 

taught, it should be presented as only a theory”). 

The political motivation for embracing creationism is clear: 

Recent Gallup polls highlight the different levels of acceptance 

of evolution among Republicans, Democrats, and Independents 

(Newport 2008, 2009). In one poll, 60% of Republicans claim that 

humans were created in their present form by God within the last 

10,000 years, a belief shared by 40% of Independents and 38% of 

Democrats (Gallup 2008). Of those polled agreeing that humans 

evolved and God had no part, 4% are Republicans, 19% are Independents, 

and 17% are Democrats. These data are consistent with 

findings that Republicans are more likely to attend church regularly, 

and Americans who attend church weekly are highly likely 

to believe in creationist explanations for human origins (Newport 

2006, 2008). For example, of those who attend church weekly, 

70% believe that God created humans in their present form (a 

central tenet of young-Earth creationists, or YEC); of those who 

seldom or never attend church, 24% are YEC (Newport 2008). 

These data suggest that religiosity correlates with one’s tendency 

to vote Republican and one’s likelihood to doubt evolutionary 

interpretations of origins, specifically, as highlighted herein, 

an Earth that is 4–5 billion years old. We do not intend to claim that 

ignorance of science is restricted to Republicans, nor that there 

are no creationist Democrats; rather, Republicans frequently embrace 

creationism more explicitly than do their counterparts and 

have benefited in recent years by making creationism a campaign 

issue. 

Implications 

Our research suggests that students who are liberal, agnostic, 

or atheistic in their religious views, are politically liberal, were 

taught evolution in high school, and accept the science behind 

evolutionary theory are more likely to understand the theoretical 

concepts and empirical findings related to evolution than those 

who are more conservative politically and religiously, received 

either no evolution or a diluted form of evolution instruction in 

high school, and who do not accept an old Earth. However, our 

findings also reveal a possible exception to this latter formulation: 

holding young-Earth views may not significantly impede a

student’s ability to learn facts about evolutionary theory. Thus, 

although it is not the role of biology instructors to engage in 

political or religious proselytizing, there remains the possibility 

of changing what students know about evolution via academic 

instruction. 

A student’s vote is likely a proxy for religious views, and 

therefore the association between their voting and their acceptance 

of evolution appears robust and bears further investigation. 

Given that adherence to young-Earth beliefs requires a refutation 

not only of modern biology, but also geology, paleontology, 

and physics, such convictions may serve as a proxy for scientific 

ignorance in general. Consequently, a commitment to comprehensive 

conceptual-change instruction in Earth’s age, the scientific 

method, and evolutionary theory could have practical, real-world 

implications that include nothing less than who we elect for political 

office. 


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Associate Editor: T. Meagher 

Appendix I 

KNOWLEDGE OF EVOLUTION EXAM (KEE) 

(1) Which of the following support the theory of evolution? 

A. artificial selection (also known as selective breeding), an 

analogue of natural selection 

B. comparative biochemistry, where similarities and differences 

of DNA among species can be quantified 

C. vestigial structures that serve no apparent purpose 

D. comparative embryology, where the evolutionary history 

of similar structures can often be traced 



E. all of the above provide evidence to support the theory of 

evolution 

(2) Resistance to a wide variety of insecticides has recently 

evolved in many species of insects. Why? 

A. mutations are on the rise 

B. humans are altering the environments of these organisms, 

and the organisms are evolving by natural selection 

C. no new species are evolving, just resistant strains or varieties. 

This is not evolution by natural selection 

D. humans have better health practices, so these organisms 

are trying to keep up 

E. insects are smarter than humans 

(3) Which of the following is the most fit in an evolutionary sense? 

A. a lion who is successful at capturing prey but has no cubs 

B. a lion who has many cubs, eight of which live to adulthood 

C. a lion who overcomes a disease and lives to have three 

cubs 

D. a lion who cares for his cubs, two of whom live to adulthood 

E. a lion who has a harem of many lionesses and one cub 

(4) How might a biologist explain why a species of birds has 

evolved a larger beak size? 

A. large beak size occurred as a result of mutation in each 

member of the population 

B. the ancestors of this bird species encountered a tree with 

larger than average sized seeds. They needed to develop 

larger beaks to eat the larger seeds, and over time, they 

adapted to meet this need 

C. some members of the ancestral population had larger 

beaks than others. If larger beak size was advantageous, 

they would be more likely to survive and reproduce. As 

such, large beaked birds increased in frequency relative 

to small beaked birds 

D. the ancestors of this bird species encountered a tree with 

larger than average sized seeds. They discovered that by 

stretching their beaks, the beaks would get longer, and 

this increase was passed on to their offspring. Over time, 

the bird beaks became larger 

E. none of the above 

(5) Which of the following statements about natural selection is 

true? 

A. natural selection causes variation to arise within a population 

B. natural selection leads to increase likelihood of survival 

for certain individuals based on variation. The variation 

comes from outside the population 

C. all individuals within a population have an equal chance 

of survival and reproduction. Survival is based on choice 


D. natural selection results in those individuals within a population 

who are best-adapted surviving and producing 

more offspring 

E. natural selection leads to extinction 

(6) All organisms share the same genetic code. This commonality 

is evidence that 

A. evolution is occurring now 

B. convergent evolution has occurred 

C. evolution occurs gradually 

D. all organisms are descended from a common ancestor 

E. life began millions of years ago 

(7) Which of the following statements regarding evolution by 

natural selection is FALSE? 

A. natural selection acts on individuals 

B. natural selection is a random process 

C. very small selective advantages can produce large effects 

through time 

D. natural selection can result in the elimination of certain 

alleles from a population’s gene pool 

E. mutations are important as the ultimate source of genetic 

variability upon which natural selection can act 

(8) A change in the genetic makeup of a population of organisms 

through time is 

A. adaptive radiation 

B. biological evolution 

C. LaMarckian evolution 

D. natural selection 

E. genetic recombination 

(9) Which of the following is the ultimate source of new variation 

in natural populations? 

A. recombination 

B. mutation 

C. hybridization 

D. gene flow 

E. natural selection 

(10) Which of the following best describes the relationship between 

evolution and natural selection? 

A. natural selection is one mechanism that can result in the 

process of evolution 

B. natural selection produces small-scale changes in populations, 

whereas evolution produces large-scale ones 

C. natural selection is a random process whereas evolution 

proceeds toward a specific goal 

D. natural selection is differential survival of populations or 

groups, resulting in the evolution of individual organisms 

E. they are equivalent terms describing the same process

Conservation and 

Behaviour 

Richard Buchholz, Department of Biology, University of Mississippi, Mississippi, USA 

Patrick Yamnik, Department of Biology, University of Mississippi, Mississippi, USA 

Cassan N Pulaski, Department of Biology, University of Mississippi, Mississippi, USA 

Chelsea A Campbell, Department of Biology, University of Mississippi, Mississippi, USA 

Conservation behaviour is an area of conservation biology particularly suited to 

investigate problems of species endangerment associated with managing animals in 

fragmented habitats and isolated parks. It employs a theoretical framework that 

examines the mechanisms, development, function and phylogeny of behavioural 

variation in order to develop practical tools for preventing extinction. This framework 

can be used to attract animals to suitable habitat, restore migratory movements, 

identify individual reproductive strategies affecting conservation and focus protection 

on species most susceptible to extinction. The future success of conservation behaviour 

requires that behaviourists link individual variation in behaviour to processes that 

determine population viability. 

Introduction 

Conservation behaviour is an emerging discipline that utilizes 

the framework and methods of ethology to help solve 

issues important to the biodiversity crisis (Buchholz, 2007). 

Species are becoming extinct or threatened with extinction 

at an accelerating rate due to human population growth 

and our unsustainable use of natural resources. The relatively 

new field of conservation behaviour aims to use a 

scientific understanding of animal behaviour to both determine 

the reasons for differential susceptibility to extinction, 

and to manage threatened animals and their habitats 

to promote population viability. Conservation behaviour 

is not merely the description of the natural history of an 

animal. Instead conservation behaviour uses the framework 

of ethology, originally posed by the Nobel laureate 

Niko Tinbergen, to allow conservation issues to be investigated 

from four complementary behavioural perspectives: 

mechanisms, ontogeny, adaptive function and 

phylogeny. The proximate mechanisms of behaviour include 

the physiological and neuro-endocrine underpinnings 

of animal action. The ontogeny of behaviour 

ELS subject area: Ecology 

How to cite: 

Buchholz, Richard; Yamnik, Patrick; Pulaski, Cassan N; and, Campbell, 

Chelsea A (December 2008) Conservation and Behaviour. In: 

Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester. 

DOI: 10.1002/9780470015902.a0021217 

. Introduction 

. Habitat Selection 

Advanced article 

Article Contents 

. Dispersal, Migration and Conservation 

. Reproductive Behaviours and Population Growth 

. Effects of Small Population Size on Behaviour 

. Managing Human–Wildlife Conflict 

. Implications for Management 

Online posting date: 15 th December 2008 

explores the genetic and learned basis of behavioural development 

over the lifetime of individual animals. Ultimately 

behaviour patterns may cause differential survival 

or reproduction of individuals, and thus serve an adaptive 

function. Finally the ultimate origins of inter-specific variation 

in the behaviour may be investigated by exploring 

how behaviour has evolved among a set of phylogenetically 

related species. These four approaches can be integrated to 

allow conservation behaviourists to propose novel solutions 

to conservation problems. See also: Biodiversity – 

Threats; Modern Extinction; Tinbergen, Nikolaas 

Although the interdisciplinary field of conservation biology 

was formalized as a science in the mid-1980s with the 

formation of the Society for Conservation Biology, recognition 

that behavioural biology could contribute uniquely 

to conservation did not coalesce for another decade, as 

evidenced by a flurry of symposia and publications on the 

subject (listed by Caro, 2007). Conservation behaviour 

came about as there was an increasing realization that 

population-level investigations of genetics and ecology 

were insufficient to explain some rather dramatic species 

declines. For example, cheetah Acinonyx jubatus population 

decline was linked to cheetah-cub killing by lions 

Panthera leo and other large carnivores (Laurenson et al., 

1995). Because cheetah-cub killing is not simply a form of 

predation for food, a more complex behavioural investigation 

of the origins and causes of this behaviour by lions is 

warranted. A conservation behaviour approach to this 

problem would include an investigation of the sensory cues 

that lions use to find cheetah litters (mechanism), the ability 

of cheetah mothers to learn to reduce their risk of litter 

predation (ontogeny), the effect of cheetah-cub killing on 

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net 1

the lion’s survival and reproduction (adaptive function), 

and a comparative analysis of the ecological and life-history 

factors associated with inter-specific infanticide 

among species in the order Carnivora (phylogeny). This 

comprehensive approach to conservation holds promise 

for ameliorating conservation problems if it can be translated 

into management actions that help threatened populations 

grow to a sustainable equilibrium (Beissinger, 

1997). 

When a species is reduced to just a few animals, the behaviour 

of every individual has a direct and obvious impact 

on the species’ survival. When animals are endangered, but 

not at the brink of extinction, the role of behaviour may be 

less obvious but is no less important. Natural selection is 

expected to mould the decision-making of individual animals 

so that they weigh the potential lifetime fitness costs 

and benefits of their options before choosing a course of 

action. The conservation behaviourist’s objective is to understand 

how animal decisions may have become maladaptive 

in a human-dominated landscape, and to 

participate in management efforts that correct or compensate 

for behaviour that reduces survival or reproduction. 

Although there are myriad ways that behaviour might impact 

population dynamics, five behavioural topics will play 

major roles in protecting biodiversity: habitat selection, 

dispersal and migratory movements, reproduction, living 

in small populations and human–animal conflict over resource 

use. See also: Conservation of Populations and 

Species 

Habitat Selection 

Habitats that look fairly homogeneous to the untrained 

human eye may be heterogeneous in features important to 

the survival and reproduction of a particular animal species. 

Even within species, suitable habitat can vary with the 

age, sex and condition of the individual. Thus we expect 

animals to be choosy about where they live, and to move to 

places that maximize their lifetime reproductive success. If 

landscape changes by humans cause animals to bypass 

good habitats, or to become attracted to poor habitats, 

population decline may occur. The framework of conservation 

behaviour provides us with potential management 

tools to manipulate the habitat use of animals so that they 

use habitats optimally in light of anthropogenic alterations 

to which they have not had time to adapt in an evolutionary 

sense. 

Getting animals past human obstacles 

Goal-oriented movements of animals might cover very little 

geographic distance or alternatively occur for just a few 

minutes of the animal’s life, but be of great importance to 

the survival and reproductive success of individuals. For 

example, some species have a critically important transition 

from the location where they are born or hatched, and 

the place where they will be reared. Understanding the cues 

2 

Conservation and Behaviour 

that these naïve, fledgling animals use to find their way 

allows the conservationist to avoid conflicts between this 

critical transition and anthropogenic changes. For example, 

newly hatched sea turtles and fledgling petrels must 

move from their nests to the ocean, but can become disoriented 

by some wavelengths of artificial night lighting 

(Witherington, 1997). Likewise, roadways and hydroelectric 

dams can function as barriers to animal movement that 

could be circumvented through management of the cues 

that imperilled species use to find their way. There will be 

times when the findings of conservation behaviourists may 

run into conflict with other efforts at environmental protection. 

For example, migratory tree bats (Lasiurus species) 

appear to be using wind turbines as mating sites along migration 

routes. Cryan and Brown (2007) have suggested 

that these normally solitary bats may use a behavioural rule 

such as ‘go to the tallest structure’ to rendezvous during fall 

migration. As a result dozens or hundreds of bats are killed 

during a several week period, and the protection of biodiversity 

finds itself at odds with efforts to use alternative 

energy sources to reduce global climate change. Conservation 

behaviourists must be involved in efforts to make 

wind turbines less attractive or less deadly to bats, as well as 

participate in other situations where acute animal contact 

with human landscape structures cause mortality and interrupt 

crucial events in a species’ life cycle. 

Getting animals to use good habitat 

In human-dominated landscapes habitat patches are likely 

to be relatively small and susceptible to local extinctions. 

Small populations in those habitat fragments may decline 

for a number of reasons, including inbreeding depression 

and greater exposure to climatic extremes. Suitable patches 

in some cases may remain unoccupied if cues used in habitat 

selection are absent, if the patch is outside of an organism’s 

perceptual range or if misleading cues are present 

that deter settlement (Gilroy and Sutherland, 2007). 

Behavioural knowledge may be used to lure individuals 

to settle in these unoccupied or underutilized habitats. 

Many species display conspecific attraction wherein the 

presence of conspecifics is likely to be indicative of suitable 

habitat (Ahlering and Faaborg, 2006). Ward and 

Schlossberg (2004) successfully attracted endangered territorial 

black-capped vireos Vireo atricapilla to unoccupied 

habitat using recorded vocalizations. Heterospecific cues 

are also used in habitat selection; least flycatchers, Empidonax 

minimus were attracted to habitat utilized by 

American redstarts Setophaga ruticilla (Fletcher, 2007). 

Similarly, marbled newts Triturus marmoratus oriented towards 

the calls of natterjack toads Bufo calamita (Diego- 

Rasilla and Luengo, 2004). In addition to conspecific or 

heterospecific auditory cues, olfactory, chemical and visual 

cues may also be used to attract individuals to unoccupied 

habitat (Gilroy and Sutherland, 2007). Habitat cues such as 

light and vegetation are also used by organisms in selecting 

suitable habitat, and these cues may be manipulated to 

attract individuals to unoccupied patches. Similarly 

ENCYCLOPEDIA OF LIFE SCIENCES & 2008, John Wiley & Sons, Ltd. www.els.net

animals may adopt microhabitat choices by observing the 

behaviour of experienced individuals. 

Getting animals to avoid bad habitat 

Alternatively it may be necessary to dissuade animals from 

using an attractive habitat patch that is actually harmful. 

Such ‘ecological traps’ occur when cues that historically 

indicated suitable habitat have become disconnected from 

habitat quality due to human disturbance. An ecological 

trap functions as a population sink (Schlaepfer et al., 2002). 

The conservation behaviourist may develop tools for 

masking misleading cues to eliminate the sensory allure 

or introduce additional cues to indicate the habitat’s poor 

suitability for settlement. The majority of ecological trap 

studies have focused on birds, and a number of these have 

found forest edge habitats to function as traps due to increased 

predation and nest-parasitism (Battini, 2004). 

Edge-effect traps may be countered by creating openings 

in the canopy of the forest interior which may attract birds 

away from the habitat edge (Battini, 2004). Heterospecific 

cues may also be used to dissuade individuals from settling 

in unsuitable habitat. American redstarts S. ruticilla were 

more likely to avoid habitats with least flycatcher, E. minimus 

vocalizations than control habitat patches (Fletcher, 

2007). Understanding behavioural cues and mechanisms 

resulting in ecological traps will allow for the management 

of these problematic habitats and their associated wildlife. 

Dispersal, Migration and Conservation 

The direction, rate and motivational basis for animal 

movement varies throughout the day, seasonally and with 

life stage. If we employ the Tinbergen framework to the 

problem of an animal’s movement out of its traditional 

home range, conservation behaviour might consider, for 

example, the hormonal (mechanistic) basis for an individual’s 

decision to move elsewhere, whether it learned about 

the direction of movements from its parents (ontogeny) 

and the fitness consequences of the move (adaptive function). 

Comparing the relationship between life-history 

traits and the movement patterns of a group of related 

species might be useful in anticipating conservation conflicts. 

Individual differences in the distance that an animal 

moves provides additional structure for our discussion of 

how animal locomotion relates to conservation of biodiversity. 

Geographical scales of animal movement can be 

divided into two broad categories: dispersal over relatively 

short distances, and migration over much longer distances. 

Short distances 

Short distance dispersal entails emigration from the natal 

or home range wherein an individual’s objective for moving 

may be to avoid inbreeding, reduce competition with kin or 

to locate better food resources. There are a wide range of 

abiotic and biotic factors that determine dispersal. In 

fragmented or isolated habitat patches, dispersing individuals 

may suffer high mortality and reduce the viability of 

the local population. Dispersing animals, particularly large 

carnivores, may come into conflict with humans when they 

travel through human-dominated habitats, reducing public 

support for wildlife preservation. Thus investigating the 

motivation behind individual dispersal can be critical to 

species conservation. For example, Zedrosser et al. (2007) 

demonstrated that male brown bears Ursus arctos will migrate 

up to 119 km to avoid inbred mating, exposing them 

to a greater risk for human contact. Proper management of 

the brown bear might involve translocation of breedingage 

animals to create local breeding opportunities for bears 

that would otherwise disperse. Alternatively manipulating 

environmental cues to redirect the movement of dispersing 

bears through protected corridors may reduce bear mortality 

and conflict with humans. See also: Range Limits 

The causes of animal dispersal will be of increasing concern 

as disease epidemics and emerging zoonotic pathogens 

threaten both human and wildlife health. The social systems 

of chimpanzees Pan troglydytes and gorillas Gorilla 

gorilla, for example, may explain the differential impact of 

the ebola virus on these great ape species. In Great Britain 

Eurasian badgers Meles meles serve as reservoirs of bovine 

tuberculosis, and areas with high densities of badgers typically 

have higher incidences of bovine tuberculosis 

(McDonald et al., 2008). Reducing the density of badgers 

through culling, however, disrupts the social and territorial 

structure of the badgers. This resulted in the surviving 

badgers travelling greater distances and utilizing larger 

areas, effectively spreading bovine tuberculosis. The latter 

example highlights the need for a behaviourist’s understanding 

of individual behavioural strategies for anticipating 

the complexities of disease transmission in landscapes. 

Long distances 


Seasonal migration may involve non-stop movement 

across thousands of kilometres of unsuitable habitat, resulting 

in the mortality of individuals in poor condition or 

those unable to orient correctly. Unfortunately there is little 

information known about how the different stages of 

migratory movement affect survival and reproduction. For 

example, how might the migratory routes or duration of 

stopovers at resting sites affect fecundity in the subsequent 

breeding seasons? These migratory options are behavioural 

decisions suitable for investigation by conservation behaviourists. 

The most information available is for birds, with 

virtually no data available for the highly threatened migrations 

of hoofed mammals (Bolger et al., 2008). Comparative 

studies in birds have revealed that migratory 

species are more susceptible to decline or extinction than 

non-migratory species (references in Thomas et al., 2006). 

In a phylogenetically controlled analysis of population 

status in North American shorebirds, Thomas et al. (2006) 

found that species that opted for inland (rather than 

coastal) migratory routes were more threatened. The authors 

suggest that additional protections for ephemeral 


Number declining or extinct 

wetlands and upland area stopover sites might stem the 

decline of these bird species. Green sea turtles Chelonia 

mydas that both reproduce and forage in the Cocos Islands 

have very brief migrations compared to other populations, 

and are thus hypothesized to have spared energetic resources 

that should result in greater fecundity or survival 

(Whiting et al., 2008). If confirmed, this population of turtles 

might be more resilient to human disturbance, allowing 

conservationists to focus their preservation efforts on the 

more susceptible long-distance migrants. 

Migratory motivation and compass orientation can have 

both learned and instinctual components. New migratory 

routes seem to evolve rather quickly, and thus may not be 

reflected in broad brush genetic determinations of ‘evolutionary 

significant units’, a measure of population uniqueness 

favoured by policy makers (Davis et al., 2006). Efforts 

to recover the endangered whooping crane Grus americana 

in North America have entailed using behavioural biology 

to stop migration in some reintroduced populations (central 

Florida, USA), and establish new migratory routes 

(between north Florida and Wisconsin, USA) in others 

(Canadian Wildlife Service and U.S. Fish and Wildlife 

Service, 2005), in both cases through the manipulation of 

learned cues in the rearing environment. Virtually nothing 

is known about the mechanistic and developmental basis of 

migration in ungulates (Bolger et al., 2008); however, a 

better understanding of how their behaviour might be 

managed so that they can circumvent anthropogenic 

obstacles will be critical to the conservation of these land-bound 

mammals (Figure 1). See also: Migration: Orientation 

and Navigation 

Wildlife corridors 

14 

12 

10 

8 

6 

4 

2 

0 

Dispersal behaviour is of particular interest to conservation 

biologists due to its potential impacts on population 

Overhunting Habitat loss 

Threats 

Migration obstacle 

Figure 1 More migratory populations and species of hoofed mammals are endangered by anthropogenic obstacles to animal migration such as fences, roads 

and reservoirs, than by overhunting or agricultural development of natural areas. Data from Bolger et al. (2008). 

4 


genetics. Animals confined to small, disconnected populations 

have only genetic relatives to reproduce with, resulting 

in low genetic variability, inbreeding depression and 

poor disease resistance. Dispersal behaviour significantly 

affects population connectivity, and may be facilitated by 

the creation of suitable habitat corridors within the fragmented 

landscape. Behavioural studies can provide important 

insight into designing corridors based on 

behavioural responses of wildlife to habitat edges and corridors. 

See also: Landscape Ecology 

Behavioural studies will provide valuable insight into 

determining when corridors are needed and how to design 

them. Behavioural studies have demonstrated that many 

species, including spotted salamanders Ambystoma maculatum, 

and two butterfly species, Phoebis sennae and 

Eurema nicippe, detect and avoid habitat edges, and this 

behaviour leads to a greater probability of corridor use 

(Haddad, 1999; Rittenhouse and Semlitsch, 2006). The 

habitat quality within the corridor itself may determine its 

effectiveness. The Chucao tapaculo Scelorchilus rubecula 

disperses well through low-quality shrub habitat to access 

forest patches but avoids large open gaps between habitat 

patches (Castello´ n and Sieving, 2005). The salamander 

Ensatina eschscholtzii travels more rapidly between suitable 

habitat patches if corridor quality is poor (Rosenberg 

et al., 1998). Thus, behavioural studies can greatly inform 

the use and design of management by understanding which 

organisms are likely to use corridors effectively based on 

their response to habitat edges, their behaviour within corridors 

and other factors. 

An important application of corridor theory is the use of 

highway overpasses and underpasses to provide connectivity 

between habitat patches that are bisected by roads. 

Understanding how animals respond to roads, traffic and 

the structural design of under- and overpasses will allow 

managers to design corridors that maximize wildlife use 


and minimize traffic-induced wildlife mortality. For example, 

highway crossings by elk Cervus elaphus in Arizona, 

USA, decreased with increasing traffic volume, although 

crossings were more likely to occur near important resources 

and depended on the season (Gagnon et al., 2007). 

Importantly Ng et al. (2004) found that the structural design 

of crossings can greatly affect their utility. Over- and 

underpass design may be the most important factor affecting 

which, if any, species are likely to use them, with some 

species such as grizzly bears, U. arctos preferring wide, 

short and tall crossings, whereas other species such as cougars 

Puma concolor prefer more constricted passages 

(Clevenger and Waltho, 2005; Mata et al., 2005). Understanding 

an organism’s behaviour will allow managers to 

most efficiently plan highway crossings that will suit wildlife 

needs. 

Reproductive Behaviours and 

Population Growth 

The rate and productivity with which animals breed determine 

in part whether their population can compensate for 

losses due to anthropogenic changes such as climate 

change, hunting and competition with invasive species. 

Differential mating success, or sexual selection, occurs 

through mate choice and intra-sexual competition, with 

myriad implications for conservation (Quader, 2005). 

See also: Sexual Selection 

Mating systems and genetic diversity 

Mating systems provide broadly defined categories encompassing 

how the sexual strategies of females and males 

are integrated under natural conditions. Polygamous mating 

systems have been linked to an increased risk of extinction 

in birds (Doherty et al., 2003), perhaps because the 

effective population size (N e) is lower in mating systems 

where only a few males are mating with the majority of 

females (Parker and Waite, 1997). In small populations in 

particular low genetic diversity may be exacerbated by extreme 

differences in male mating success, an effect that may 

be ameliorated by behavioural management. For example, 

Alberts et al. (2002) found that the temporary removal of 

dominant males in the threatened Cuban iguana (Cyclura 

nubile) allowed other males to mate, theoretically increasing 

genetic variability and population persistence. If female 

choice is the primary determinant of male mating success, 

however, it might be appropriate to manipulate positively 

the apparent quality of a male not normally attractive to 

females. Fisher et al. (2003) showed that by redistributing 

scent markings of individual male loris in captivity, it was 

possible to increase the likelihood that females would subsequently 

mate with them. 

Human efforts to promote conservation can have inadvertent 

negative effects on population viability when they 

focus on natural selection and ignore sexual selection. 

Trophy hunting has been traditionally thought of as a relatively 

benign way to both remove surplus males from 

populations and provide financial resources to human 

communities surrounding protected areas. Infanticide by 

males that replace trophy hunted males, unfortunately, 

may destabilize lion prides. Thus the intra-sexual competition 

of male lions enabled by trophy hunting may result in 

unsustainable use if male age is not considered (Whitman 

et al., 2004). In the case of bighorn sheep Ovis canadensis 

removal of males with trophy size horns removes fastgrowing 

males whose ‘good genes’ may normally benefit 

female reproductive success indirectly through the survival 

of their offspring (Coltman et al., 2003). Even when wildlife 

managers attempt to positively affect female condition, for 

example, through supplemental feeding, sexual selection 

can cause unexpected population consequences. Supplemental 

feeding of female endangered kakapo parrots Strigops 

habroptilus in New Zealand resulted in male-biased 

clutches of offpring (Clout et al., 2002). Because males must 

be large to compete with other males for matings, mothers 

apparently produce more sons if they have an abundance of 

food. See also: Natural Selection: Sex Ratio 

Parental behaviour 


Parental care of offspring must also be considered in managing 

endangered animal populations. In some species, 

adults may be present at nesting sites and breeding burrows, 

but are not contributing their genes to the next generation. 

In cooperatively breeding, or ‘helping’, species, 

offspring from previous breeding seasons may stay with 

their parents and assist them in rearing additional siblings. 

Most helpers appear to help because no breeding opportunities 

are available elsewhere. A population census 

would mistakenly incorporate them in an analysis of population 

viability, when in fact the N e is much lower than it 

appears. To reduce the risk of extinction of the Seychelles 

warbler Acrocephalus sechellensis, which was restricted to a 

single island, Komdeur et al. (1995) translocated helpers to 

an unoccupied island. These helpers bred successfully and 

eventually accumulated helpers of their own when the new 

island’s territories became fully occupied. Thus knowledge 

of the adaptive function of cooperative breeding was used 

to found a new population of this endangered species without 

reducing the effective population size of the single 

source population. See also: Eusociality and Cooperation 

In other cases, wildlife management intended to protect 

endangered species has had unintended negative consequences 

on parental care. Poaching of rhinos for their 

horns resulted in drastic declines of African rhino species. 

In Namibia wildlife managers captured and removed the 

horns of their few remaining rhinos to make them worthless 

to horn-poachers. Unfortunately the calves of de-horned 

mother rhinos had low survival, probably due to the reduced 

ability of their mothers to protect their offspring 

from predators (Berger and Cunningham, 1994). 


Effects of Small Population Size on 

Behaviour 

The reduced reproductive success of individuals in small 

populations, called the ‘Allee Effect’, is of great concern to 

conservationists. Sometimes this reduced reproduction is 

simply a consequence of low population densities and the 

inability of individuals to find one another for mating. In 

other cases the adaptive benefits of living in social groups 

are reversed below a threshold group size. For example, in 

some normally social species it might be more costly to 

lifetime reproductive success to live in a too small group 

than to live an entirely solitary existence. Allee effects are 

not readily predicted if a ‘species typical’ viewpoint of behaviour 

is adopted, but will be anticipated by conservation 

behaviourists because they focus at the level of individual 

differences in decision-making behaviour. We explore several 

examples of the Allee effect in endangered mammal 

species. 

African wild dogs 

Small population sizes may have particularly profound 

effects on the behaviour and population viability of highly 

social animals such as the African wild dog, Lycaon pictus. 

Courchamp et al. (2002) demonstrated that small African 

wild dog populations may suffer reduced viability due to a 

trade-off between hunting and pup-guarding. Wild dog 

hunting is performed predominantly by the pack, and 

larger hunting groups are typically more successful at capturing 

prey. Additionally, although the majority of the 

pack is hunting, one adult usually remains to guard pups 

from predation. Thus, when packs reach a threshold level 

of fewer than about five individuals, the trade-off between 

hunting success and pup protection may have serious 

effects on population viability. Either hunting success or 

pup survival will be reduced at low group sizes. African 

wild dog populations composed of very small groups can be 

viable only if the risks of pup predation are also very low. 

Saiga antelope 

Behavioural shifts associated with reduced population size 

have also been demonstrated in the saiga antelope (Saiga 

tatarica) in Asia. Saiga populations have seen a catastrophic 

decrease in the number of males, due to an increase 

in poaching for saiga meat and horns. Poaching of adult 

males resulted in an extremely female-biased sex ratio, 

which in turn led to a decline in the number of pregnancies 

(Milner-Gulland, 2003). Normally, in the polygnous mating 

system used by saiga antelopes, males will defend a 

harem of 12–30 females. In female-biased populations, 

dominant females aggressively excluded subdominant females 

from mating with the few remaining males (Milner- 

Gulland, 2003). As a consequence first-year females in 

poached populations do not conceive, and the populations 

decline due to the direct mortality of males by poaching, 

6 


and the reduced fecundity of females due to a behavioural 

Allee effect. 

Hawaiian monk seals 

In contrast to the saiga, small populations of the endangered 

Hawaiian monk seal Monachus schauinslandi have 

unusually high numbers of adult males. Although the reasons 

for the male-biased sex ratios seen in this species are 

unknown, small population size may be a contributing 

factor (Starfield et al., 1995). Male-biased sex ratios are 

thought to increase the probability of mobbing, a form of 

intra-sexual competition in which individuals or groups of 

males may injure and/or kill adult females and immature 

pups during mating attempts. Mobbing exacerbates the 

male-biased sex ratios by further reducing the numbers of 

breeding females. Conservation behaviourists have effectively 

reduced mobbing by translocating surplus males to 

islands unoccupied by seals, allowing females to mate and 

rear pups more successfully. 

Managing Human–Wildlife Conflict 

Utilitarian value through sustainable use of wildlife by humans 

is thought to be an essential incentive for nature 

preservation (Hutton and Leader-Williams, 2003). An understanding 

of how and why animals behave the way they 

do will be instrumental in managing the population-level 

consequences of the direct and indirect effects of harvesting 

animals. Examples of wildlife (or their habitat) use by humans 

that benefit from a conservation behaviour approach 

include bycatch reduction in marine fisheries, management 

of ecotourism, reducing crop raiding by elephants and disruption 

of animal communication by pollution. 

Bycatch reduction 

An estimated 27 million tons of non-target species are discarded 

annually in fisheries worldwide (Alverson et al., 

1994). Of greatest concern is the destruction of individuals 

of long-lived, slow breeding (also called ‘K-selected’) species 

such as porpoises, sea turtles and albatrosses, whose 

populations cannot recover quickly from high rates of 

adult mortality. Understanding how and why non-target 

species are being caught in these fisheries are intrinsically 

behavioural questions. The development of sensory deterrents, 

such as acoustic ‘pingers’ to warn porpoises away 

from gill nets (Kastelein et al., 2006), and olfactory repellants 

to keep sea birds from pursuing baited hooks in longline 

fisheries (Pierre and Norden, 2006) will require 

continued study to understand how their effectiveness is 

impacted by individual learning, and how evolutionary 

history determines which species respond to these bycatch 

reduction methods. Bycatch reduction devices that allow 

non-target species to exit trawl nets without reducing the 

capture of the target organism will require further investigation 

of the sensory world of these species and the 


decision rules they use in response to those stimuli. Differential 

light preferences of target and non-target species may 

also be useful in developing more selective fisheries 

(Marchesan et al., 2005). See also: Reproductive Strategies 

Ecotourism 

Generally, ecotourism is thought to change wildlife behaviour, 

but some studies have been able to link human disturbance 

with positive effects on animal populations. for 

example, the presence of bear viewing tours in British Columbia 

temporarily displaces adult male brown bears 

U. arctos, which in turn allows for females with cubs to 

spend more time fishing and foraging due to the fact that 

female bears appear to be less vigilant around humans than 

adult males. The displacement of large males by the presence 

of ecotourists is thought to create a temporal refuge 

that enhances feeding opportunities for subordinate age/ 

sex classes (Nevin and Gilbert, 2005). More commonly investigators 

conclude that human disturbance has a neutral 

or only slightly negative effect on wildlife. Minimal reaction 

to human observers occurs in eastern chimpanzees 

(Pan troglodytes schweinfurthi) in the Kibale Forest, 

Uganda, provided that tourists visit in small groups 

(Johns, 1996). Magellanic penguins Spheniscus magellanicus 

in Argentina show both behavioural and physiological 

habituation to tourist visitation (Walker et al., 

2006). It is not known, however, if the ontogenetic habituation 

of these penguins serves an adaptive function. What 

if becoming tamer around humans puts penguins at greater 

risk of ignoring other predators? Inter-specific comparisons 

of stress responses to disturbance of penguin species 

that evolved in the absence of native terrestrial predators, 

such as the Galapagos penguin Spheniscus mendiculus (Figure 

2), with those that show fearful reactions would be 

helpful to predict the conservation consequences of expanding 

ecotourism to additional penguin species. The 

challenge of ecotourism has always been to combine the 

demands of tourists with the needs of local populations and 

the conservation of protected areas. Not all behavioural 

change by animals visited by ecotourists is harmful to 

population viability. Sustainable ecotourism requires that 

conservationists minimize disturbance that impairs the 

lifetime reproductive success of individual animals. 

Crop raiding by elephants 

Human–elephant conflict over crop raiding is a significant 

threat to elephant conservation efforts in Africa and Asia. 

In addition to imposing significant economic burdens on 

humans that farm near elephant reserves, elephants may 

harm or even kill humans who attempt to repel them. 

Conservation behaviourists are attempting to properly understand 

the proximate and ultimate factors that promote 

crop raiding. The benefits of crop raiding to the elephants 

are dependent on the proximity of natural habitats to the 

crop fields, the timing of crop ripening and the spatial distribution 

of wild forage items (Rode et al., 2006). Males 

between the ages of 10 and 14 years and between the ages of 

20 and 24 years are associated with crop raiding, potentially 

due to three factors: social independence, risk tolerance 

and male–male competition (Chiyo et al., 2005). In 

addition to practical methods for preventing elephants 

from reaching crop fields (such as trenches, electric fences 

and grass buffers), behaviourists must develop management 

techniques that co-opt male elephant strategies that 

promote conflict with their human neighbours. 

Pollution 


Figure 2 Sustainable ecotourism provides financial incentives to protect 

natural areas. Conservation behaviour studies are needed to determine if 

island species, such as this Galapagos penguin, habituate more easily to 

human disturbance because they have evolved without terrestrial predators. 

Photo courtesy of Clifford Ochs. 

Human activities contaminate nearby animal habitats with 

a wide range of pollutants that may interfere with the 

communication systems of animal species. In the presence 

of such information disruptors, organisms may fail to detect 

important environmental cues required for the acquisition 

of food, mates, habitats and predators. For example, 

pesticides and heavy metals may interfere with antipredator 

responses (Lu¨ rling and Scheffer, 2007). Excess 

artificial light (light pollution) disrupts orientation cues in 

hatchling marine turtles (Witherington, 1997) and other 

nocturnally active wildlife. The nocturnal beach mouse is 

unable to forage efficiently in areas illuminated by artificial 

lights (Bird et al., 2004). Man-made noises, also serve as 


stressors to animal populations causing increased hypothalamic 

response resulting in physiological stress that may 

cause dispersal or impair reproduction. 

Implications for Management 

Problems of animal behaviour occur in most areas of conservation, 

and conservation behaviour is likely to become 

an even more pertinent tool to prevent biodiversity loss as 

wildlife becomes restricted to parks and preserves surrounded 

by anthropogenic environments (Buchholz, 

2007). Unfortunately most conservation biologists and 

wildlife managers have little training in the ethological 

framework or methodology that underpins conservation 

behaviour. Despite calls for the inclusion of behaviourists 

on conservation planning teams (Arcese et al., 1997), conservation 

behaviour remains poorly integrated with conservation 

biology (Caro, 2007; Angeloni et al., 2008). Our 

ability to protect biodiversity despite global climate 

change, exponential human population growth and unsustainable 

resource use will require that ethologists participate 

in conservation management, and demonstrate more 

effectively that the mechanisms, ontogeny, adaptive function 

and evolutionary history of animal behaviour have 

practical import to conserving nature. 

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Caro T (1998) Behavioral Ecology and Conservation Biology. New 

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Oxford University Press. 


Behavioural biology: an effective and 

relevant conservation tool 

Richard Buchholz 

Opinion TRENDS in Ecology and Evolution Vol.22 No.8 

Department of Biology, University of Mississippi, University, MS 38677-1848, USA 

‘Conservation behaviour’ is a young discipline that 

investigates how proximate and ultimate aspects of 

the behaviour of an animal can be of value in preventing 

the loss of biodiversity. Rumours of its demise are 

unfounded. Conservation behaviour is quickly building 

a capacity to positively influence environmental decision 

making. The theoretical framework used by animal behaviourists 

is uniquely valuable to elucidating integrative 

solutions to human-wildlife conflicts, efforts to reintroduce 

endangered species and reducing the deleterious 

effects of ecotourism. Conservation behaviourists must 

join with other scientists under the multidisciplinary 

umbrella of conservation biology without giving up on 

their focus: the mechanisms, development, function and 

evolutionary history of individual differences in behaviour. 

Conservation behaviour is an increasingly relevant 

tool in the preservation of nature. 

The origins of conservation behaviour 

Behavioural biology did not rank among the fields included 

under the multidisciplinary umbrella of conservation 

biology when this new science was created in 1985 [1]. 

Perhaps as a consequence, behavioural study was not 

incorporated into the first conservation biology textbooks 

and conservation was not mentioned in the animal behaviour 

texts of the era [2]. It required another decade for the 

nascent field of ‘conservation behaviour’ to coalesce from 

symposia, workshops and the resulting multi-authored 

volumes that appeared after the mid-1990s (citations in 

[3]). Some have suggested that behavioural biologists 

became interested in conservation only because they 

anticipated a new source of research funding [3,4], but 

those of us who were graduate students at the time know 

the real reason that conservation behaviour arose: in the 

face of biodiversity loss and widespread habitat destruction, 

we wanted our science to be relevant to saving the 

natural world. 

Wishing for behavioural biology to be useful to 

conservation, however, is not evidence that it is. Indeed, 

some early proponents of conservation behaviour recently 

seem to have lost their faith in the discipline * . Likewise, I 

have observed that some aspiring conservation behaviourists 

are questioning the success of conservation behaviour 

at integrating with mainstream conservation efforts. Their 

Corresponding author: Buchholz, R. (byrb@olemiss.edu). 

* Caro, T. (2006) Challenges and opportunities for behavioural ecologists to save 

Planet Earth. 25 July Plenary session, 11th Congress of the International Society for 

Behavioral Ecology, Tours, France. 

Available online 27 June 2007. 

www.sciencedirect.com 0169-5347/$ – see front matter ß 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2007.06.002 

pessimism is in sharp contrast to my own view: a decade 

after I co-edited the first book on the subject [5], Iam 

pleased with recent developments in the adolescence of 

conservation behaviour. After only a decade of existence, it 

is premature to dismiss the relevancy of the conservation 

behaviourist to saving biodiversity. Here, I show evidence 

of the vibrancy of this growing field (Box 1) and then 

recount how the theoretical framework of conservation 

behaviourists is already positioning them to help solve 

the types of conservation issues that will be especially 

vexing in the coming decades. 

Defining conservation behaviour 

It is obvious that species-typical patterns of animal 

movement, feeding and mating must be considered in 

conservation planning. Thus, the debate over the role of 

modern animal behaviour studies in conservation is not a 

question of whether major differences in species comportment 

(e.g. seasonal migration versus year-round residency) 

are important to conservation planning. Instead, 

it is a disagreement over whether the discipline-specific 

training of animal behaviourists, sensu stricto, is a valuable 

addition to conservation action teams [6]. I have 

observed two possible reasons why conservation behaviour 

has not made major in-roads in traditional conservation 

biology circles: conservation ecologists believe that they 

already ‘do’ behaviour, and many think that animal behaviourists 

work at scales of minor value to protecting entire 

landscapes, the most cost-effective means of conservation. 

Behaviour thinking 

On the surface, ‘doing’ behaviour seems relatively easy. For 

example, conservation biologists might walk through a 

forest quantifying territorial vocalizations to census a 

population of songbirds. Such superficial uses of behavioural 

biology are no doubt useful, but they, like 

species-typical behavioural descriptions by natural historians 

[7], are not conservation behaviour. Conservation 

behaviour takes advantage of an investigatory framework 

implicit to all modern animal behaviour studies. This 

framework is commonly referred to as Tinbergen’s ‘four 

questions’, because it was first proposed by Nobel-Prizewinning 

ethologist Niko Tinbergen as a way to guide 

behavioural research [8]. Tinbergen suggested that we 

can ask four mutually exclusive questions about any one 

behaviour by considering both proximate and ultimate 

explanations for the cause and origin of that behaviour 

pattern (see Table I in Box 2). Some refer to this use of 

Tinbergen’s framework as ‘behaviour thinking’, and to

402 Opinion TRENDS in Ecology and Evolution Vol.22 No.8 

Box 1. The influence of conservation behaviour is growing 

This tenth anniversary of the publication of the first books on 

conservation behaviour [5,44] is an arbitrary date on which to assess 

this young discipline’s success at integrating with conservation 

biology. Rather than expecting conservation behaviour to be fully 

fledged at this point, we should look for signs that it continues to 

strengthen in terms of training resources, pervasiveness in the 

published literature, and acceptance by grant-awarding agencies 

and career mentors. Supportive evidence includes the following. 

Eighty percent of recently published animal behaviour texts 

address conservation in some fashion [2]. Page content that 

contains reference to conservation now averages 2% for texts 

published during the past five years, compared with 0% in the 

decades before that. 

Conservation behaviour training resources are readily available 

on the Internet (http://www.animalbehavior.org/Committees/ 

Conservation). It is now easier for aspiring conservation behaviourists 

(and their mentors) to access background information, 

including a general bibliography, funding sources and graduate 

programs. Also available for download is ‘The Conservation 

Behaviorist’, a journal written for both behaviourists and nonscientist 

decision makers. 

The use of behavioural biology in published conservation studies 

is not uncommon; in fact, it is growing. Linklater [45] discovered 

that the percentage of conservation publications that mention 

behaviour has increased nearly threefold since the conception of 

conservation behaviour in the early 1990s. 

The EO Wilson Student Conservation Research Grant Award of 

the Animal Behavior Society (ABS) was created to provide an 

annual small grant to foster the career development of conservation 

behaviourists. Conservation grant awardees have 

studied logging effects on tree shrew mating systems, stream 

pollution interference with fish communication and dragonfly 

oviposition requirements as bioindicators of wetland quality. 

Perhaps more significant than these new conservation behaviour 

research funds are the types of research that ‘regular’ student 

behaviourists are doing. In 2006, 15% of the standard Student 

Research Awards from the ABS were for projects with conservation 

themes. 

The ‘father’ of conservation biology, Michael Soulé, said that 

the new discipline: ‘‘should attract and penetrate every field 

that could possibly benefit and protect the diversity of life’’ [46]. 

These demographics suggest that the population of conservation 

behaviourists is indeed growing. 

proximate and ultimate explanations as ‘how’ and ‘why’ 

questions. 

Proximate questions about behaviour consider how 

an individual is able to perform an activity. They ask 

about the mechanisms within an organism that make it 

possible for it to behave in a certain way. The proximate 

causes of behaviour include the sensory and endocrine 

mechanisms that regulate behaviour. However, we know 

that these mechanisms can be modified by individual 

experience; thus, we must consider the proximate origins 

of behaviour as well (i.e. how learning modifies behaviour). 

Ultimate questions about behaviour, on the other hand, 

ask why animal species have evolved the proximate systems 

that enable them to behave the way they do. The 

ultimate cause of a behaviour must explain how it helps the 

individual survive and reproduce. If we ponder the ultimate 

origin of that same behaviour pattern, we are examining 

its evolutionary history by comparing how that 

behaviour differs across a group of related species. Tinbergen’s 

framework is most easily explained by applying it to a 

behavioural example (Box 2). 

www.sciencedirect.com 

Box 2. Understanding Tinbergen’s framework for studying 

behaviour 

Tinbergen’s four complementary approaches to studying a behaviour 

pattern are implicit to modern animal behaviour studies (see 

Table I). This framework is most easily explained by applying it to an 

example of human behaviour: automobile drivers stop their cars 

when a traffic light turns red. 

Mechanisms 

We can ask how automobile drivers are able to perceive the red 

colour of the traffic light, the pattern of neural depolarization that 

allows a decision to be made in the central nervous system and how 

that decision is conveyed to the muscles that control the placement 

of the foot on the brake. The problem of ‘road rage’ suggests that 

latency to apply the brake may be affected by the hormonal milieu of 

the driver. 

Ontogeny 

Humans are not born knowing how to drive an automobile. We can 

ask questions about how humans go about learning to stop at a red 

light and how it is that development affects the ability to learn. For 

example, accident statistics suggest that teenagers and senior 

citizens may have greater difficulty stopping at red lights than other 

drivers. 

Function 

We can investigate why stopping at red lights allows drivers to live 

longer and reproduce successfully. The legal and financial costs and 

benefits that contribute to the individual fitness of drivers are 

worthy of study. We might also consider why some individuals are 

more likely to cooperate with other drivers in their society. 

Phylogeny 

An investigation of the history of traffic signals might tell us how 

responses to red lights have changed over time. In humans, we can 

look at how populations have independently developed means of 

making intersections safer. If we compare humans to other species, 

we might ask how the colour red has evolved as a warning signal. 

Table I. Tinbergen’s framework for organizing the study of 

behaviour proposes that any behaviour pattern should be 

investigated from four complementary perspectives 

Cause Origin 

Proximate Mechanisms Ontogeny 

Ultimate Function Phylogeny 

The beauty of Tinbergen’s four questions is that they 

force us to consider multiple, complementary explanations 

for the same behaviour [9]. In terms of saving biodiversity, 

this framework is especially effective in situations in which 

the behavioural adaptations of wildlife are at odds with 

anthropogenic landscapes [10]. Conservationists might 

eventually stumble upon the need for knowing both 

the ‘how’ and the ‘why’ of animal behaviour (Box 3), but 

it would be much more cost effective and time efficient 

if Tinbergen’s framework was applied at the onset of 

conservation research. 

Where does conservation behaviour fit? 

It would be preposterous to claim that behavioural biology 

is the conservation ‘cure all’. Behavioural study is neither 

appropriate nor a priority at all levels of conservation 

action (Table 1 and [11]). The need for behaviourists will 

be greatest when we are confronted with the challenge of 

maintaining animals marooned in protected islands of 

habitat, isolated in a sea of humanity, and managing

Box 3. Harbour porpoises and gill nets: application of 

Tinbergen’s framework 

In 1994 y , Marquez and I used the example of a ‘real-world’ 

conservation problem, the drowning of harbour porpoises Phocoena 

phocoena following entanglement in the gill nets of commercial 

fisherman, to explain how Tinbergen’s four questions could guide 

conservation research. Read and colleagues [47] had called for 

improved understanding of the behaviour of harbour porpoises 

around gill nets. Incidental bycatch of harbour porpoises in the US 

Gulf of Maine groundfish gill net fishery alone averaged over 2000 

individuals per year in the early 1990s, more than twice the 

allowable take rate. 

For heuristic purposes, we suggested that behavioural aspects 

of gill net bycatch research could be approached simultaneously 

from mechanistic, ontogenetic, functional and phylogenetic 

perspectives. Revisiting the problem now, it is rewarding to see 

that anti-entanglement research evolved within Tinbergen’s 

framework. 

Harbour porpoises appear to be in the vicinity of nets because 

nets are placed where porpoise prey are abundant [48]. Making nets 

from material that is more reflective of porpoise sonar did reduce 

bycatch significantly, but perhaps only because the nets were stiffer 

and less likely to entangle the porpoises [49]. Adding acoustic 

alarms, called ‘pingers’, to gill nets reduces the bycatch mortality of 

harbour porpoises [50]. Harbour porpoises show aversive reactions 

to pinging, including spatial avoidance and increasing respiration 

rate [51]. 

Other small cetaceans, however, do not necessarily react the 

same way [51]. In a field experiment, bottlenose dolphins Tursiops 

truncatus (Figure I) appeared to use fish caught in the gill net as a 

food source, but dolphin groups were less likely to approach the 

net’s ‘zone of vulnerability’ when the pingers were activated [50]. 

There is considerable interest in investigating how these species will 

react to long-term use of acoustic alarms. Will cetaceans become 

sensitized to pingers and avoid them more often, or will pingers 

become a ‘dinner bell’ of sorts, attracting porpoises and dolphins to 

pre-caught fish? 

Although the gill net responses of relatively few cetaceans 

have been studied so far, some researchers have hypothesized 

that vulnerability to natural predators, such as sharks and killer 

whales Orcinus orca, might explain species differences in the 

efficacy of using acoustic alarms to reduce incidental bycatch 

mortality. 

I do not mean to suggest that these studies are the result of our 

Society for Conservation Biology poster; these works developed 

organically from the need to solve the gill net entanglement 

problem. Nevertheless, this conservation problem demonstrates 

how a priori use of a conservation behaviour framework would 

foster an efficient conservation research plan [52]. 

Figure I. Bottlenose dolphins are attracted to the fish caught in commercial gill 

nets (photo by Jill Frank). 

y Marquez, M. and Buchholz, R. (1994) An Ethological Framework for 

Conservation Biology. Poster at the annual meeting of the Society for 

Conservation Biology, University of Guadalajara, Jalisco, Mexico. 


Opinion TRENDS in Ecology and Evolution Vol.22 No.8 403 

the inevitable conflicts between the daily needs of humans 

and other animals. It is not pleasant to think of a future in 

which most of nature is drastically altered by humans, but 

the reality is undeniable [12]. 

Global warming 

Conservation behaviourists are developing predictive tools 

for understanding which species in pristine communities 

will need behavioural management when their habitats 

are altered by direct and indirect human disturbance. Paz 

y Miño [13] has termed these circumstances ‘behavioural 

unknowns’ (after Myers ‘environmental unknowns’ [14]). 

The most pressing of these, perhaps, is the need to understand 

how the mechanisms, ontogeny, adaptiveness and 

phylogenetic diversity of animal behaviour will respond to 

climate change due to global warming. Conservation behaviourists 

have already begun to develop a body of literature 

that addresses behavioural responses to rapid climatic 

alterations (Box 4). 

Restoring balance to ecosystems 

Other behavioural unknowns may have less to do with how 

we are destroying habitat and more to do with our attempts 

to restore ecological integrity to human-altered landscapes. 

The reintroduction of large carnivores appears to 

enhance ecosystem biodiversity and stability [15]. Nonetheless, 

game managers fear that huntable (by humans) 

prey species will be decimated because of their naiveté 

after generations without non-human predation. By experimentally 

investigating the anti-predator responses of 

ungulates to predator cues before and after carnivore 

reintroduction, Berger [16] found that prey typically return 

to ‘normal’ anti-predator strategies within one generation 

of carnivore return. If politically feasible, conservation 

behaviour data such as these will be used to support the 

repatriation of carnivores so that balanced ecosystems are 

restored. 

Ecological prediction is a mainstay of traditional 

conservationists [17]. Game theory, and other skills in 

the behaviourist’s toolbox that take advantage of individual 

differences in behaviour, are currently being used to 

anticipate the population consequences of management 

options [18]. In addition to predicting how animals will 

respond to anthropogenic disturbances, animal behaviourists 

are influencing conservation management directly. 

Conservation behaviourists in action 

To date, the contributions of conservation behaviourists 

are much more than theoretical. Conservation behaviourists 

are already involved in hands-on efforts to restore and 

protect animal species. Here, I briefly review some recent 

contributions of note. 

Species reintroduction 

Although the future of biodiversity is in the wild, captive 

breeding of endangered species is sometimes an irreplaceable 

component of the conservationist’s toolbox [11,19]. 

Conservation behaviourists have concentrated on two 

important aspects of captive propagation of endangered 

species: preventing ‘captive selection’ (i.e. maladaptive 

heritable changes in behaviour), and behavioural training


Table 1. Behavioural biology is relevant to multiple conservation contexts 

Conservation context Conservation tool Example of use 

Preventing biodiversity loss Reserve design a 

[37] 

Ecosystem management b 

[15] 

Population viability analysis b 

[43] 

Compromises with economic development Sustainable use b 

[29] 

Species and habitat restoration Field recovery of endangered species a 

[23] 

Captive breeding and reintroduction a 

[20] 

Ecosystem restoration a 

a 

Tools with current behaviour usage. 

[16] 

b 

Tools that will need more behaviourist input as habitat degradation continues (after Beissinger [11]). 

Box 4. Etho-conservation tackles global warming 

The weather systems of the Earth are expected to become more 

extreme, perhaps suddenly and with great spatial heterogeneity, 

owing to the atmospheric retention of heat energy from anthropogenic 

‘greenhouse gas’ production. How animals might react to 

climate change is one of the many ‘behavioural unknowns’ caused 

by environmental degradation [13] that is being investigated using 

Tinbergen’s four questions. 

Mechanisms 

Cactus-living Drosophila species might respond to climate 

change via selection on the timing of their active period in the 

circadian clock mechanism [53]. By becoming active at cooler 

times of the day, they are able to avoid deleterious exposure to 

heat extremes. The physiological stress responses of vertebrate 

organisms are likely to be dependent on individual differences in 

social status and the social function of dominance in that species 

[31,54]. 

Ontogeny 

Culturally determined foraging movements of sperm whale Physeter 

macrocephalus clans might make some song clans predictably 

susceptible to changes in ocean-current-dependent food sources 

[55]. For species with temperature-mediated sex determination, 

such as turtles and crocodilians, behavioural commitment to 

reusing traditional nest sites will impede adaptive population-level 

responses in these long-lived animals. For example, if global 

warming occurs as forecast, modelling suggests that natal site 

philopatry by egg-laying painted turtles will condemn them to 

producing such biased sex ratios that the population becomes 

inviable [43]. 

Function 

Species with poor mobility might experience rapid evolutionary 

behavioural adaptation in response to micro-climatic divergence. 

For example, wood frog tadpoles in shaded, cool ponds appear to 

evolve adaptive thermal preferences quickly [56]. Populations in 

warmer sun-lit ponds, however, seem to lack growth-benefiting 

thermal preferences, suggesting that global warming would cause 

meta-population sinks with predictable localized patterns of species 

extirpation. Hawksbill turtle Eretmochelys imbricata females might 

be able to adjust to a hotter climate through existing preferences for 

tree-shaded beach nesting sites. Unfortunately, beach deforestation 

may prevent this endangered species from avoiding climateinduced 

biased sex ratios [57]. 

Phylogeny 

Sexual selection may have an impact on the response of animals 

to climate change. The degree of advancement of spring migration 

in birds is associated with the strength of female choice across 

species [58]. Colonizing warmer habitats appears to release 

energetic constraints on sexual selection in dark-eyed juncos Junco 

hyemalis [59]. The relaxation of cold climate extremes might select 

against isolating mechanisms, such as reproductive diapause in 

mustelids [60]. 


and management to maximize post-release survival of 

reintroduced individuals. 

Often, captive conditions impose different selection 

pressures on animal genomes than natural selection, 

resulting in behaviour that is advantageous to the survival 

and reproduction of individuals in captivity, but maladaptive 

should they be reintroduced to the wild. For example, 

captivity selects for aggressive behaviour in place of foraging 

behaviour in breeding colonies of the endangered 

butterfly splitfin fish Ameca splendens [20]. Behaviourists 

are helping to modify aquaculture programs to produce fish 

that will forage rather than fight when released to their 

restored habitat. 

In other cases, the protected nature of captive 

environments might allow genetic release from directional 

selection. The escape behaviour of captive-bred oldfield 

mice Peromyscus polionotus, for example, is never subjected 

to selection by owls, stoats, snakes or any of the 

predators that normally threaten the survival of free-living 

rodents. As a result, they have long escape latencies that 

would make them highly susceptible to predators in the 

wild [21]. By considering the genetic mechanisms underlying 

variation in behaviour, McPhee and Silverman [22] 

conclude that we need not abandon reintroduction of such 

individuals. Their solution is to simply use the variance in 

escape behaviour to recalculate the number of released 

animals sufficient to ensure a surviving nucleus of breeders. 

By understanding the genetic mechanisms underlying 

behaviour, conservation behaviourists are able to 

provide release and survival estimates that are more 

realistic. This would thus engender more reasonable expectations 

and cost planning by wildlife managers and 

political decision-makers, and more patience for success 

from the general public. 

Similarly careful behavioural preparation of captiveraised 

animals will lessen animal welfare concerns over 

the poor survival of individuals released to the wild for 

conservation purposes. Anti-predator training of captivereared 

prairie dogs Cynomys ludovicianus appears to 

increase survival upon reintroduction [23]. But the value 

of behavioural manipulation is not limited to potential prey 

species. Poor attention to the social management of African 

wild dog Lycaon pictus groups during ‘soft’ releases to the 

wild might explain several costly reintroduction failures 

[24]. If individuals are chosen to minimize dominance 

conflicts among members of the released wild dog pack, 

the reintroduced animals are more likely to behave cooperatively 

and hopefully survive to reproduce.

Conservation behaviour and natural populations 

There are two major areas of inquiry in which ‘behaviour 

thinking’ is already being applied to the conservation of 

wild populations: improving population viability by adaptively 

managing individual survival and reproductive success 

in isolated populations, and identifying and managing 

deleterious effects of ecotourism. 

Managing survival and reproduction 

Re-establishing prairie dog populations in protected areas 

is important to ecosystem functioning [25], and is crucial to 

efforts to establish a prey base to grow viable populations 

of the highly endangered black-footed ferret Mustela 

nigripes. Behaviourist Debra Shier took advantage of existing 

behavioural information on the adaptive nature of kin 

groups to demonstrate experimentally that translocating 

entire wild prairie dog families achieves conservation goals 

more successfully and efficiently than moving unrelated 

animals [26]. The red-cockaded woodpecker Picoides borealis 

is another endangered US species that has benefited 

from a behaviourist’s understanding of kin recognition 

mechanisms. Wallace and I showed that, by exchanging 

nestlings between nesting cavities at an age young enough 

that parents had not yet learned to identify their offspring, 

we could overcome genetic isolation in a fragmented 

habitat without reducing survivorship of translocated 

individuals [27]. 

Behaviourists have shown how evolutionary conflicts 

among individual animals can give us insight into management 

methods that would not be apparent to a 

traditionally trained wildlife ecologist or conservation 

geneticist. When it comes to population viability, larger 

population size is usually better. Unfortunately, small 

populations do not always have room to grow. A case in 

point is the threatened Cuban iguana Cyclura nubile 

population confined to the US Naval base at Guantanamo 

Bay, Cuba. In the absence of opportunities to 

increase the overall lizard population, Alberts et al. 

[28] showed how the negative impact of male dominance 

on population-wide genetic variation (N e) could be overcome 

through behavioural management. Temporarily 

removing dominant males allowed other adult males to 

obtain mates. 

Sustainable ecotourism 

Ecotourism, the other doyen of sustainable-use advocates, 

must also consider the behaviourally mediated impact of 

human disturbance on population viability. Descriptive 

behavioural studies are likely to find that wildlife change 

their behaviour in response to human visitors, but that 

changes in behaviour are not necessarily bad for the 

animal under observation. For example, although foraging 

brown bears Ursus arctos alter their feeding activities so 

that they can be vigilant in the presence of tourists, this 

behavioural change has no apparent effects on body condition 

[29]. Therefore, human disturbance probably does 

not translate into reduced survival and lower population 

viability in this case. Nesting Magellanic penguins Spheniscus 

magellanicus appear to habituate to frequent tourists, 

but previously undisturbed colonies are markedly 

stressed by the arrival of human visitors [30]. Because 



stressed animals are likely to experience tradeoffs in 

reproductive investment or survival [31], opening new 

colonies to tourism is not recommended without careful 

determination of the human activities that cause the most 

stress to nesting penguins. The complexity of the interspecific 

and intraspecific responses of wild animals to 

anthropogenic and natural stressors benefits from being 

managed in a conservation behaviour framework. 

Should conservation behaviour conform to the 

emphases of conservation biology? 

I think the only way that behavioural biology makes 

sense for conservation is if we retain our unique 

perspective on animal diversity. The ecologists that 

helped found the Society for Conservation Biology [32] 

did not abandon island biogeography theory to work in 

conservation; they applied the concept to the habitat 

islands that are nature reserves. Likewise, population 

geneticists did not ignore Hardy–Weinberg equilibrium 

to promote the conservation of bottlenecked populations; 

rather, they found ways to inform us of the practical 

importance of theoretical genetics. Conservation behaviourists 

are conservation biologists; we should be 

constructively critical of endangered species recovery 

plans [33]. Decisions are often made with very little or 

faulty evidence. For example, decisions to allow habitat 

destruction in the dwindling range of the endangered 

Florida panther Puma concolor coryi were based on 

questionable evidence and the illogical opinion of one 

researcher that this subspecies is a forest obligate (for a 

shocking review, see [34]). 

It has become a conservation platitude of sorts that 

conservation behaviourists must ‘‘translate behavior into 

currencies relevant to conservation at large spatial scales’’ 

[11]. But conflicts with large carnivores and other species of 

potential harm to humans attract much popular press 

and political interest. It is the young panther that 

disperses 350 miles [34] or the few African elephants 

Loxodonta africana that invade villages or kill rhinos 

[35,36] that threaten to scuttle goodwill for conservation, 

not the average behaviour of the population. It is ridiculous 

to suggest that individualistic responses of animals are 

unimportant to conservation. 

Conservation behaviourists will rise to the challenge 

of the important discoveries being made at the interface 

of conservation ecology and genetics. For example, Riley 

and colleagues [37] recently used microsatellite analysis 

combined with radiotelemetry to discover that carnivore 

territories tend to pile up at habitat edges along an 

automotive freeway in California, USA. The intense 

social challenges faced by individual bobcats Lynx rufus 

and coyotes Canis latrans attempting to disperse 

through the gauntlet of territories concentrated near 

large roadways accentuated the limits on gene flow 

imposed by the physical barrier of the road itself. Populations 

on either side of the highway show evidence of 

genetic differentiation as a result. The problem of 

‘territory piling’ [37] along roadways is one well suited 

to Tinbergen’s framework. These crowded carnivores 

should expect a visit from some local conservation 

behaviourists [38].


The next step 

Caro’s [3] charges of irrelevancy levied against conservation 

behaviour are genuine, but not unique to our field. 

There are problems with the application of any science to 

public policy. Academic scientists get caught up in grant 

writing, hypotheses testing and data collection, whereas 

conservation practitioners need practical advice today [39]. 

The reverse is also true; conservation monitoring programs 

often take on a life of their own and do not achieve conservation 

objectives [40]. 

Nearly 100 years ago, conservationist William T Hornaday 

[41] declared: ‘‘We will endeavor to avoid the discussion 

of academic questions, because the business of 

conservation is replete with urgent practical demands’’. I 

believe that it is this sort of concern, that there is an 

opportunity cost to the ‘theoretical’ concerns of conservation 

behaviour, that has led some of my colleagues to 

retreat from conservation behaviour. Instead, they must 

come to realize that we approach a time of desperate need 

for applied behaviourists. One need only look at costly 

efforts to recover species listed under the US Endangered 

Species Act [42] to see that, although all is not lost, all is not 

well either. Wildlife managers have stopped many endangered 

species from going extinct, but few species have 

recovered sufficiently to be de-listed. We can improve 

conservation management decisions. The behaviour of 

individual animals matters to conservation. The growing 

pains of conservation behaviour are not symptoms of dysfunction, 

but rather positive signs of a thriving adolescence. 

Conservation behaviour is relevant right now and 

the time is ripe for the conservation behaviourist to make a 

difference. 

Acknowledgements 

I am grateful to Cliff Ochs, Guillermo Paz y Miño and Suhel Quader for 

commenting on an earlier draft of this paper. Detailed suggestions by Dan 

Blumstein, Marco Festa-Bianchet and an anonymous reviewer improved 

the manuscript. Communications with Steve Beissinger and Joel Berger 

were helpful ten years ago and now too. Tim Caro suggested that I put it 

in writing, and I am very appreciative of his and the editors’ assistance 

and generous patience. Jill Frank and Glenn Parsons kindly offered the 

use of their dolphin photos. 

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175–183 

This special issue of Current Biology takes a broad look at the importance of sociality in biology, from the evolution of 

cooperation to the way that social living might have facilitated the evolution of human intelligence. The issue 

illustrates the fascinating variety of biological societies with articles on social amoebae, social spiders, eusocial 

insets, crows, hyenas and humans. 

Guest Editorial 

All life is social 

Steve Frank 

Reviews 

Evolutionary explanations for cooperation 

Stuart West, Ashleigh Griffin and Andy Gardner 

Kin selection versus sexual selection in eusocial 

insects 

Jacobus Boomsma 

Social learning 

Lars Chittka 

The Cold War of the social amoebae 

Gad Shaulsky and Richard Kessin 

Social cognition in humans 

Chris Frith 

Sociality, evolution and cognition 

Richard Byrne and Lucy Bates 



Social immune systems 

Sylvia Cremer 

Primers 

The social life of corvids 

Nicky Clayton and Nathan Emery 

Hyena societies 

Heather Watts and Kay Holekamp 

Social spiders 

Duncan Jackson 

Quick Guide

Anim Cogn (2009) 12:43–53 

DOI 10.1007/s10071-008-0169-9 

ORIGINAL PAPER 

Evidence of teaching in atlantic spotted dolphins 

(Stenella frontalis) by mother dolphins foraging in the presence 

of their calves 

Courtney E. Bender Æ Denise L. Herzing Æ 

David F. Bjorklund 

Received: 10 January 2008 / Revised: 18 March 2008 / Accepted: 5 June 2008 / Published online: 29 July 2008 

Ó Springer-Verlag 2008 

Abstract Teaching is a powerful form of social learning, 

but there is little systematic evidence that it occurs in 

species other than humans. Using long-term video archives 

the foraging behaviors by mother Atlantic spotted dolphins 

(Stenella frontalis) were observed when their calves were 

present and when their calves were not present, including 

in the presence of non-calf conspecifics. The nine mothers 

we observed chased prey significantly longer and made 

significantly more referential body-orienting movements in 

the direction of the prey during foraging events when their 

calves were present than when their calves were not present, 

regardless of whether they were foraging alone or with 

another non-calf dolphin. Although further research into 

the potential consequences for the naïve calves is still 

warranted, these data based on the maternal foraging 

behavior are suggestive of teaching as a social-learning 

mechanism in nonhuman animals. 

Keywords Teaching Dolphins Social learning 

Foraging 

Electronic supplementary material The online version of this 

article (doi:10.1007/s10071-008-0169-9) contains supplementary 

material, which is available to authorized users. 

C. E. Bender (&) D. F. Bjorklund 

Department of Biological Sciences, Florida Atlantic University, 

777 Glades Road, Boca Raton, FL 33431-0991, USA 

e-mail: courtbender@yahoo.com; cgreen21@fau.edu 

D. L. Herzing 

Department of Biological Sciences, Wild Dolphin Project, 

Florida Atlantic University, 777 Glades Road, Boca Raton, 

FL 33431-0991, USA 

Introduction 

Although one of the most potent forms of social learning in 

humans, there has been little evidence to suggest that 

teaching occurs in nonhuman animals. Some theorists have 

suggested that this may be because teaching requires 

advanced social-cognitive skills, including the ability to 

take the perspective of another and theory of mind, the 

ability to appreciate that an individual’s behavior is based 

on its knowledge and its desires (Boesch and Tomasello 

1998; Tomasello 1996, 2000; Tomasello et al. 1993). For 

example, previous examples of suggested teaching behavior 

by meerkats, cheetahs, and domestic cats seem to 

benefit the prey-handling abilities of the young, but do not 

require the use of higher cognitive mechanisms (Thornton 

and McAuliffe 2006; Caro and Hauser 1992). However, 

Caro and Hauser (1992) provided a definition of teaching 

that may be more inclusive for nonhuman animals, defining 

it as, ‘‘An individual actor A can be said to teach if it 

modifies its behavior only in the presence of a naive 

observer, B, at some cost or at least without obtaining an 

immediate benefit for itself. A’s behavior thereby encourages 

or punishes B’s behavior, or provides B with 

experience, or sets an example for B. As a result, B 

acquires knowledge or learns a skill earlier in life or more 

rapidly or efficiently than it might otherwise do, or that it 

would not learn at all’’ (p. 153). 

Previous studies that suggested teaching in primates and 

cetaceans, although promising, lacked systematic measurement 

of the behavior. Probably the best evidence of 

teaching in nonhuman primates to date is Boesch’s studies 

of mother chimpanzees (Pan troglodytes) in the Tai 

National Park of the Ivory Coast (Boesch 1991, 1993; 

Greenfield et al. 2000). Boesch suggested that the 

chimpanzee mothers facilitated the development of their 

123

44 Anim Cogn (2009) 12:43–53 

offspring’s nut-cracking skills by means of stimulation, 

facilitation, and active teaching. Nut cracking is observed 

in only a few populations of chimpanzees, despite the 

availability of nuts and appropriate tools (i.e., rocks 

appropriate for use as anvils and hammers), qualifying, by 

some definitions, as an example of culturally-transmitted 

behavior (Whiten 2005; Whiten et al. 1999). The interpretation 

of such episodes as ‘‘teaching’’ has been 

questioned, however (Bering 2001; Bering and Povinelli 

2003). Moreover, such episodes are rarely observed, suggesting 

that direct teaching is not a common form of 

cultural transmission in chimpanzees. 

Although evidence of social learning is easier to document 

in these terrestrial great apes than it is in marine 

mammals, nongenetic transmission of behavior across 

generations has also been observed for cetaceans (Kruetzen 

et al. 2005; Rendell and Whitehead 2001), suggesting that, 

like the great apes, these large-brained, slow-developing, 

and socially complex species (Bjorklund and Bering 2003) 

have evolved powerful social-learning mechanisms. 

Similar to research with great apes, little is known about 

the actual mechanism of transmission across generations in 

cetaceans. Herzing (2005) described some potential scenarios 

and mechanisms observed for a group of free-ranging 

Atlantic spotted dolphins (Stenella frontalis), including 

implications of vertical, horizontal, and oblique directions 

of transmission of information during various behavioral 

contexts. Recently, Spininelli et al. (2006) described preytransfer 

between mother and calf in the marine tucuxi dolphin 

(Sotalia fluvialis). Observations such as these suggest 

that the mother-calf relationship may be one of the most 

important sources of information in the young calf’s life. 

There is some evidence of presumed maternal teaching 

behavior associated with stranding behavior as a foraging 

specialization used by part of the population of killer whales 

(Orcinus orca) in the Crozet Islands and off Punta Norte, 

Argentina to capture seal pups on pinniped breeding beaches. 

Adult females demonstrated a modification of their strand 

foraging behavior in the presence of naïve juvenile observers 

(presumably their calves), suggesting that teaching may be 

involved in the development and the rate of success of calves 

in mastering these behaviors (Guinet and Bouvier 1995). 

This comparison between purported teaching in chimpanzees 

and killer whales is interesting because any 

commonalities would have been derived through convergent 

evolution, as the last common ancestor of primates with 

cetaceans is estimated to have lived over 90 million years ago 

(Marino et al. 2007). However, despite the multitude of 

observations of chimpanzees and killer whales in the wild, 

incidences of mother–infant teaching are scarce and 

anecdotal in nature. 

Foraging behavior is a likely candidate for social 

learning among wild dolphins, particularly between mother 

123 

and calf. The mother/calf relationship is the strongest 

association that Atlantic spotted dolphins have in their 

lifetimes (Herzing and Brunnick 1997). The prolonged 

developmental period provides both ample time and situational 

possibilities for a calf to learn foraging strategies 

from its mother (Herzing 1996). The majority of daytime 

feeding behavior of Atlantic spotted dolphins is benthic 

foraging, in which dolphins use echolocation to locate fish 

in the sandy bottom and then dig prey items out of the sand 

in order to catch and eat them (Herzing 1996). 

Much of what we know about marine mammal social 

learning comes from research with captive animals due, in 

part, to the difficulty of studying such phenomena in the 

wild. Attempts to assess teaching among captive animals 

often involve contrived situations, which may affect the 

animals’ success or failure (Kuczaj et al. 2005). Studies 

that assess social learning in wild populations of marine 

mammals are needed to validate and supplement the findings 

from captive animals and to better understand the 

spontaneous occurrence of social learning in natural 

settings. 

In the present study, using video archives from a longterm 

naturalistic study, we investigated social learning and 

possible teaching behavior by the Atlantic spotted dolphin. 

Unlike most previous research examining social learning in 

nonhuman mammals in which the focus is on the observer/ 

learner (e.g., Bjorklund et al. 2002; Guinet and Bouvier 

1995; Herman 2002; Tomasello et al. 1993), the present 

study shifted the focus from the observer (in our case, the 

calf observing the foraging behavior) to the model (the 

mother performing the foraging behavior) to explore the 

possibility of teaching behavior. We examined the foraging 

behavior by mother dolphins when foraging in the presence 

of their young (less than 3-year-old) calves in comparison 

to when the calves were not present. Additionally, comparisons 

were then made between mothers foraging alone 

and when they were foraging with non-calf conspecifics. 

Should the mothers alter their foraging behavior in the 

presence of their young, it would be suggestive of teaching 

and provide a possible mechanism for cultural transmission 

within this dolphin species. 

Methods and analysis 

Natural history 

This study was performed using underwater video recordings 

of the Atlantic spotted dolphin collected by the Wild 

Dolphin Project (Herzing 1997) in the study area north of 

Grand Bahama Island, Bahamas during summer field seasons 

between 1991 and 2004 (Fig. 1). Unlike many other 

marine mammal habitats, this area is optimal for behavioral

Anim Cogn (2009) 12:43–53 45 

Fig. 1 Map of study area for the wild dolphin project underwater 

video recordings collected over sandbanks north of Grand Bahama 

Island Study population of Atlantic spotted dolphins ranges over an 

area of approximately 500 km 2 

observation with clear, warm waters that allow for excellent 

visibility up to 90 ft and long observational periods 

(Herzing 1996). The dolphins in this study have been 

observed since 1985, and include over 200 dolphins that 

have been individually recognized and sexed. Atlantic 

spotted dolphins can be categorized into four age classes, 

based on the pigmentation of the individual (Herzing 

1996). The number of spots on the individual is correlated 

with age, with a newborn having no spots. Although most 

individuals in the population are tracked from birth, this 

allows for approximating the individual’s age when it is not 

known from previous sightings. Calves in the sampled 

foraging events 3-years-old or younger were still observed 

to be nursing during the encounter year. The year of the 

calf’s birth was determined from previous sightings of the 

pregnant female followed by a sighting with a closely 

associated calf or a sighting of the mother with a suckling 

calf (Herzing 1997). 

Apparatus and procedure 

Video was recorded using various underwater cameras 

(Sony CCDV9 8-mm, Yashica KXV Hi8-mm with attached 

Labcore 76 hydrophone, Sony DCR-SC100 NTSC, or Sony 

DCR-PC110 NTSC Digital Video). Underwater video 

sequences were analyzed using focal follow (of the mother 

with and without the calf) as a sampling rule and continuous 

sampling as a recording rule. Video sequences from 

the long-term video archives from the Wild Dolphin Project 

Ò between 1991 and 2004 were assessed for the 

presence of benthic foraging events by individual mothers, 

either with or without their calves present, based on a 

behavioral ethogram designed to measure the individual 

benthic foraging behavior of the mother dolphins (see 

Fig. 2). Each benthic fish catch was broken down into a 

series of behaviors that made up a typical foraging event. 

For the purpose of this study, a foraging event was 

defined as the series of behaviors performed by the dolphin 

in order to catch the prey animal. For benthic feeding, the 

series of events was as follows: 

scanning ! rooting ! chase ! ingestion 

Scanning is observed when the dolphin moves its head 

horizontally or vertically repeatedly while performing a 

directional swim, and usually occurs near the sea floor and 

can be followed by a dig or fish catch (Miles and Herzing 

2003). Rooting or digging is observed when the dolphin 

inserts the rostrum into the sea floor or sandy bottom to dig 

the prey out of the substrate in the attempt to capture the 

prey. Chasing is observed as swimming in the direction of 

the prey object, as in pursuit of the prey. For our purposes, 

ingestion was defined as the food going into mouth and 

never being seen again. The categories of foraging 

behaviors measured were chase latency and number of 

body-orienting movements during pursuit. Chase latency, 

the length of time the prey was pursued, was operationally 

defined as the period of time when the fish appeared out of 

the sand (was rooted out) until the time of ingestion by the 

dolphin, or the dolphin no longer pursued prey (lost interest 

in prey). Body-orienting movements were measured to 

examine the dolphin’s attention to the prey object. A bodyorienting 

movement was measured in foraging events as a 

movement of the body reorienting in direction of prey 

object, often seen during pursuit of prey, from the time the 

prey was rooted out of the sand. Body-orienting 

movements were particularly interesting as they appeared 

to be exaggerated movements in the direction of the prey, 

which may be an attention-directed referential behavior 

similar to the spontaneous pointing observed by dolphins 

during experiments in captivity (Xitco et al. 2001). 

Figure 2 is a visual ethogram describing the sequence of 

the benthic foraging behavior (Miles and Herzing 2003). 

123


Fig. 2 Visual ethogram of 

select foraging behavioral 

events (Miles and Herzing 

2003). The visual ethogram 

includes the possible positions 

in which calves were observed 

during foraging events in 

relation to their mother and the 

sequence of behaviors for a 

benthic foraging event 

The segments from the video archives in which mothers 

were observed engaged in foraging behavior with or 

without their calves were then viewed and then examined 

for further criteria. Thirty-eight video segments were used 

in the study based on the selection criteria: fourteen video 

segments of mothers foraging with their calves present and 

24 video segments of those mothers foraging without their 

calves present. Videos were selected based on the presence 

of a target female performing an individual foraging event, 

as well as on the following designated video acceptance 

criteria: (a) the individuals were identifiable; (b) it was 

possible to identify the beginning and end of the chase 

sequence; (c) the prey was visible, or if the prey was not 

completely visible, it was possible to identify the position 

of the prey based on the behavior of the dolphin; (d) if the 

calf was present, the calf was in a nearby position (within a 

proximity of two body lengths) from which it was capable 

of observing its mother; and (e) if the calf was present, it 

was possible to identify the position of the calf relative to 

the mother during the foraging event. The position of the 

calf relative to the mother was recorded as Infant, Headunder-head, 

Echelon, Observation, or Other, with comments 

where necessary, as depicted in Fig. 2. 

The mothers’ foraging behaviors were then individually 

measured for the variables of chase latency and body-orienting 

movements, both when foraging alone (or with other 

juvenile or adult dolphins) and when foraging in the 

presence of their calves. Other variables, such as types of 

play involved in that foraging encounter, position of calf 

relative to the mother, directionality of the calf, age of the 

mothers and their calves, whether the mother eventually ate 

the prey; the prey species, when identifiable, were also 

recorded for each foraging event. 

Participants 

Positions of Calf Relative to Mother 

The foraging behaviors of nine mother dolphins were 

recorded both with (n = 14) and without (n = 22) their 

123 

Echelon Position Infant Position Head-under-head Observation Position 

Sequence of Behaviors for 

Benthic Foraging Event 

Position 

Individual Scanning Dig/Root Chase 

calves present. Ten different calves were observed with the 

nine mothers in the 14 foraging events, with one mother 

observed during separate events with two different calves. 

Calves ranged in age from neonate to 3 years old. All 

calves were observed to be nursing within the same field 

season as the foraging event. Ages of the mothers were 

known, or were estimated based on their age class. It is 

important to note that some foraging events without calves 

present (10 of the 22) occurred while the target female was 

still a juvenile (prior to sexual maturity); however, during 

those events, the ‘‘mothers to be’’ were already past the age 

of weaning and were independently foraging. The minimum 

age of any female during foraging events over the 

12-year period was 10 years for mothers foraging with 

their calves and 4 years for mothers-to-be foraging without 

calves present. Of the observations without calves present, 

four of the females were observed foraging as juveniles, 

prior to becoming mothers. Of the nine mothers observed, 

foraging events were observed for one female both when 

she was a calf with her mother, and later as a mother 

herself with her own calf. 

The video segments of the foraging events were shortened 

to within 1 min of the beginning and end of the 

foraging event and labeled with the foraging event number 

and the individuals involved. Segments were then watched 

by the first author and two independent observers to measure 

the desired behaviors. Of the 38 total foraging events 

measured, 32 were measured by the first author and two 

independent observers; the other six were measured by the 

first author and only one independent observer. For the 

measurement of chase latencies of foraging events, there 

was significant correlation between the author and the first 

independent observer, r 36 = 1.0, P \ 0.001, between the 

author and the second independent observer, r30 = 0.999, 

P \ 0.001, and between the first and second observer, 

r30 = 0.998, P \ 0.001. For the measurement of number of 

body-orienting movements, there was significant correlation 

between the author and the first independent observer,


Table 1 Mean chase latency of mothers with and without calf 

Mother Little Gash Mugsy Nassau Nippy PR1 PR2 Rosemole Trimy Uno Mean SD 

Mean chase latency 

without calf (n) 


with calf (n) 

Mean number of BOM 


Mean number of BOM 

with calf (n) 

r36 = 1.0, P \ 0.001, between the author and the second 

independent observer, r30 = 0.988, P \ 0.001, and 

between the first and second observer, r30 = 0.988, 

P \ 0.001. 

The videos were watched and timed using Windows 

Media Player version 10 on a Hewlett Packard laptop 

computer and a projector in order to enlarge the viewing 

area. Due to the restrictions of the media software used for 

editing and playing the video, a ‘‘second or less’’ rule was 

instituted for measurement of latencies in which the 

latencies appearing to be less than 1 s were rounded up to 

1 s in duration. 

Results 

Chase latencies 

Mean chase latencies for each of the nine mothers, both 

when foraging with and without their calves, is presented in 

Table 1. The mothers chased the prey significantly longer 

when their calves were present (M = 22.24 s, SD = 9.36) 

than when their calves were not present (M = 2.74 s, 

SD = 1.47), t8 = 6.57, P \ 0.001, d = 1.14. Mean chase 

latencies were longer when foraging with their calves than 

without their calves for each of the nine mothers (Fig. 3). 

Body-orienting movements 

5.6 (5) 2.25 (4) 2.00 (3) 2.00 (1) 2.17 (2) 4.00 (1) 1.67 (3) 4.00 (4) 1.00 (1) 2.74 1.47 

38.33 (1) 23.00 (2) 16.33 (2) 36.00 (1) 24.33 (3) 19.67 (1) 16.50 (2) 12.00 (1) 14.00 (1) 22.24 9.36 

0.80 (5) 0.00 (4) 0.33 (3) 0.67 (1) 0.50 (2) 0.00 (1) 0.00 (3) 0.25 (4) 0.00 (1) 0.28 0.31 

0.00 (1) 2.50 (2) 1.50 (2) 0.00 (1) 2.33 (3) 2.00 (1) 0.00 (2) 2.00 (1) 1.00 (1) 1.26 1.04 

Bold indicates mothers who performed significantly more body-orienting movements in the presence of their calves. Chase latencies were 

significantly longer for all nine mothers 

Mean number of body-orienting movements for each of the 

nine mothers, both when foraging with and without their 

calves, is presented in Table 1. The mothers made significantly 

more body-orienting movements when their calves 

were present (M = 1.26, SD = 1.04) than when their 

calves were not present (M = 0.28, SD = 0.31), t8 = 2.46, 

P = 0.04, d = 2.31. Six of nine mothers made more bodyorienting 

movements when foraging in the presence of 

their calves than when not foraging with their calves. 

45.00 

40.00 

35.00 

30.00 

25.00 

20.00 

15.00 

10.00 

5.00 

0.00 

38.33 

5.60 

23.00 

Chase Latency of Mothers 

16.33 

36.00 

Cross-generational comparisons 

Two consecutive generations of the mother/calf pairs in the 

study showed the same altered foraging behavior. In the 

first generation, one mother, Nippy, and her calf, Nassau, 

demonstrated the presumed teaching behavior. In the second 

generation, Nassau, now a mother, showed the same 

altered foraging behavior as her mother with her calf, 

Neptune. 

Foraging with non-calf individuals 

Of the foraging events without calves, three mothers were 

observed foraging both alone and with other individuals 

that were not calves, at least juveniles or older. The chase 

latencies and body-orienting movements for these mothers 

were compared for the two conditions (alone and with noncalf 

individuals). There were too few subjects (n = 3) to 

perform a statistical test; however, the chase latencies of 

these three mothers foraging alone (M = 1.33, SD = 0.58) 

were comparable to the chase latencies of these same 

mothers foraging with non-calf individuals (M = 3.44, 

SD = 1.50), and both were much lower than the chase 

24.33 

2.25 2.00 2.00 2.17 

Mother 

19.67 

4.00 

Mothers Chasing 

With Calves 

Mothers Chasing 

Without Calves 

Fig. 3 Mean chase latencies of mothers foraging with and without 

their calves present 

16.50 

1.67 

12.00 

4.00 

14.00 

1.00 

123


latencies of those mothers foraging with their calves 

present (M = 17.56, SD = 6.26). Additionally, the number 

of body-orienting movements of these three mothers foraging 

alone (M = 0.17, SD = 0.29) was comparable to the 

number of body-orienting movements when they were 

foraging with non-calf individuals (M = 0.33, SD = 0.58), 

and both were less than the number of body-orienting 

movements of those mothers foraging with their calves 

present (M = 1.94, SD = 0.42). 

Additional analyses 

The differences observed for chase latencies and number of 

body-orienting movements could not be attributed to prey 

type, as there were no significant differences in the foraging 

behaviors between prey species. Prey species were identified 

for 14 observations. When foraging with calves present, 

mothers were observed foraging for Snakefish (family 

Synodontidae), n = 5, flounder (family Bothidae), n = 2, 

and razorfish (family Clinidae), n = 1. The mean chase 

latencies, M Snakefish = 19.0 (SD = 11.03), M Flounder = 20.5 

(SD = 14.85), MRazorfish = 25.0 (SD = 0.0), and number 

of body-orienting movements, MSnakefish = 0.6 (SD = 

0.89), M Flounder = 25.0 (SD = 2.12), M Razorfish = 3.0 

(SD = 0.0), were comparable for all three species of prey 

when foraging with calves present. Both snakefish, n = 9, 

and flounder, n = 4, were observed as prey types when the 

females were observed foraging without calves present. The 

mean chase latencies, MSnakefish = 2.22 (SD = 1.09), 

M Flounder = 3.83 (SD = 3.57), and number of body-orienting 

movements, MSnakefish = 0.5 (SD = 0.76), MFlounder = 

0.5 (SD = 0.58), were comparable for both species when 

foraging without calves present, and both were lower than 

when foraging with calves present. 

Additionally, individual foraging events of dolphins not 

included in the study observed foraging for either snakefish 

or flounder were collected and analyzed. Ten foraging 

events each for catches of snakefish and flounder using 

both dolphins in the present study and dolphins not used in 

the study were randomly selected, and their corresponding 

chase latencies and number of body-orienting movements 

were compared between the two types of prey using an 

independent samples Student’s t-test. There were no significant 

differences found between the two types of prey for 

either chase latencies, (M flounder = 4.60, SD flounder = 3.86, 

Msnakefish = 2.80, SDsnakefish = 1.62) t18 =-1.36, 

P = 0.19, or number of body orienting movements for 

dolphins foraging without calves present, (M flounder = 0.50, 

SDflounder = 0.71, Msnakefish = 0.37, SDsnakefish = 0.48) 

t18 =-0.49, P = 0.63. This supports the conclusion that 

the observed differences in this study for mothers foraging 

with calves present would not likely be due to the type of 

prey, as chase latencies and the number of body-orienting 

123 

movements do not normally vary significantly between 

snakefish and flounder, the two main types of prey observed 

being caught by mother dolphins in this study. 

To assess possible effects of age of calf and age of 

mother on the dependent measures, correlations with each 

dependent measure were computed separately with the age 

of the calf and the age of the mother for the foraging events 

when the calf was present. Correlations between age of the 

calf and chase latency, r13 = 0.37, P = 0.10, and number 

of body-orienting movements, r13 =-0.30, P = 0.15, 

were both nonsignificant. Correlations between mother’s 

age and number of body-orienting movements were significant, 

r13 =-0.47, P = 0.046, with older mothers 

making fewer body-orienting movements than younger 

mothers. The correlation between mother’s age and chase 

latencies was not significant, r13 = 0.01, P = 0.48. When 

comparing the foraging behaviors to the age of the mothers 

when the calves were not present, correlations with both 

chase latencies r23 =-0.07, P = 0.73, and number of 

body-orienting movements, r 23 =-0.12, P = 0.58, were 

nonsignificant. The foraging behaviors of eight of the nine 

mothers without calves were compared between those 

females observed as juveniles and those observed as adults, 

with three mothers being observed foraging as juveniles 

and five mothers observed foraging as adults. 1 There were 

no significant differences between chase latencies, t (6) =- 

0.10, P = 0.92, or number of body-orienting movements, 

t(6) =-0.12, P = 0.91, of females observed foraging 

when juveniles or adults. 

Additionally, of the nine mothers observed in this study, 

three of the mothers, Little Gash, Mugsy, and PR2, were 

observed foraging both with and without their calves 

present during the same year, and each of those three 

mothers being observed foraging both with and without 

calves during the same field encounter. The mean chase 

latencies for these three mothers are compared in Table 2. 

The chase latencies were much longer foraging with calves 

than foraging alone for the mothers at the same age and 

comparable to the mean chase latencies of foraging alone 

for the mothers at an earlier age. 

The position of the calf during the chase period was 

indicated for each of the foraging events (N = 14) in which 

the calf was present. Although some foraging events 

involved multiple calf positions, the observation position 

1 One mother, Little Gash, was observed foraging without her calf 

present both as an adult and as a juvenile. When group means were 

compared including Little Gash there were no significant differences 

between adults and juveniles for either chase latencies, t(8) = 0.05, 

P = 0.96, or body-orienting movements, t (8) = 0.41, P = 0.69. Both 

the mean chase latencies, M A = 3.67 and M J = 6.89, and mean 

number of body-orienting movements, M A = 0.5 and M J = 1.0, for 

Little Gash were comparable as an adult and as a juvenile.


Table 2 Maternal age 

comparison for mean chase 

latency and number of bodyorienting 

movements 

was found to be the most common, taking place in 11 

(79%) of the foraging events. Head-under-head position 

was present in one of the foraging events, Echelon was 

present in two foraging events, and Infant position was 

seen in one foraging event. Only Infant, Echelon, and 

Observation positions were seen solely in an individual 

foraging event, with one, one, and nine occurrences, 

respectively. 

For the foraging events collected in which the ingestion 

by the mother was known (as seen by video or first-hand 

account), there were five events, one event each for five of 

the nine mothers, in which the prey was not eaten. Each of 

these foraging events occurred when the mothers’ calves 

were present (36% of the total events with calves). In 

addition, the calves were allowed to pursue the prey in each 

of these events and were confirmed to have eaten the prey 

in three of the foraging events, despite the fact that they 

were still nursing and not dependent upon fish for food. 

Four of the nine mothers were observed eating the prey in 

seven of the fourteen events in which calves were present. 

In two of the events in which calves were present it was not 

known whether the prey was eaten. 

Discussion 

Encounter dates 

by mother 

The nine mother dolphins observed in this study displayed 

significantly longer chase latencies and made significantly 

more body-orienting movements when foraging in the 

presence of their calves than when foraging alone. The 

chase latency data are particularly impressive. Mean chase 

latencies were eight times longer for the female dolphins 

when foraging with their calves (22.24 s) than without 

them (2.74 s). As illustrated in Fig. 3, the distributions 

were non-overlapping, with every mother having a longer 

latency when foraging with her calf than when foraging 

without her calf. 

Although differences were not as robust for the bodyorienting 

movements, the overall number of body-orienting 


with calf (n) 



Mean BOM 

with calf 

Mean BOM 

without calf 

Little Gash 

30 May 2000 38.33 (1) 3.67 (2) 0.00 (1) 0.50 (2) 

27 May 1991 

Mugsy 

– 4.00 (2) – 1.50 (2) 

29 August 1993 34.00 (1) 2.00 (1) 5.00 (1) 0.00 

13 May 2000 – 4.00 (1) – 0.00 

11 August 2000 

PR2 

12.00 (1) – 0.00 – 

14 June 1994 19.67 (1) 4.00 (1) 2.00 0.00 

movements was significantly greater when the mothers 

were foraging with their calves than when foraging alone, 

with six of nine mothers displaying this pattern. Previous 

research has shown that dolphins are capable of understanding 

the human gesture of pointing (Herman et al. 

1999; Pack and Herman 2004), and of producing spontaneous 

referential gestures in artificial experimental 

contexts (Xitco et al. 2001). Although these body-orienting 

movements were not demonstrated by all sampled mothers, 

the present results may be evidence of referential gesturing 

in a more ecologically valid context. 

In addition to the elongated chase and presumed referential 

body-orienting movements in the direction of the 

prey, the altered foraging behavior in the presence of the 

calf appeared more exaggerated when compared to the 

mothers foraging alone or with another non-calf dolphin. 

Mothers seemed to toy with their prey, making it more like 

play behavior and less like the typical foraging behavior of 

mothers observed foraging without their calves present, 

similar to descriptions of possible teaching of predatory 

behavior from other species such as cats and killer whales 

(Caro and Hauser 1992; Guinet and Bouvier 1995). Some 

of the mothers were observed letting the prey swim away 

and then digging them back out of the sand, sometimes 

multiple times, after initially digging the fish out of the 

sand, and also make jawing motions in the direction of the 

prey. Mothers also allowed the seemingly attentive calves 

to participate in the chase, and calves were observed eating 

the prey in three of the events. Although 4 of the 9 mothers 

were observed eating the prey in 7 of the 14 events, all of 

the mothers were observed allowing the calves to participate 

and made little to no effort in these events to consume 

the prey, only seemingly facilitating the calves’ experience 

in chasing the prey. Despite the altered foraging behavior, 

mothers were never observed losing the prey. In all events 

in which ingestion of the prey was observed, either the 

mother or the calf ate the prey, or the mother made no 

further attempts to ingest the prey and left the prey to the 

calf to chase. This altered foraging behavior can be 

123


observed in the online supplemental movies S1 and S2 

which exemplify the markedly different foraging behavior 

of an adult female foraging alone (S1) with the foraging 

behavior of a mother foraging in the presence of her calf 

(S2). 

There was a potential cost of the alteration of the 

mothers’ foraging behavior in their calves’ presence. The 

elongated chase time allowed more opportunity for prey to 

escape, although this did not occur in any of the events 

observed, as well as taking time away from catching 

additional fish or other activities. Instead of the typical grab 

and ingestion, these mothers toyed with their prey as their 

calves watched, and, as mentioned above, sometimes even 

avoided ingestion in these altered foraging events. Often in 

teaching, the model will provide an exaggerated or elongated 

version of the typical behavior in front of the naïve 

observer, much as the mother chimpanzees observed in 

Boesch’s (1991) work. These exaggerated foraging 

behaviors may provide a window of opportunity for the 

calves to observe, and possibly learn from, the example 

provided by their mothers, and thus be worthy of the extra 

time and energy put forth by the mothers at a cost to 

themselves in order to help ensure the success of their 

offspring. 

An alternative explanation for the altered foraging 

behavior may be that the mothers were distracted by their 

calves, resulting in longer chase latencies and exaggerated 

movements to compensate for their divided attention. 

However, we do not believe this to be the cause of the 

altered foraging behavior for a few reasons. First, three of 

the nine mothers observed in the present study demonstrated 

the ability of dolphin mothers to forage without 

distraction even when their calves were in the nearby 

vicinity, but not directly observing the mothers. These 

three mothers, Little Gash, Mugsy, and PR2, were 

observed foraging both with and without their calves 

present during the same field encounter. These mothers 

only altered their behavior when the calves were 

observing the mother, but not during the fish catches in 

which the calves were within the vicinity and not 

observing. Table 2 compares the means for those events, 

in which the mean chase latencies were much longer 

foraging with calves than foraging alone during the same 

field encounter and comparable to the mean chase latencies 

of foraging alone during separate field encounters. 

These data suggest that the calves’ being merely nearby is 

not a distraction for the mothers, but instead the altered 

foraging behavior only occurred when the calves were 

directly observing the mothers’ behavior. If the calves 

were a distraction for the mothers, the altered foraging 

behavior should have occurred whenever the calves were 

within the vicinity, regardless of whether the calves were 

directly observing the mothers. 

123 

Second, Atlantic spotted dolphins participate in alloparenting, 

which permits mothers to frequently forage 

separately from their calves (Herzing 1996). If the mother’s 

nutritional needs are being met in the absence of their calf 

with the help of alloparenting, this would enable more time 

and energy on the part of the mother for altered foraging 

events for teaching when the calf is present. Additionally, it 

would not be advantageous for the mother to forage with 

the calf present solely for her nutritional purposes if there is 

an alloparent available. In this study, there were potential 

alloparents, juvenile or adult female dolphins, available in 

all 14 of the calf-present events that would have permitted 

the mothers to forage without distraction, which is often 

observed in Atlantic spotted dolphins (Herzing 1996), 

including the events for the previously mentioned three 

mothers observed foraging with and without calves during 

the same field encounter. 

Third, young dolphin calves are very precocious and the 

calves in the observed foraging events appeared attentive 

and interactive. Some of the evidence for the calves’ 

attentiveness to the mothers’ foraging behavior was 

observed through the calves’ positions relative to the 

mothers, which was indicated during the chase period for 

each of the foraging events in which the calf was present. 

Although previous research (Mann and Smuts 1999) has 

shown that dolphin calves in the wild, and in captivity 

spend the majority of their time in infant or echelon position 

until the time of weaning, calves were most commonly 

found during the chase period in the observation position 

relative to their mothers in which the calf was potentially 

exposed to both visual and acoustic information and in 

which calves appeared attentive to both the mother and the 

prey 2 (Figure 2). 

Additionally, the calves were allowed to pursue the prey 

in five of the foraging events and were confirmed to have 

eaten the prey in three of the events, despite the fact that 

they were still nursing and not dependent upon fish for 

food. It is important to note that the only time when the fish 

was not ingested was when the mothers were foraging with 

their calves as part of their altered foraging behavior. The 

prey was always consumed when foraging alone or in the 

presence of a non-calf dolphin. This is potentially a costly 

behavior for the mother as she is depriving herself of calories 

needed to nourish her still nursing calf by allowing 

2 It is important to note that research in captivity (Pack and Herman 

1995) has demonstrated the ability of dolphins to perceive and 

recognize objects through either vision or echolocation. In addition, 

their perceptions are readily shared or integrated across the senses, 

regardless of which modality the dolphin originally perceived the 

external stimuli. However, the sounds emitted from the dolphins were 

not measured in the present study, but should be looked at in future 

research in order to determine what sensory information the calf is 

receiving.


the prey to escape or allowing the calf to eat the prey, as 

well as the energy to play with the prey rather than just 

eating it quickly and efficiently herself. It would be more 

efficient and less costly for the mothers to have simply 

caught and consumed the fish, or perhaps to have left the 

calf in the care of an alloparent, as opposed to this altered 

foraging behavior observed in these events. 

Furthermore, the chase latencies and foraging behaviors 

were drastically different with their calves present, not just 

with the longer latencies but also with the presumed referential 

behaviors toward the prey objects and allowing the 

still nursing calf to participate, which would be more 

indicative of social learning. If the calves were merely a 

distraction, the mothers could have either immediately 

consumed the prey or disciplined the calf, as previously 

observed by mothers in the population for undesirable 

behaviors (Miles and Herzing 2003), rather than allowing 

the calf to participate. Therefore, because the calves 

appeared attentive, interacted with the prey and the mother, 

and appeared to need little care during the event, they were 

not likely a distraction to the mother. 

Reciprocally, the mothers may have been altering their 

foraging behavior because their calves were attentive, so 

that a calf’s attention may have stimulated the altered 

maternal foraging behavior. Further analysis into the 

calves’ behavior is warranted and may also elucidate the 

exact learning mechanism at play on behalf of the calf. 

For the majority of the mothers, there was a difference 

in maternal age between the events observed foraging 

without their calves compared to the events foraging with 

their calves. It is not likely that the age differences, or 

resulting level of experience would have resulted in the 

observed differences in chase latencies and number of 

body-orienting movements. Rather, an older or more 

experienced dolphin should be expected to have quicker 

chase latencies and fewer body-orienting movements due 

to increased efficiency, not the longer latencies and 

increased number of body-orienting movements as 

observed here. Additionally, of the nine mothers observed 

in this study, three of the mothers, Little Gash, Mugsy, and 

PR2, were observed foraging both with and without their 

calves present during the same year, and each of these 

three mothers were observed foraging both with and 

without calves during the same field encounter. For these 

three mothers, mean chase latencies were much longer 

foraging with calves than foraging alone at the same age 

and comparable to the mean chase latencies of foraging 

alone at an earlier age (Table 2). This suggests that there 

was not a difference in foraging behavior due to difference 

in age or experience, but rather due to the presence of their 

calves. 

There were also no significant differences for chase 

latencies or number of body-orienting movements for the 

prey species observed in this study: thus the altered foraging 

behaviors were also not likely due to the difficulty of 

catching a specific type of prey. 

The three episodes in which a target dolphin was 

observed foraging with a non-calf individual, juvenile in 

age or older, produced chase latencies and number of bodyorienting 

movements comparable to when these dolphins 

foraged alone, and both substantially different from the 

levels of behavior observed when these dolphins foraged 

with their calves present. This suggests that the change in 

behavior was not merely a social phenomenon seen in the 

presence of other individuals, but instead reflects teaching 

behavior targeted at a naïve observer. However, the naïve 

observers in this study were presumably the calves of the 

observed mothers. Future research is needed to explore if 

these same mothers or other alloparents also exhibit similar 

altered foraging behavior when in the presence of other 

naïve observers that are not their offspring. 

This altered foraging behavior on behalf of the mothers 

may be a valuable social learning mechanism for Atlantic 

spotted dolphins. The mothers in the study clearly altered 

their typical foraging behavior in the presence of their 

calves at a potential cost to themselves due to the exaggerated 

behavior, as well as sometimes foregoing ingestion 

of the prey. However, as per Caro and Hauser’s definition 

of teaching, the observer must benefit from the model’s 

altered behavior, in this case through more rapid or skillful 

acquisition of foraging behavior. In dolphin society this 

skill would be essential, as mothers give birth approximately 

every 3 years, at which time the older calf would 

become weaned and rely more on independently caught 

fish. It is advantageous for the mother to ensure the success 

of her offspring, presumably by investing her time and 

energy into the calf’s foraging capabilities before the calf 

is weaned. Weaning is a gradual process in spotted dolphins, 

and although the calves were not dependent upon 

fish for food, consuming the fish may have been an 

important part of the development of the calves’ foraging 

behavior, perhaps because it reinforced the social-learning 

process. 

Future research is warranted to explore the development 

and skillfulness of the young calf’s pre-weaning foraging 

capabilities in order to examine the full effect of the 

mother’s presumed teaching efforts. If this is true teaching 

behavior, the calf will derive some benefit from observing 

the mother’s altered foraging behavior. Additionally, a 

comparison is needed to compare the calves of teaching 

and non-teaching or less attentive mothers. However, 

because all of the mothers observed in this study demonstrated 

the altered foraging behavior, it may be difficult to 

assess the consequences of naturally occurring individual 

differences in the mothers’ foraging behavior on the calves. 

Although the full benefit for the calf is unknown, it seems 

123


that the calf is indeed the target of this altered behavior, 

which was observed only in the presence of the calf. 

Additionally, further research is needed into the calf’s 

behavior and attention to the mother. Future research can 

hopefully clarify if the calf is indeed attentive to the 

mother’s potential teaching behavior to gain something 

from the experience, as well as clarify what mechanism 

the calves may be using to learn from the mothers, such 

as imitation, stimulus enhancement, or local enhancement. 

Data from this study, such as the calves being 

predominantly in the observation position relative to the 

mother during the events, some of the calves chasing and 

ingesting the fish, and the calves’ interactions with both 

the mothers and prey objects, may be evidence that the 

calves were attentive to the mothers’ altered foraging 

behavior and support the argument for teaching. Future 

data from the calf behavior will also hopefully 

strengthen our argument that the altered maternal foraging 

behavior may be an example of teaching. The data 

from the calf behavior are currently being collected and 

analyzed as part of a separate ongoing project and will 

be available for future publication. Despite this drawback, 

we believe that this study detailing the altered 

foraging behavior of the mothers is a significant finding 

in the area of animal cognition, even without data on the 

calf behavior. 

Despite previous research that has shown that dolphins 

pass mirror self-recognition tests (Reiss and Marino 2001), 

understand referential pointing (Herman et al. 1999), and 

spontaneously use referential gesturing in captive situations 

(Xitco et al. 2001), further evidence is needed before 

attributing theory of mind to dolphins, which some 

researchers argue is required for true teaching (Tomasello 

et al. 1993). Regardless of the lack of conclusive evidence 

supporting theory of mind in dolphins, the perspectivetaking 

abilities by dolphins supported by previous research 

(Herman et al. 1999; Xitco et al. 2001) might be sufficient 

for the presumed teaching behavior shown here. Although 

the cognitive abilities behind the clear alteration of foraging 

behavior of the mother dolphins in the presence of their 

calves are yet to be determined, the observed teaching 

behaviors in dolphins are nonetheless remarkable. Mother 

dolphins provide opportunities for calves to observe foraging 

behaviors, and sometimes even provide opportunities 

for calves to practice foraging. Teaching, then, may be an 

important way in which aspects of cetacean social learning 

and possibly culture are transmitted from one generation to 

the next. 

Acknowledgments We would like to thank Stan Kuczaj and Jesse 

Bering for their helpful comments on earlier drafts of this manuscript, 

and John Bender, Miley Fishero, Megan Rothrock, Melissa Ingui, 

Wisline Shepherd, Sheryl Spencer, and the Wild Dolphin Project for 

their assistance on the project. 

123 

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Aquatic Mammals 2009, 35(1), 62-71, DOI 10.1578/AM.35.1.2009.62 

Characterization of Resting Holes and Their Use by the 

Antillean Manatee (Trichechus manatus manatus) 

in the Drowned Cayes, Belize 

Marie-Lys C. Bacchus, 1, 2 Stephen G. Dunbar, 1, 2 3, 4 

and Caryn Self-Sullivan 

1 Department of Earth and Biological Sciences, Loma Linda University, Loma Linda, CA 92350, USA; 

E-mail: mlbacchus@gmail.com 

2 Marine Research Group, Loma Linda University, Loma Linda, CA 92350, USA 

3 Texas A&M University, Department of Wildlife and Fisheries, College Station, TX 77843, USA 

4 Sirenian International, Inc., 200 Stonewall Drive, Fredericksburg, VA 22401, USA 

Abstract 

In the Drowned Cayes area of Belize, manatees 

(Trichechus manatus manatus) are commonly 

observed resting in depressions in the substrate, 

locally referred to as manatee resting holes. To 

understand why manatees prefer locations with 

resting holes, the physical and environmental 

attributes of the depressions were characterized 

and diurnal and nocturnal use by manatees at four 

resting hole sites were documented over two summers. 

Twelve resting hole sites were compared 

with 20 non-resting hole sites in the Drowned 

Cayes, using water depth, substrate type, vegetation, 

water velocity, salinity, and water temperature. 

Four resting holes were chosen for repeated 

diurnal and nocturnal observations, during which 

sea and weather conditions were recorded in addition 

to the presence/absence of manatees. Resting 

holes were significantly deeper and had slower 

surface water velocity than areas without resting 

holes. A total of 168 point scans were conducted 

over 55 d, resulting in 39 manatee sightings over 

two summers. There was a significant difference 

in the number of sightings between research years 

and between day and night scans. Given the large 

number of resting holes in the Drowned Cayes, 

many of which are in sheltered areas with slow 

currents, it is possible that manatees select these 

spots based on the tranquility of the water and 

environment. The combination of slow currents, 

protection from waves, low numbers of boats, and 

nearby seagrass beds would make these ideal resting 

areas. These findings have implications for the 

conservation of important manatee habitat. 

Key Words: Antillean manatee, Trichechus 

manatus manatus, Belize, resting holes, nocturnal, 

diurnal, conservation, habitat, sightings 

Introduction 

The West Indian manatee (Trichechus manatus) 

is one of only four extant species in the Order 

Sirenia, which is the only group of herbivorous 

marine mammals. The species is subdivided into 

Florida (T. m. latirostris) and Antillean (T. m. 

manatus) manatees (Domning & Hayek, 1986). 

The 2007 IUCN Red List categorized the species 

as “vulnerable” and both subspecies as “endangered” 

(Deutsch et al., 2007). 

West Indian manatees inhabit rivers, lakes, 

lagoons, and coastal marine environments from 

southeastern North America to northeastern 

South America, including Central America and 

the Caribbean (Lefebvre et al., 2001; Deutsch 

et al., 2007). Within Central America, aerial 

surveys have indicated that the cayes east of 

Belize City are important manatee habitat (Auil, 

2004). Manatees osmoregulate and thermoregulate 

behaviorally by moving between activity 

centers (Deutsch et al., 2007). They can survive 

in marine environments for extended periods of 

time; however, a dependence on periodic access to 

fresh water is presumed (Ortiz et al., 1998, 1999; 

Deutsch et al., 2003). Thus, when found in marine 

or coastal environments, they tend to be located 

near freshwater sources (Powell et al., 1981; 

Powell & Rathbun, 1984; Rathbun et al., 1990; 

Olivera-Gomez & Mellink, 2005). Proximity to 

seagrass beds is another important characteristic in 

determining manatee habitat preference (Hartman, 

1979; Powell et al., 1981; Deutsch et al., 2003). In 

Chetumal Bay, Mexico, manatee movements were 

most strongly associated with food distribution 

(Axis-Arroyo et al., 1998), and in Florida, aerial 

surveys indicated a strong association between 

location of manatees and distribution of seagrass 

beds. Work by Kinnaird (1985) and Provancha 

& Hall (1991), showed manatee density was 

positively correlated with seagrass abundance

(Halodule wrightii and Syringodium filiforme) in 

the northern Banana River, Florida. Some of the 

most important manatee food items around the 

cayes of Belize are turtle grass (Thalassia testudinum), 

manatee grass (S. filiforme), and shoal grass 

(H. wrightii) (LaCommare et al., 2008). There 

is also evidence that resting areas for cows and 

calves, as well as travel corridors between activity 

centers, may be critical habitats for manatees 

(Packard & Wetterqvist, 1986; Deutsch et al., 

2007). Major threats to survival of the species 

include habitat degradation and loss, illegal hunting, 

boat strikes, entanglement in fishing gear, 

entrapment in water control structures, pollution, 

disease, and human disturbance (Deutsch et al., 

2007). 

Conservation of this species is dependent on 

conservation of habitat that meets the requirements 

described above. Compared to osmoregulation, 

thermoregulation, and foraging requirements, 

little is known about manatee resting 

behavior and the importance of resting habitat 

for conservation of the species. Hartman (1979) 

and Bengtson (1981) described Florida manatees 

as arrhythmic, spending most of their time feeding, 

resting, idling, cruising, and socializing with 

no correlation of activity with time of day. The 

hypothesis that Florida manatees lack a daily 

activity pattern is supported by two lines of evidence: 

(1) similar nocturnal and diurnal behaviors 

(Hartman, 1971) and (2) lack of a pineal body 

(Ralph et al., 1985; Wally Welker, pers. comm.). 

Hartman (1979) also found that Florida manatees 

devoted considerable time to resting behavior 

with no strict preference for resting sites, which 

included limestone shelves, oyster bars, and vegetation. 

However, more recent studies indicated 

that manatees have a diurnal or nocturnal preference 

for resting in different areas of Florida. For 

example, during winter along the Atlantic coast, 

manatees rested in canals during the day and foraged 

at night (Deutsch et al., 2003). In Sarasota, 

they will bottom-rest in deeper areas during the 

winter when it is colder, and then will switch to 

surface resting when temperatures increase (Sheri 

W. Barton, pers. comm.). Along the Gulf Coast 

during winter months, manatees use the warm 

water springs in Crystal River to rest at night and 

often travel downriver to feed on Ruppia during 

the day (Reep & Bonde, 2006). Similar evidence 

of resting during certain times has been found for 

other manatee species. Observations of a solitary 

Amazonian manatee (T. inunguis) suggested an 

activity pattern with the individual sleeping for the 

first half of the night (Mukhametov et al., 1992). In 

areas with high instances of hunting, there is evidence 

that manatees (including the West African 

manatee, T. senegalensis) may have shifted to 

Resting Holes of the Antillean Manatee in Belize 63 

greater nocturnal activity and a more diurnal resting 

pattern (Rathbun et al., 1983; Reynolds et al., 

1995; Powell & Kouadio, 2006). 

Manatees also appear to follow patterns in 

both resting times and resting sites. During low 

tides and the dry season in Venezuela and Costa 

Rica, they often take refuge in holes or channels 

in the rivers that range from 6 to 12 m in depth 

(O’Shea et al., 1988; Smethurst & Nietschmann, 

1999). Anecdotal observations suggest that manatees 

in Nicaragua rest in quiet, sheltered, deep 

water during most of the day, leaving to feed only 

during the night, early morning, and late afternoon 

(Jiménez, 2002). In Belize, resting behavior 

has been correlated with the presence of a “resting 

hole” (CSS & K. LaCommare, unpub. data), 

which has also been identified as a significant 

factor for predicting the presence of manatees at 

54 permanent sampling points in the Drowned 

Cayes during a daytime study (LaCommare et al., 

2008). The objectives of this study were to determine 

what factors influence the use of previously 

identified resting holes by manatees and whether 

manatees use the resting holes more often during 

the day or at night. 


Study Area 

The study was conducted over the summers of 

2005 and 2006 in the Drowned Cayes of Belize 

(located about 15 km east of Belize City at N 17° 

28.0', W 88° 04.5'; Figure 1), which are a labyrinth 

of mangrove islands approximately 13 km 

long separated by lagoons, coves, and bogues 

(channels that separate the mangrove cayes both 

within and between ranges) (Ford, 1991). The 

ecosystem is marine with an average salinity of 

35 ppt, although a few low salinity sites have been 

identified (CSS, unpub. data). Extensive seagrass 

beds surround these islands, making them excellent 

foraging habitats for manatees. 

Characterization of Resting Holes 

For the purpose of this study, a resting hole is 

defined as an area where manatees have consistently 

been observed in a resting state of behavior. 

Twelve resting holes in the Drowned Cayes 

were chosen as a subset of 54 permanent scanpoints 

where manatees have been studied since 

2001 (LaCommare et al., 2008). The holes were 

characterized by depth using a HondexTM digital 

depth sounder (Forestry Suppliers), substrate 

(mud or sand), and vegetation (seagrass, algae, 

none). Water temperature (using a Taylor ® classic 

instant read pocket digital thermometer), salinity 

(using a WP-84 conductivity-TDS-temperature 

meter from TPS Pty), and water velocity (using

64 Bacchus et al. 

Figure 1. Map of Belize (inset) and the Drowned Cayes in relation to Belize City 

a General Oceanics mechanical flowmeter model 

2030R from Forestry Suppliers; speed range 

10 cm/s to 7.9 m/s) were measured at three points 

in the water column—surface, mid-water, and 

bottom—above each resting hole. Latitude and 

longitude were recorded above the deepest point 

of each resting hole with a GPS (Garmin ® Global 

Positioning System 12 Personal Navigator ® ). For 

comparison, these variables were measured at 20 

non-resting hole scan-points.

Diurnal and Nocturnal Scans 

Four of the 12 resting holes were selected for systematic 

diurnal and nocturnal scans during the summers 

of 2005 and 2006: B1Co, 30 CCo, 31 CLa, 

and 50 GiCr. Two 30-min scans focused around 

a fixed survey point were conducted at each site 

daily, once between 1000 and 1500 h, and again 

between 1900 and 0000 h (sunset occurred ~1900 

h). This survey method is referred to as a point 

scan (Self-Sullivan et al., 2003; LaCommare et al., 

2008). The order in which sites were scanned was 

randomly chosen by the researcher each day. An 

8-m fiberglass boat with an outboard engine was 

used with observers standing in the boat during 

the scans. As the scan-point was approached, the 

boat engine was turned off, a long pole used to 

pull the boat to the scan-point, and the boat tied 

to the grounded pole. During each point scan, the 

research team continuously searched for manatees 

by performing 180° visual scans from different 

points on the boat and listening for breaths (for 

detailed point scan methods, see Bacchus, 2007; 

Self-Sullivan, 2008). Nocturnal scans were performed 

in the same manner as diurnal scans, with 

the addition of spotlights to help sight manatees. 

Data collected during each point scan included 

manatee sighting (a sighting was defined as detection 

of one or more manatees during the 30-min 

scan), sea and weather conditions, tidal state, sea 

surface temperature (SST), salinity, and air temperature. 

Data Analyses 

All statistics were run in SPSS, Version 13.0, 

with α = 0.05. Summary statistics were run for 

resting hole characterizations and data collected 

during the diurnal and nocturnal scans. The variable 

“depth” was adjusted to account for tides 

using predictions from a Belize City tide chart 

and visually verified via water level marks on the 

mangrove roots during each scan. The variable 

“water velocity” was calculated from 5-min rotation 

counts using the formula provided by General 

Oceanics: 


(1) 

where 26,873 is the rotor constant, and 999,999 

is the maximum number of rotations divided 

by 5 min and multiplied by 60 s to obtain cm/s. 

T-tests were used to test for differences in depth 

and water velocity between areas with and areas 

without resting holes. Water velocity was ranked to 

adjust for unequal variances to meet assumptions 

of normality. T-tests were also run to analyze SST 

and salinity between the two years, and between 

day and night. Log likelihood ratio tests (G 2 ) were 

run to test for variance in the number of manatee 

sightings between the two years and between day 

and night. A step-wise, logistic regression was 

used to detect any associations between specific 

habitat factors and manatee sightings. Factors 

included location, tide, salinity, SST, day/night, 

and year. 

Results 


There was a significant difference in water depth 

between resting holes and scan-points without 

resting holes (t(15) = 4.541, p < 0.001) with a mean 

difference of 1.5 ± 0.32 m. Mean water depth for 

resting holes was 3.5 ± 0.30 m (n = 12; range: 2.0 

to 5.2 m) compared with non-resting hole areas 

with a mean depth of 2.0 ± 0.12 m (n = 20; range: 

1.4 to 3.3 m) (Table 1). 

Mean surface water velocity for resting holes 

was 0.89 ± 0.51 cm/s (n = 10; range: 0 to 5.20 

cm/s). Non-resting hole areas had a mean surface 

water velocity of 4.26 ± 1.14 cm/s (n = 20; range: 

0.01 to 17.12 cm/s) (Table 1). These represent a 

significant difference in surface water velocity 

between resting holes and areas without resting 

holes (t(28) = -2.880, p = 0.008). All of the holes 

characterized had little or no bottom vegetation. 

The substrate in and around the resting holes 

tended to be a silty mixture of mud and sand, 

which was easily compressed and resuspended. 

Sparse to abundant vegetation was found proximal 

to resting holes, usually consisting of shoal 

grass (Halodule sp.), macro algae (Halimeda and 

Penicillus sp.), and/or turtle grass. One of the resting 

holes also had a visible “manatee highway” to 

and from the hole where manatees swim or paddle 

along the bottom with their forelimbs and/or torso 

in contact with the seafloor. This deeper, narrow 

channel started at the entrance of the small cove 

containing the resting hole near the mangroves 

and followed a straight path to the deepest part of 

the resting hole. 

Diurnal and Nocturnal Scans 

A total of 168 scans were conducted at four resting 

hole sites during the summer of 2005 (n = 81) 

and the summer of 2006 (n = 87). Manatees were 

sighted during 39 scans—26 times in 2005 and 13 

times in 2006 (Figure 2)—representing a significant 

difference in the number of sightings at these 

four sites between years (G 2 (1) = 7.01, p < 0.01). 

Table 2 shows that SST and salinity were significantly 

different for these four points between 

years (SST: t(158) = 3.292, p = 0.001; salinity: t(166) = 

20.629, p < 0.001). There was no significant difference 

in air temperature between years.


Table 1. Descriptive statistics of environmental characteristics of areas without and with resting holes; means are reported 

with ± 1 SE. 

There were 107 day scans and 61 night scans 

over both summers, with 34 day sightings 

and 5 night sightings (Figure 3), resulting in a 

significant difference in the number of manatee 

sightings between day and night (G 2 (1) = 13.68, p < 

0.001). Table 3 shows that both sea surface and air 

temperatures were significantly different between 

day and night, although surface salinity was not 

significantly different between day and night. 

A forward, step-wise logistic regression was conducted 

to determine which independent variables 

Non-resting hole sites Resting hole sites 

N Min Max Mean ± SE N Min Max Mean ± SE Significance 

Depth (m) 20 1.4 3.3 2.0 ± 0.12 12 2.0 5.2 3.5 ± 0.30

Figure 3. The number of scans (white bars) and sightings 

(black bars) during diurnal (left) and nocturnal (right) scans 

for each location 


Sites with resting holes were located in dead end 

bogues, lagoons, and coves close to the mangroves 

with little current and calm sea state. Water 

depth was greater and surface velocity was lower 

at resting holes than at scan-points without resting 

holes. However, comparison of water velocity 

between resting holes could not be made because 

measurements within resting holes were all less 

than 10 cm/s, which was the lower threshold for 

the flowmeter. Slow current and calm waters may 

enable manatees to rest without exerting energy 

to hold their position. These results support previous 

studies that reported manatees are found in 

areas sheltered from high currents, surf, and wind 

(Hartman, 1979; Powell et al., 1981; Lefebvre 

et al., 2001; Jiménez, 2005; Olivera-Gomez & 

Mellink, 2005). 

Although there was no seagrass growing in 

the resting holes themselves, many seagrass beds 

were nearby. This would facilitate a short distance 

of travel for manatees between resting sites and 

feeding sites in calm waters. Given their large 

body mass and dependence on a low-energy, lowprotein 

diet, manatees must spend a large proportion 

of their time feeding to meet metabolic 

requirements. Manatees tend to feed from 5 to 

8 h/d, consuming about 7% of their body weight in 

wet vegetation (Hartman, 1979; Bengtson, 1983; 


Etheridge et al., 1985). Manatees may choose foraging 

strategies that allow them to maximize food 

intake while minimizing energy output. Similar 

studies in the Drowned Cayes indicated that sightings 

of manatees were most probable near resting 

holes and seagrass beds (LaCommare et al., 2008). 

The more familiar an animal is with locations of 

essential resources, the more efficient it will be in 

energy acquisition since this reduces searching 

time (Deutsch et al., 2003). 

Manatees were frequently encountered at three 

of the four previously identified resting holes 

within the Drowned Cayes. All four holes were 

located in protected coves or lagoons with minimal 

current, making it likely that manatees choose 

these areas because of the quiet conditions and 

create, or at least maintain, resting holes at these 

sites. Although previously categorized as a resting 

hole (LaCommare et al., 2008), the scan-point 

B1Co was likely not being used as a resting site in 

the summers of 2005 and 2006; it had a uniform 

1.5 m depth, with patches of shoal grass and no 

depression. However, there were many feeding 

scars and forelimb marks where manatees had dug 

into the mud to eat seagrass roots and rhizomes. 

Only one manatee was observed resting at this 

site in the summer of 2005, and no manatees were 

observed resting in the cove during the summer 

of 2006. This may indicate that manatee use of 

particular resting holes changes over time. 

Although manatees frequently used known 

resting holes, there was no evidence that manatees 

intentionally excavated or maintained the holes. 

Our current hypothesis is that they make use of 

natural depressions at these sites. The substrate 

in the holes is primarily uncompacted silt with 

high interstitial space, which is easily stirred-up 

as manatees rise off the bottom to surface for 

breaths. By resting regularly in the same place, 

the presence and vertical movement of a manatee 

during breathing cycles could easily deepen and 

maintain the depression. 

However, we do not yet know if individual 

manatees return to preferred holes exclusively 

or if resting hole use is indiscriminate. Also, it is 

unknown how manatees learn about the presence 

Table 3. Descriptive statistics for sea surface temperature, surface salinity, and air temperature during day and night scans 

of four locations 

Day Night 

N Min Max Mean ± SE N Min Max Mean ± SE Significance 

Sea surface temperature (°C) 106 27.2 34.3 30.9 ± 0.12 61 28.6 31.8 30.4 ± 0.10 0.001 

Surface salinity (ppt) 107 13.0 39.0 34.0 ± 0.30 61 28.0 37.0 34.0 ± 0.30 NS 

Air temperature (°C) 107 26.6 33.4 31.5 ± 0.12 61 27.4 32.0 29.4 ± 0.08


of these specific resting holes. In Florida, individual 

manatees show strong site fidelity to warmseason 

and winter ranges where manatee mothercalf 

pairs have been tracked remotely over time 

(Deutsch et al., 2003). Use of specific sites, initially 

with their mothers and then as independent 

subadults, has demonstrated natal philopatry to 

specific warm-season and winter ranges as well 

as to migratory patterns and travel routes among 

sites. Similarly, Antillean manatees may learn of 

specific resting holes as dependent calves and 

return to these same areas as adults. 

Diurnal and Nocturnal Use of Resting Holes 

There was a significant difference in the number 

of sightings of manatees between day and night. 

Although spotlights were used to increase the 

probability of detection during night scans, we 

acknowledge the increased potential for observer 

error during nocturnal scans. However, this potential 

was further reduced by increased vigilance 

during night scans, both visually and aurally. To 

increase successful detection and maintain consistency 

in effort, the same researchers and assistants 

were used for all night scans during this study. 

Despite concerns over detectability, these data 

suggest that manatees used resting holes more 

frequently during the day than at night in the 

Drowned Cayes. These results are consistent with 

observations in Florida where manatees leave 

the warm water refuge of Blue Spring in the late 

winter afternoons to feed all night, returning to the 

refuge in the morning (Bengtson, 1981; Rathbun 

et al., 1990). However, the animals abandoned 

the diurnal resting behavior in Blue Spring when 

water temperatures warmed in the spring. If use 

of resting sites is driven more by resources than 

a daily activity pattern, perhaps manatees use the 

resting holes in the current study area during the 

day when human activity on the water is high, 

then leave at night to feed in nearby seagrass beds 

or travel to freshwater sites. Interviews with local 

people indicated a similar pattern in Nicaragua 

where manatees rest in deep, quiet waters during 

the day and move to shallow waters to feed during 

late afternoon, night, and early morning, presumably 

to avoid hunting predation (Jiménez, 2002). 

Another possible reason for different resting 

hole uses during the day and night is the need for 

fresh water. Behavioral, ecological, and physiological 

evidence suggest that manatees require 

fresh or low salinity water for osmoregulation 

when living in a marine environment and feeding 

exclusively on seagrasses (Hartman, 1979; Powell 

& Rathbun, 1984; Ortiz et al., 1998, 1999). A lack 

of fresh water for extended periods leads to dehydration, 

although manatees may be able to osmoregulate 

via oxidation of fat for short periods of 

time (Ortiz et al., 1999). In Puerto Rico, where 

manatees are primarily observed in marine habitats, 

Powell et al. (1981) noted that 85.8% of 

manatee sightings were within 5 km of freshwater 

sources. Those authors also reported anecdotes 

by local fisherman indicating that manatees often 

visited nearby rivers to drink water. In aerial surveys 

in Belize, a higher number of manatees have 

been observed in near-shore habitat (e.g., estuary, 

lagoon, and river) than in cay habitat, with one 

of the highest numbers recorded from the Belize 

River (Auil, 2004). Also, more manatees were 

sighted in near-shore habitat during the dry season 

(November to May), and more manatees were 

sighted in the cay habitat during the wet season 

(May/June to November) (Auil, 2004). 

Similar to the situation in Ten Thousand Islands, 

Florida (Butler et al., 2003; J. P. Reid, pers. 

comm.), manatees in the Drowned Cayes travel to 

the Belize River, the closest source of substantial 

fresh water (about 12 to 15 km away) during the dry 

season (Auil, 2004). Manatees may also be traveling 

to the Belize River on a shorter time frame. 

Since boat traffic, both on the river and between 

the river and the cayes, is much higher during the 

day, manatees that travel from the Drowned Cayes 

to the river at night may reduce the probability 

of being struck by boats. This hypothesis is supported 

by studies in Florida and Costa Rica, where 

manatees have been known to avoid areas of high 

boat traffic, changing their behavioral state and 

moving out of a geographical area in response to 

approaching vessels (Buckingham et al., 1999; 

Smethurst & Nietschmann, 1999; Miksis-Olds, 

2006). 

There was a significant difference in sightings 

between the two summers with twice as 

many manatees seen in the summer of 2005 than 

in the summer of 2006. The reasons for this are 

unclear, but longer-term data for all 54 scanpoints 

detected no significant difference in the 

probability of encountering manatees over the 

period of 2001 to 2004, even as a result of season 

(Self-Sullivan, 2008). There was a significant 

difference in water temperature and salinity for 

the four scan locations between these two summers, 

with 2005 being warmer and more saline. 

However, the difference in temperature (0.5° C), 

although significantly different between years, is 

relatively small and probably not significant to 

manatees given what is known about their range. 

A similar situation occurred with day and night 

SST with only a 0.5° C difference. Although manatees 

can sense water temperature and salinity differences 

(Deutsch et al., 2003), the differences in 

the temperature readings in this study seem small 

enough to insignificantly affect manatee habitat 

choices. Salinity was 36 ppt in 2005 and 32

in 2006. Although this difference is fairly small, 

this may indicate a slightly more rainy summer 

season, which might have some impact on the 

probability of manatee presence at the four resting 

holes studied. Even though manatees were 

not seen as often in the summer of 2006, this does 

not necessarily mean that they used the Drowned 

Cayes habitat less frequently but rather that they 

were not detected as often at the particular resting 

holes being studied. 

West Indian manatee populations must deal 

with environmental changes on a daily (e.g., 

tides, currents, weather, human activity levels), 

seasonal (e.g., rainfall, temperature), and generational 

basis as human development continues to 

dramatically alter their habitats throughout the 

Caribbean (Deutsch et al., 2007). Although little 

is known about habitat use in the population over 

long periods of time, changes in habitat use by 

manatees have been observed at Swallow Caye 

in the Drowned Cayes of Belize, presumably as 

a result of increased human disturbance. When 

tour operators began and then ended a "swimwith" 

program at Swallow Caye, manatee use of 

the resting hole decreased during the program but 

increased again when the program was discontinued 

(Self-Sullivan, 2008). For generations of 

manatees, the undeveloped Drowned Cayes have 

provided a safe haven within a short distance of 

essential fresh water from the Belize River. 

Between 2001 and 2004, there was an exponential 

increase in cruise ship tourism in Belize. 

In 2001, there were 48 cruise ships with 48,116 

passengers; in 2002, there were 200 ships with 

319,690 passengers, representing a 584% growth; 

in 2003, there were 315 ships with 575,196 passengers, 

an 80% growth from 2002; and in 2004, 

there were 406 ships with 851,436 passengers, 

which is a 49% growth from 2003 (Belize Tourism 

Board, 2006). Although cruise ship numbers have 

leveled-off since 2005, the impact of cruise ship 

tourism remains above the 2003 level with a continued 

increase in development and human disturbance 

of manatee habitat in the Drowned Cayes 

area. Manatee mortality rate near Belize City is 

relatively high (Auil, 2004). This might be due to 

the increase in boat traffic as passengers are ferried 

from the ships by tender boats and are taken 

on tours to the reef, around the Drowned Cayes, 

and to small sandy cayes in the area (Self-Sullivan, 

2008). Also, there has been an increase in development 

of some of the other cayes in the Drowned 

Cayes, causing increases in boat traffic in these 

areas with the potential to cause siltation that may 

destroy the seagrass beds that the manatees feed 

on. 

The implications of our findings should be taken 

into consideration by conservation managers who 


are concerned with development in the Drowned 

Cayes. Conservation strategies designed to protect 

manatees should include preservation of 

low-energy, secluded areas where manatees can 

continue to maintain resting holes near seagrass 

beds. Results of the current study not only increase 

understanding of manatee resting habitats but provide 

necessary data for decisionmakers and wildlife 

managers to establish limits of acceptable change 

within the Drowned Cayes area and other strategies 

for the conservation of manatee habitat in Belize. 


This work was supported by a Marine Research 

Group (LLU) grant to M-LB, funding from Dr. 

Robert Ford in the Department of Social Work and 

Social Ecology (LLU), the Earthwatch Institute, 

and the Hugh Parkey Foundation for Marine 

Awareness and Education. We thank our Belizean 

field assistants and boat drivers, Gilroy Robinson 

and Dorian Alvarez, as well as field assistants 

Leigh Bird, Shauna King, Haydée Domínguez, 

Karen Petkau, Ryan Roland, Austin Bacchus, 

Coralie Lallemand, and the volunteers from the 

Earthwatch Teams 2, 3, and 4 in 2005 and 2006. 

We are also grateful to multiple colleagues at 

Loma Linda University; Dr. William Hayes and 

Dr. Zia Nisani who helped with statistics; and 

Daniel Gonzalez who helped in the field. Thanks 

to Rick Ware for providing the Belize City tide 

tables. Our research was carried out in compliance 

with the laws of the United States and Belize under 

MNREI Forest Department Permits, Ref. Nos. 

CD/60/3/05(29) and CD/60/3/06(32), and LLU 

IACUC Protocol #86006. This is contribution 

Number 8 of the Marine Research Group (LLU). 


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Resting Holes of the Antillean Manatee in Belize 71

J Coast Conserv (2011) 15:573–583 

DOI 10.1007/s11852-011-0146-3 

Aerial surveys of manatees (Trichechus manatus) in Lee 

County, Florida, provide insights regarding manatee 

abundance and real time information for managers 

and enforcement officers 

Deirdre J. Semeyn & Carolyn C. Cush & 

Kerri M. Scolardi & Jennifer Hebert & 

Justin D. McBride & Denis Grealish & John E. Reynolds 

Received: 8 October 2010 /Accepted: 7 January 2011 /Published online: 28 January 2011 

# Springer Science+Business Media B.V. 2011 

Abstract Conservation and management of the endangered 

Florida manatee is often centered on reducing mortality 

caused by watercraft collisions. Lee County, Florida, has 

led the state in watercraft-related mortality for eight of the 

last 10 years. This county is of particular concern as it 

contains important habitat for manatees, including extensive 

feeding grounds and an artificial warm-water refuge 

where more than 900 manatees have been recorded on a 

single day. Distributional aerial surveys were conducted 

from April 2007 through April 2009 over Lee County 

waters. Surveys yielded higher numbers of manatees than 

D. J. Semeyn 

5507 S. Bernie St., 

Tampa, FL 33611, USA 

C. C. Cush : K. M. Scolardi : J. E. Reynolds (*) 

Mote Marine Laboratory, 

1600 Ken Thompson Parkway, 

Sarasota, FL 34236, USA 

e-mail: reynolds@mote.org 

J. Hebert 

2740 Chariton Street, 

Oakton, VA 22124, USA 

J. D. McBride 

Lee County Division of Natural Resources Marine Program, 

1500 Monroe Street, 

Fort Myers, FL 33902, USA 

D. Grealish 

Florida Fish and Wildlife Conservation Commission, 

Division of Law Enforcement, 

Edwards Drive, 

Fort Myers, FL 33901, USA 

previously observed in this area. Using GIS methodology, 

kernel density analysis illustrated seasonal changes in 

distribution patterns and highlighted areas where manatees 

were most densely clustered. For example, during summer 

months, manatees were widely distributed throughout the 

survey area, with high-density areas associated with 

seagrass beds. During winter months, manatees were 

densely clustered at warm-water sites and over feeding 

grounds within close distance of these sites. These seasonal 

distribution patterns coincide well with speed zone designations. 

Counts and distributions of manatees were made 

available, almost immediately if necessary, to local marine 

law enforcement in an attempt to focus resources toward 

reducing manatee-watercraft collisions. Future studies 

should implement similar communication strategies to 

improve conservation efforts. 

Keywords Florida manatee . Aerial survey . Kernel density 

analysis . Lee County . Conservation . Management 

Introduction 

Over the past 40 years, aerial surveys have been used to 

monitor and assess number and distribution of Florida 

manatees, Trichechus manatus latirostris (e.g., Craig and 

Reynolds 2004; Wright et al. 2002). Aerial survey data are 

one of the primary sources of information used to create 

state and federal manatee sanctuaries and boat speed 

regulatory zones, as well as individual county manatee 

management plans (Laist and Shaw 2006). 

Listed as endangered under the Endangered Species Act of 

1973, the Florida manatee continues to face anthropogenic

574 D. J. Semeyn et al. 

and natural hazards that threaten the long-term viability of the 

species. Human related threats contributing to manatee 

mortality include watercraft collisions and coastal development 

leading to habitat loss and degradation (e.g. effects on 

warm-water availability). Naturally occurring events such as 

harmful algal blooms, intense coastal storms, and prolonged 

exposure to cold temperatures are also major causes of 

mortality in manatees (Ackerman et al. 1995; Langtimmand 

Beck 2003). The subpopulation of manatees in southwestern 

Florida is affected by all of these anthropogenic and natural 

factors, leading to the highest annual mortality rate (Florida 

Fish and Wildlife Conservation Commission 2010) and 

lowest estimated adult survival rates for manatees in the 

state (Langtimm et al. 2004). 

Lee County is often the focus of scrutiny with regard to 

management of manatees in southwestern Florida. This 

county contains critical habitat for manatees with over 590 

miles of natural shoreline (USA Cities 2009), extensive 

seagrass beds, and three important warm-water refuges: 

Florida Power & Light Company power plant (FPL) on the 

Orange River, the dredged canals of Matlacha Isles, and 10 

Mile Canal off of Estero Bay. It is also home to nearly 

600,000 people, and 50,464 total registered vessels, 48,853 

of which are recreational (United States Census Bureau 

2009; Florida Fish and Wildlife Conservation Commission 

2008). Consequently, manatee and human use of waterways 

overlap, creating increased potential for watercraft related 

collisions and mortality. 

The Florida Fish and Wildlife Conservation Commission 

(FWC) and U.S. Fish and Wildlife Service (USFWS) have 

developed and implemented boat speed and boat access 

regulations throughout the county in an attempt to reduce 

watercraft mortality. Seven types of regulatory zones exist 

throughout Lee County, although it is mainly comprised of three: 

1) Slow speed all year; 

2) Slow speed April 1-November 15; 25 mph rest of year; 

and 

3) 25 mph within marked channel. 

Even with these regulatory zones, Lee County surpasses 

almost all other counties in terms of annual human-related 

mortality of manatees, with an average of 15 per year over the 

last 10 years (Florida Fish and Wildlife Conservation 

Commission 2010). The Potential Biological Removal level 

(PBR) determined for the statewide population of manatees 

is 12 individuals (U.S. Fish and Wildlife Service 2009). 1 

Thus, human-related mortality in this one county exceeds the 

current (i.e. 2010) maximum number of manatees that may 

1 NOTE that this figure was calculated prior to the extremely high 

aerial survey counts of January 2010. As a consequence of there being 

more manatees than was previously believed, the PBR value of 12 

manatees is likely to be adjusted upward. 

be removed from the entire statewide population by such 

causes each year (U.S. Fish and Wildlife Service 2009). 

The original objective of this study was to conduct aerial 

surveys in order to provide current distributional data to Lee 

County managers for use in reviews of permits for new or 

modified marine facilities or other developments. This county 

is one of the 13 “key counties” in Florida, which are mandated 

by the State to develop and implement a Manatee Protection 

Plan (MPP). A major component of each MMP is the Marine 

Facility Siting Element (MFSE). The MFSE component of the 

Lee County MPP creates a slip-to-shoreline ratio for existing 

and proposed projects, based upon each project’s projected 

risk to manatees. The MFSE utilizes a series of input 

components including manatee mortality and distribution 

data. Whereas mortality data are updated each calendar year, 

until the completion of this project, Lee County resource 

managers had used distribution data collected in 1997–1998 

to evaluate marine facilities proposals. As the study progressed, 

we realized that managers could utilize survey data 

immediately to enhance, and later to evaluate, two other 

features of the MPP: law enforcement coordination and sitespecific 

boat speed zones (mentioned above). 

This study was not designed to provide a statistically robust 

estimate of manatee abundance in Lee County. However, it 

does provide an approach for monitoring spatial and temporal 

changes in distribution and relative abundance of manatees in 

order to formulate effective and proactive management and 

enforcement for this highly protected endangered species. 

Methods 

Aerial survey 

Aerial surveys were selected as an efficient and cost effective 

method to collect information regarding number and distribution 

of manatees (Reynolds et al. 2010). Lee County 

encompasses 803.6 square miles, and is criss-crossed with 

rivers, creeks, islands and canals (United States Census 

Bureau 2009). To prevent observer fatigue and ensure the 

entire county was surveyed in optimal light and weather 

conditions, the survey area was divided into northern and 

southern sections. From April 2007 through April 2009, two 

simultaneous surveys were flown twice each month; one 

covered waters of the northern county, and the other surveyed 

waters of the southern portion. Each route followed a 

racetrack pattern along shorelines and over open water. With 

the exception of the Gulf of Mexico, the entirety of Lee 

County’s waterways was surveyed as well as five miles 

beyond the county boundary where a water body continued 

into Charlotte, Collier, or Hendry Counties. Two high-winged 

aircraft (Cessna 172 or 182) were used. Each plane flew at an 

altitude of 250 m and a speed of 80–90 knots.

Aerial surveys of manatees (Trichechus manatus) in Lee County, Florida 575 

A Garmin GPSmap 76 recorded the survey path in each 

aircraft. Observers recorded the number of manatees (adults 

and calves), location, habitat and behavior for each sighting. 

Manatees within close proximity of each other and displaying 

similar behavior were grouped together as one sighting. Wind 

speed and direction were recorded based on local airport 

conditions. Other environmental conditions such as water 

clarity, percent cloud cover, and water surface conditions were 

estimated and recorded by the surveyor. To ensure that water 

clarity and visibility were acceptable for efficient spotting of 

manatees, surveys were terminated when sustained winds 

exceeded 15 knots or surface conditions scored four or higher 

on the Beaufort Wind Scale. 

Spatial analysis 

Kernel density estimation calculates home range and animal 

density by estimating the probability of locating an 

individual at a specific place and time (Horne and Garton 

2006; Worton 1995). The method creates a “kernel” or 

probability density over each point in a dataset (Seaman 

and Powell 1996). The density estimate is calculated by 

averaging the densities of all kernels that overlap each point. 

Kernel density acts as a decay-function with high estimates in 

locations with numerous points (sightings), and low densities 

in locations with few points (Seaman and Powell 1996). 

Using ArcGIS 9.3 (ESRI), survey data were exported as 

point shapefiles, and the Spatial Analyst Extension was used to 

calculate kernel densities for the total number of manatees per 

time period in the survey area. To reflect seasonal shifts, 

consideration of manatee distribution and habitat use is often 

divided into two periods: winter (November 15–March 15) and 

non-winter (March 16–November 14). These two seasonal 

designations were used to create two new point shape files 

from the survey point dataset. In addition, kernel densities were 

generated for sightings in the Central region (Fig. 1) forwinter 

(as usually defined, above) and three other time periods: postwinter 

(March 16–April 30), summer (May 1–September 30), 

and pre-winter (October 1–November 14). The Central region 

is of particular importance because 1) its seagrass beds are the 

closest foraging grounds to the primary warm-water refuge at 

the FPL power plant (Fig. 2) and 2) most manatees that use 

this refuge must travel through the Central region. This region 

was analyzed separately and according to shorter time periods 

in order to identify fine-scale temporal and spatial changes in 

the distribution of manatees in this area. 

An output cell size of 90 and a search radius of 2500m 2 

were applied to both analyses to generate density estimates 

for each survey point. The distribution of data was best 

represented on maps by using quantile classifications of 

numeric data. This method creates classes that may be close 

together in terms of the values, but provides a scale that 

groups the majority of the data most appropriately given the 

density distribution of manatees at survey points. Color 

intensity was used to depict areas of high and low density. 

Management 

When large numbers or notable shifts in distribution of 

manatees occurred, counts and observations were reported to 

local and state managers and shared with law enforcement via 

the Lee County Marine Law Enforcement Task Force 

(LCMLETF). This group was formed in 2003 and includes 

members from the Lee County Sheriff’s Office, Fort Myers 

Police Department, Cape Coral Police Department, Sanibel 

Police Department, U.S. Coast Guard Station Fort Myers 

Beach, U.S. Coast Guard Cutter Marlin, USFWS Division of 

Law Enforcement, USFWS/J.N. “Ding” Darling National 

Wildlife Refuge, FWC Division of Law Enforcement Fort 

Myers Field Office, Florida Department of Environmental 

Protection Division of Law Enforcement, U. S. Power 

Squadrons, and U.S. Army Corps of Engineers. The group’s 

Mission Statement specifically addresses resource protection: 

“The agencies of the Lee County Marine Law 

Enforcement Task Force are committed to providing 

the highest quality of marine law enforcement to 

protect the users of Lee County’s waterways, safeguard 

property, and conserve/protect marine life 

along with its environment.” (Lee County Marine 

Law Enforcement Task Force 2004) 

This well-organized group meets monthly to coordinate 

and maximize efforts to enforce boating safety and marine 

wildlife regulations. The goal of providing survey information 

to this task force was to allow the leaders of state and 

local law enforcement to deploy officers in ways that 

optimized manatee protection, while also ensuring that 

other enforcement obligations were handled as well. 

Current speed zone regulations for the county were 

acquired (Fig. 3) and compared with the kernel density maps 

to evaluate the zonal boundaries, both year-round and 

seasonal, and the potential need for regulatory improvement. 

Results 

Survey counts 

A total of 34 flights with both the north and south surveys 

completed was considered for both spatial and numerical 

analysis; all incomplete flights (n=3) were removed from 

the dataset for this analysis. Each point (n=4,000) 

corresponded to a sighting of 1–102 manatees. The 

majority of sightings were single animals or small groups 

(mode=1, mean=3). Total counts among survey dates for 

northern and southern surveys combined ranged from 135


Fig. 1 Reference map of study 

area showing the locations of 

warm-water refuges at FPL 

Fort Myers, Matlacha Isles and 

Ten Mile Canal. The spatial 

extent of the Central region is 

indicated by the black rectangle. 

manatees to 626 manatees (Table 1). The mean number of 

manatees counted per flight was 345 (± 23). An independent 

T-test showed that mean counts were significantly 

different (P


Fig. 2 Map illustrating locations of seagrass beds throughout the entire 

study area (source: South Florida Water Management District 2003) 

(Fig. 5a, b). This movement coincides with a significant 

increase in mean number of manatees sighted per survey 

(p=0.00102). From pre-winter to winter, manatees 

became even more densely clustered (Fig. 5c), but the 

increase in the mean number of manatees per survey was 

not significantly different (p=0.582). During post-winter 

there were generally fewer high-density areas and fewer 

manatees sighted than there were for winter, indicating a 

dispersal of manatees as the weather warmed (Fig. 5d). 

Management 

With regard to our study, the LCMLETF provided a stable 

infrastructure for quick dissemination of individual flight 

results to enhance conservation efforts with the near real-time 

information gathered. The information we provided regarding 

distribution, density, and behavior of manatees was reported to 

resource managers and LCMLETF coordinators, and was 

subsequently used to position marine enforcement units in the 

most critical areas to provide additional protection in needed 

areas. 

A comparison between the Kernel density analyses 

(Figs. 4 and 5) and the county’s site-specific boat speed 

zones (Fig. 3) show that, with a few exceptions, areas with 

high densities of manatees year-round overlap well with 

year-round speed zones, and areas with high densities 

during “non-winter” months overlap remarkably well with 

the seasonally (Apr 1–Nov 15) designated zones. There 

appear to be relatively few areas where high densities of 

manatees are found year-round in seasonally designated 

zones and vice versa. While it would be in the interest of 

local and state officials to identify these areas where 

enforcement zones could be added or re-assessed, it is not 

within the scope of this paper to do so. 

Discussion 

Aerial survey counts 

The results reaffirm that Lee County supports large 

numbers of manatees, particularly during fall and winter 

months, and further emphasize the need for careful 

management of this particular population. These results 

can be compared to results from statewide synoptic surveys 

which also indicate that a large proportion of the state’s 

manatees is found in Lee County during winter. In the 

January 2010 synoptic survey, biologists counted 5,067 

manatees statewide, with 877 (approximately 17%) in Lee 

County (H. Edwards FWC pers. comm.). This count was 

approximately 200 manatees more than the highest count in 

this study; however synoptic surveys are flown on days 

where sighting conditions are optimal. In February of the 

same year, after a prolonged period of cold weather, 905 

manatees were counted at the Orange River FPL plant alone 

(Reynolds, unpub. data). 

Our surveys produced much higher counts of manatees 

than did previous studies conducted in the area. The most 

recent study prior to ours was completed by FWC from 

1994 to 1998. For reference, the previous study reported an 

average of 147.6 manatees counted per survey (Fish and 

Wildlife Commission unpublished), whereas the mean 

count in our study was 345 manatees per survey. However, 

due to differences in flight path and overall survey effort, 

comparison between the 1994–1998 counts and ours is not 

straightforward. Regardless, both studies showed that 

manatees were present in Lee County in much higher 

numbers during winter than non-winter months. Also, the 

highest counts from both studies were recorded on surveys 

where large aggregations of manatees were present at 

warm-water sites, indicating that animals traveled to Lee 

County specifically for this resource and/or that manatees 

aggregated at the plant are easier to count than smaller 

groups of widely dispersed manatees. Survey data from the 

Central region also showed that there were more manatees 

present during winter than non-winter. However, over


Fig. 3 Reference map of major 

speed zones within Lee County 

(source: Florida Fish and 

Wildlife Conservation 

Commission- Fish and Wildlife 

Research Institute) 

shorter time periods, analyses support the observation that 

the number of manatees in this region during pre-winter 

was not significantly different from winter numbers. The 

aggregation of manatees at a warm-water refuge or nearby 

seagrass beds provides an opportunity for protection of 

manatees during pre-winter and winter that is more difficult 

to achieve when the animals are dispersed during nonwinter 

months. 

Spatial analysis and management implications 

The figures depicting manatee densities provide a clear 

comparison of spatial and temporal changes in numbers and 

habitat use in Lee County. This information has important 

management implications. For example, two key months, 

October and November, mark the influx of tourists and 

seasonal residents to southwestern Florida. Density analyses 

showed that during these months, the distribution of manatees 

was highly concentrated within San Carlos Bay and Matlacha 

Pass.Thispre-winterdistributionismorelikethatofthe 

winter than the summer, suggesting that manatees may be 

positioning or “staging” themselves for quick access to 

essential warm-water habitats well before cold weather 

arrives. Bengtson (1981) noted a similar strategy where 

manatees moved closer to Blue Spring, Florida in the fall to 

be nearer to a warm water refuge. These large concentrations, 

however, may indicate more than just positioning 

for imminent movement to warm water. Given the fact that 

San Carlos Bay contains abundant seagrass beds, it is 

possible that manatees use this pre-winter time to feed in 

preparation for bouts of fasting during potentially prolonged 

residential periods within warm-water refuge (Rommel et al. 

2003). In any case, the coincidental arrival of expanded 

numbers of both people and manatees to specific waterways 

presents a significant challenge for enforcement, and 

limitations in the size of enforcement staff underscore the


Table 1 Total number of manatees observed on each of 34 flights, 

and total number of manatees observed in the Central region 

Survey date Survey total Central region total 

4/2/2007 158 24 

4/24/2007 179 44 

5/17/2007 216 70 

5/29/2007 235 52 

6/8/2007 203 18 

6/28/2007 207 56 

7/2/2007 216 78 

7/9/2007 220 96 

8/13/2007 242 90 

8/20/2007 135 37 

9/7/2007 234 84 

10/8/2007 203 90 

11/6/2007 398 180 

11/20/2007 499 211 

12/3/2007 504 233 

12/18/2007 396 163 

1/7/2008 416 89 

2/19/2008 465 193 

4/17/2008 353 117 

5/13/2008 414 104 

5/27/2008 349 105 

6/6/2008 357 125 

7/18/2008 244 106 

8/28/2008 288 96 

10/8/2008 357 187 

11/5/2008 497 294 

12/8/2008 420 151 

12/18/2008 485 283 

1/9/2009 518 188 

2/27/2009 626 328 

3/9/2009 610 211 

3/30/2009 411 127 

4/10/2009 261 91 

4/29/2009 397 113 

Total 11713 4434 

Table 2 Lee County survey study area: total number of surveys, 

manatees sighted, and the mean number of manatees sighted ± one 

standard error per survey for each specified time period 

Winter Non-winter 

# of Surveys 11 25 

Total # Manatees 4939 6774 

Mean #/Survey 494±24 282±20 

Table 3 Central Region: total number of surveys, manatees sighted ± one 

standard error, and the mean number of manatees sighted per survey for 

each specified time period 

Pre-winter Winter Post-winter Summer 

# of Surveys 4 10 6 14 

Total # of Manatees 751 2050 516 2384 

Mean #/Survey 188±42 205±21 86±17 80±8 

need to operate as efficiently as possible. Therefore, the 

identification of important seasonal habitats where management 

and enforcement efforts should be focused is an 

essential outcome of this study. 

Spatial data for the Central region also show an 

interesting post-winter pattern. At this time, manatees focus 

on feeding, but their distributions are more similar to 

summer patterns, which are more widely distributed. When 

cold weather ceases, manatees appear to disperse quickly, 

returning to forage in areas other than those within San 

Carlos Bay and Matlacha Pass. This rapid dispersal pattern 

has previously been noted as a contributing factor to the 

mass mortality of manatees and other marine animals in 

southwest Florida during a 1996 red-tide event (Landsberg 

and Steidinger 1998). This paper concluded that manatees are 

at high risk from February through April should a “perfect 

storm” of environmental factors combine to generate persistent 

red-tide blooms in the region. Exposure to the neurotoxins 

produced by the bloom-forming dinoflagellate, Karenia 

brevis, causes disorientation and severe health problems in 

manatees (O’Shea et al. 1991; Bossart et al. 1998), making 

them particularly vulnerable to boat strikes. While little can 

apparently be done to prevent manatees from encountering 

these blooms, increased protection against human-related 

threats during such events should be a priority for managers. 

Manatee travel patterns within seasons are also of concern 

to resource managers. For example, surveyors observed that 

on the coldest winter days most manatees were found at 

warm-water sites, whereas on warmer days between cold 

fronts many of them were found in San Carlos Bay, 

presumably foraging. In order to make this transition from 

one critical resource to another, manatees must travel a 

minimum of 38 km up or down the Caloosahatchee River. 

This is a concern for managers since the primary travel 

corridor for manatees coincides with the primary channel for 

boat traffic. Even more troublesome, a 1998 study assessing 

the effectiveness of speed zones at multiple sites within this 

river yielded an overall compliance of just 58% (Gorzelany 

2004). Although this study considered only a subset of Lee 

County waters, without evidence to the contrary it can be 

assumed that compliance throughout the rest of the county is 

similar to that of the Caloosahatchee. On a more positive 

note, Gorzelany (2004) also reported a significant increase in


Fig. 4 Kernel density analysis of distribution of manatee sightings within the entire study area for (a) non-winter (16 March–14 November) and 

(b) winter (15 November–15 March) 

compliance levels when law enforcement was present. The 

results from his boater compliance study imply that our 

communication efforts with the LCMLETF not only efficiently 

directed limited enforcement staff to areas of potential 

watercraft incidents, but also indirectly increased the 

likelihood of boaters obeying the posted regulations. 

Management in action 

Watercraft-related mortality within Lee County did not 

decrease over the course of this study. In their evaluation of 

the impact of boat speed restrictions on watercraft-related 

deaths, Laist and Shaw (2006) listed four reasons for a lack 

of decline in deaths state-wide after implementation of speed 

zones in 13 key counties: (1) manatees are unable to avoid 

slow-moving vessels, and therefore speed restrictions offer 

little protection (2) low boater compliance occurs within 

speed zones (3) current speed zones are not substantial 

enough to offer protection (4) increasing numbers of both 

boaters and manatees result in increase numbers of collisions, 

effectively outpacing the speed zone reductions of 

these collisions. The Laist and Shaw study revealed that 

implementing slow speed rules within two densely populated 

manatee areas substantially decreased watercraft-related 

deaths. Based on their findings and those from our study, 

which indicated that the federal and state speed zones are 

spatially and seasonally substantiated in Lee County, the first 

and third reasons for mortality not decreasing seem unlikely. 

We conclude that in the case of Lee County, the absence of a 

decline in watercraft-related mortality is most likely explained 

by an increase in numbers of both manatees and boaters and/or, 

as discussed above, low boater compliance. 

One of the major benefits realized from the original 

objective of the study was the incorporation of new spatial 

data into the evaluation process for proposed marine facilities. 

The new spatial data from our study provide managers with 

up-to-date information reflecting the distribution of manatees 

in Lee County, which is important for the siting of marine 

facilities. In addition, prompt, near real-time reporting resulted 

in excellent communication and partnership among biologists, 

managers and law enforcement. These efforts helped to 

enhance both awareness of manatee presence and protection 

needs and the enforcement of posted manatee zones, which 

will hopefully result in reduced mortality rates in the 

upcoming years. Ultimately, the law enforcement officers are 

among the most important end users of the results of our 

research, as they have more daily contact with the boating 

public than biologists or decision makers. In fiscal year 2008, 

four Lee County marine law enforcement agencies conducted 

2,665 non-citation or educational contacts (Lee County 

Department of Natural Resources, unpublished data). This 

demonstrates the tremendous potential educational impact 

that law enforcement has on the boating public. To take 

advantage of this opportunity, it is the responsibility of


Fig. 5 Kernel density analysis of the distribution of manatee sightings within the Central region for four time periods: (a) summer (01 May–30 

September); (b) pre-winter (01 October–14 November); (c) winter (15 November–15 March); and (d) post-winter (16 March–30 April)


biologists and other researchers to provide law enforcement 

with the most timely, accurate, and understandable 

information possible. 

Open dialogue among biologists, resource managers, and 

law enforcement officers is critical to reaching a balance 

between ensuring human access to waterways and resources 

contained therein and providing protection for vulnerable 

natural resources. This coordination is especially important in 

areas such as Lee County where there is high use of key 

habitats by both people and manatees, and where tension 

exists surrounding regulations aimed at protecting a species or 

habitat. Open dialogue fosters partnerships, mutual respect, 

and an understanding that is crucial for manatee conservation 

and protection. Lee County and the LCMLETF is a model for 

this type of partnership. 

Conclusions 

With minimal cost and time, this project contributed to 

conservation and management of manatees in Lee County. 

It provided: 

□ aerial survey data that clarified both the larger-thanexpected 

numbers of manatees present in Lee County 

waters and the habitats they prefer seasonally; 

□ a spatial and temporal monitoring tool for long term 

decision making with regard to balancing the development 

of coastal waterways and protection of key areas 

for manatees; 

□ real-time information on manatee numbers and locations 

to enhance enforcement actions; 

□ validation of current state regulatory zones set within 

the county. 

Possibly the largest impact was in the simplest aspect of 

the project: communication. Through building partnerships 

and interagency cooperation, studies such as this one can 

hope to promote conservation at a much higher level. Not 

only did it provide managers with information to make 

sound decisions when considering regulations or permits in 

a dynamic environment, but it allowed law enforcement to 

maximize limited resources and focus on the most critical 

areas. 

Resource managers benefit from the knowledge of 

when and where to be most vigilant when navigating the 

waterways of Lee County. This information should be 

relayed to the public through a variety of media outlets 

in several different mediums. Future research in any of 

the 13 key counties should examine distribution of 

manatees compared to existing regulatory zones and 

focus on communication between agencies and with the 

public to further conservation efforts of this endangered 

species. 

Acknowledgements We thank the pilots and observers that conducted 

the surveys including Lew Lawrence, Dr. James Powell, Greg Baker, 

Jorge Neumann, and Kat Frisch. We are especially grateful to the staff of 

Florida Power & Light Company, particularly Winifred Perkins and Jodie 

Gless, for their patience and support throughout the course of the study as 

they coordinated our surveys with FPL security staff. Special appreciation 

also goes to the air traffic controllers at Fort Myers Page Field and 

Southwest Florida International Airport. Thanks also go to the Florida 

Fish and Wildlife Conservation Commission Law Enforcement officers 

and the Lee County Marine Law Enforcement Task Force for their 

interest and cooperation. The authors would also like to thank Jay 

Sprinkel for his advice and review of the statistical analysis, Kimberly 

Miller, Alexis Levengood, and Adrien Miller for their help editing and 

formatting the manuscript, and Holly Edwards for providing information 

on present and previous studies conducted by the FWC in Lee County. 

Funding for this project was provided by the Lee County Department of 

Natural Resources, and airplane fuel was kindly donated by Dolphin 

Aviation of Sarasota, Florida. 

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(1995) Trends and patterns in mortality of manatees in Florida, 

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the Interior, National Biological Service, Information and 

Technology Report 1, pp 223–258 

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John’s River,Florida.Master’s Thesis, University of Minnesota 

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the 1996 epizootic: gross, histological, and immunohistochemical 

features. Environ Toxicol Pathol 26:276–282 

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population trends along the Atlantic coast of Florida using a 

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Enforcement (2008) Boating Accidents Statistical Report pp 23 

http://www.myfwc.com/docs/Safety/2008_Boating_Statbook.pdf. 

Accessed December 2009 

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Wildlife Research Institute (2010) Manatee Mortality Database 

1974–2009. http://research.myfwc.com/features/category_sub. 

asp?id=2241. Accessed January 2010 

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squares cross-validation for choosing the smoothing parameter in 

kernel home-range analysis. J Wildl Manage 70:641–648 

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reduce deaths of Florida manatees. Mar Mamm Sci 22:472–479 

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breve red tides implicated in mass mortalities of the manatee 

(Trichechus manatus latirostris) in Florida, USA. In: Reguera B, 

Blanco J, Fernández ML, Wyatt T (eds) Harmful algae. Xunta de 

Galicia and IOC of UNESCO Publishers, p 97–100 

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BB, Barton SL, Hartley WC (2004) Survival estimates for 

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Mar Mamm Sci 20:438–463


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marinetaskforce.com. Accessed January 2010 

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bloom. Mar Mamm Sci 7:165–179 

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and design of aerial surveys for sirenians. In: Hines E, Reynolds 

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Intraspecific and geographic variation of West Indian manatee 

(Trichechus manatus spp.) vocalizations (L) 

Douglas P. Nowacek 

Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543 and 

Sensory Biology and Behavior Program, Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, 

Florida 34236 

Brandon M. Casper 

College of Marine Science, University of South Florida, 140 Seventh Avenue South, St. Petersburg, 

Florida 33701 

Randall S. Wells and Stephanie M. Nowacek 

Chicago Zoological Society, c/o Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, 

Florida 34236 

David A. Mann a) 

College of Marine Science, University of South Florida, 140 Seventh Avenue South, St. Petersburg, 

Florida 33701 and Sensory Biology and Behavior Program, Mote Marine Laboratory, 

1600 Ken Thompson Parkway, Sarasota, Florida 34236 

Received 25 October 2003; revised 11 April 2003; accepted 14 April 2003 

Recordings of manatee Trichechus manatus spp. vocalizations were made in Florida and Belize to 

quantify both intraspecific and geographic variation. Manatee vocalizations were relatively 

stereotypical in that they were short tonal harmonic complexes with small frequency modulations at 

the beginning and end. Vocalizations ranged from almost pure tones to broader-band tones that had 

a raspy quality. The loudest frequency was typically the second or third harmonic, with average 

received levels of the peak frequency of about 100 dB re 1 Pa. Signal parameters measured from 

these calls showed the manatees from Belize and Florida have overlapping distributions of sound 

duration, peak frequency, harmonic spacing, and signal intensity, indicating no obvious 

distinguishing characteristics between these isolated populations. © 2003 Acoustical Society of 

America. DOI: 10.1121/1.1582862 

PACS numbers: 43.80.Ka, 43.30.Sf, 43.80.Ev WA 

I. INTRODUCTION 

Florida manatees, Trichechus manatus latirostris, are endangered, 

and many animals are killed or injured each year 

by boat strikes. At least 25% of annual documented manatee 

deaths are due to collisions with vessels Marine Mammal 

Commission, 2002. Despite the fact that behavioral evidence 

indicates that manatees do have the ability to detect 

and respond to approaching vessels Nowacek et al., 2000; 

Weigle et al., 1994, the animals continue to be hit. In an 

effort to contribute to solutions that might reduce manatee 

morbidity and mortality from boat strikes, we set out to build 

a device to alert boaters of the presence of manatees based 

on passive detection of their sounds. 

Most of the boat strike mitigation effort has been directed 

toward testing the hearing capabilities of manatees 

Gerstein et al., 1999; Ketten et al., 1992 and their behavioral 

response in the presence of boats Nowacek et al., 

2000; Weigle et al., 1994 in hopes of understanding if and 

how they respond to oncoming vessels. Manatee sound production 

has been documented in only four papers Evans and 

Herald, 1970; Schevill and Watkins, 1965; Sonoda and Take- 

a 

Author to whom correspondence should be addressed. Electronic mail: 

dmann@marine.usf.edu 

mura, 1973; Sousa-Lima et al., 2002, including very little 

discussion of variability inherent in the animals’ vocal repertoire. 

These reports describe several types of sounds, but the 

primary vocalization recorded was a tonal sound often having 

several harmonics with the second or third harmonic often 

stronger than the fundamental frequency; intraspecific 

variation was not reported. The fundamental frequency 

ranged from 2.5 to 5 kHz for the West Indian manatee, 

Trichechus manatus spp., and 2.6 to 5.9 kHz for the Amazonian 

manatee, Trichechus inunguis. 

Vocalizations may be the most easily detected sounds 

produced by manatees compared to chewing and flatulence 

because published reports show them to have the highest 

signal-to-noise ratio and the vocalizations occur in frequency 

bands most dissimilar to the natural background noise of the 

manatees’ environment. To determine the amount of stereotypy 

in vocalizations we recorded sounds from Antillean 

manatees Trichechus manatus manatus in Southern Lagoon, 

Belize Lat/Lon: 17° 12N, 88° 20W) and Florida 

manatees in Crystal River, FL Lat/Lon: 28° 53 N, 82° 

35W). These two groups of manatees are subspecies of the 

West Indian manatee, so comparing the structure of their 

vocalizations could add to our understanding of the similarities 

and differences between the two subspecies. 

66 J. Acoust. Soc. Am. 114 (1), July 2003 0001-4966/2003/114(1)/66/4/$19.00 © 2003 Acoustical Society of America

II. METHODS 

A. Belize recordings 

In Belize we recorded sounds on a digital archival tag, 

the DTAG Johnson and Tyack, 2003, which simultaneously 

records the attitude pitch and roll, heading, and depth of the 

animal with sounds produced or received by the animal. The 

hydrophone signal was digitized continuously at 32 kHz. Selected 

manatees were encircled by a seine net in shallow 

water and brought aboard the capture vessel for health assessment, 

measurements, and tagging. DTAGs were attached 

to three individual manatees via temporary attachments using 

standard manatee peduncle belts. Floats tethered to the belts 

carried VHF transmitters for direct radio-tracking, and in 

some cases a GPS receiver. Sonic tags incorporated into the 

FIG. 2. Power spectrum of a typical manatee vocalization. Plot shows a 

2048-point FFT of a 2048-point segment from the middle of the signal 

shown in Fig. 1a. * indicates the fundamental frequency. 

belts permitted underwater tracking. The tags were recovered 

either when the belts released via a corrodible link or animals 

were recaptured for recovery of the DTAG and removal of 

other tags and belts. Attachments lasted approximately 24 h 

with acoustic data recorded for 4 or 8 h depending on the tag 

settings used. 

B. Crystal River, FL recordings 

Recordings in Crystal River, FL were made using a hydrophone 

HTI 96-min; sensitivity 164 dBV/Pa, 20 Hz to 

32 kHz connected to a data acquisition system Tucker- 

Davis Technologies, RP2.1 24-bit ADC and laptop computer. 

Signals were acquired continuously for approximately 

2 h at 48 828.125 Hz sample rate from an anchored boat with 

the hydrophone on the bottom at 1-m depth. Recordings 

were made approximately 20 m away from a group of about 

50 manatees that were in the spring. Individuals would occasionally 

move out of the spring into the spring run to 

within 2moftheboat. 

C. Data analysis 

FIG. 1. Spectrograms of representative 

manatee vocalizations. a Typical 

tonal harmonic vocalization Crystal 

River, FL, b tonal vocalization transitioning 

to less tonal Crystal River, 

FL, c broader-band harmonic vocalization 

Crystal River, FL, and d 

typical tonal harmonic vocalization 

Southern Lagoon, Belize. The acoustic 

tag used to record manatees in Belize 

sampled at F’s32 kHz. The 

scale bar shows relative sound levels 

in decibels. 

Data were analyzed with MATLAB Mathworks, Inc.. 

Peak frequency frequency with the most energy and the 

level of the peak frequency were determined by performing a 

1024-point FFT on a 1024-point segment of the middle of 

each call. This minimized smearing of frequencies due to 

changes in frequencies during the call. Harmonic spacing 

which is equivalent to the fundamental frequency was determined 

by performing an autocorrelation of the FFT, and 

measuring the first peak after lag zero. Duration was measured 

by MATLAB with an automatic detection algorithm, 

and then verified by hand from the spectrogram. While this 

may lead to a small uncertainty in measuring the time, it was 

advantageous for signals with low signal-to-noise ratios. 

J. Acoust. Soc. Am., Vol. 114, No. 1, July 2003 Nowacek et al.: Letters to the Editor 

67

III. RESULTS 

Manatees in Florida and Belize produced vocalizations 

that were harmonic complexes with small frequency modulations 

at the beginning and end Fig. 1. These ranged from 

almost pure tones to broader-band tones that have a noisy 

quality. The loudest frequency was typically the second or 

FIG. 3. Distribution of manatee vocalization 

parameters from a Crystal 

River, FL and b Southern Lagoon, 

Belize data from 11 March 2002. 

Panels show peak frequency, level of 

peak frequency, fundamental frequency 

harmonic spacing, and duration 

from top to bottom. We show only 

the Belize data from 11 March because 

this animal was in a similar behavioral 

situation to those in Crystal River. The 

animal was with a group of manatees, 

so these samples include sounds from 

other manatees as well as from the 

tagged animal. We felt that comparing 

sounds produced in similar situations 

provided the most accurate comparison 

for our study. 

third harmonic Figs. 2 and 3. Signal parameters measured 

from these calls show the manatees from Belize and Florida 

have overlapping distributions of sound duration, peak frequency, 

harmonic spacing, and signal intensity Table I and 

Fig. 3. Statistical comparisons between these signals were 

not possible because it is not known which individuals pro- 

68 J. Acoust. Soc. Am., Vol. 114, No. 1, July 2003 Nowacek et al.: Letters to the Editor

duced which sounds. Treating each call as a separate replicate 

would lead to pseudoreplication. The rate of vocalization 

in Crystal River, accounting for the number of animals 

present, was 1.29 vocalizations per minute, and in Belize it 

ranged from 0.09 to 0.75 per minute for the three animals 

tagged. When alone, the Belize animals were often silent for 

periods of 10 min. The rates of vocalization we measured 

were similar to earlier reports Bengtson and Fitzgerald, 

1985. 

IV. DISCUSSION 

TABLE I. Basic statistics of sounds recorded from manatees in Southern Lagoon, Belize and Crystal River, FL. 

The mean for each data set is shown with standard deviation in parentheses. 

Belize 

9 March 

2002 

There are no obvious differences in the vocalizations 

produced by manatees from Florida and Belize. For the parameters 

that were characterized sound duration, peak frequency, 

and harmonic spacing manatees from Florida and 

Belize had overlapping distributions. It is possible, however, 

that there are differences that we did not characterize. 

The finding that the second or third harmonic of the 

vocalization is usually most intense could be due either to 

how the sound is produced, or to propagation effects where 

the lower frequencies do not propagate as well in shallow 

water, or a combination of the two Rogers and Cox, 1988. 

Given that previous research on captive animals also found 

the fundamental to be less intense Evans and Herald, 1970; 

Schevill and Watkins, 1965, our results are probably best 

explained by the production system of the animals. Indeed, 

in all of these recordings we do not know the distance to the 

sound-producing manatee, only a range to the manatees that 

were in the area. The data from Belize include both the animal 

wearing the DTAG as well as animals vocalizing nearby. 

Still the received levels can be taken to show the range of 

levels that might be produced by manatees, and they are 

likely within 6–15 dB of source levels given the range of 

distances over which the recordings were made assuming 

losses of 3 dB per doubling of distance. 

The motivation for this study was to determine the range 

of natural variability in manatee sounds, so that a passive 

acoustic detection device can be developed to warn boaters 

of the presence of manatees. These data show that West Indian 

manatee sounds are relatively stereotypical, even be- 

Belize 

10 March 

2002 

Belize 

11 March 

2002 

Crystal 

River 

n 26 105 208 218 

Peak frequency Hz 3180 727 7080 2207 5560 2559 5223 1937 

Peak level 

dB re 1 Pa 

97.1 4.3 92.5 6.6 100.0 4.7 103.6 6.8 

Fundamental 

frequency Hz 

3180 728 4380 1618 3630 1620 2867 1059 

Duration s 0.032 0.017 0.161 0.10 0.217 0.098 0.228 0.074 

tween subspecies, in that they are short tonal harmonic complexes, 

and lend themselves readily to this application. 


We thank John E. Reynolds III, Buddy Powell, Robert 

Bonde, Mesha Gough, and Kevin Andrewyn for their assistance 

in the field and/or their consultation on this manuscript 

and Mark Johnson and Alex Shorter for their assistance preparing 

and deploying the DTAGs. This project was supported 

by the Florida Fish and Wildlife Conservation Commission, 

Wildlife Trust, the Chicago Board of Trade, and the Chicago 

Zoological Society. 

Bengtson, J. L., and Fitzgerald, S. M. 1985. ‘‘Potential role of vocalizations 

in West Indian manatees,’’ J. Mammal. 664, 816–819. 

Evans, W. E., and Herald, E. S. 1970. ‘‘Underwater calls of a captive 

Amazon manatee, Trichechus inunguis,’’ J. Mammal. 51, 820–823. 

Gerstein, E. R., Gerstein, L., Forsythe, S. E., and Blue, J. E. 1999. ‘‘The 

underwater audiogram of the West Indian manatee Trichechus manatus,’’ 

J. Acoust. Soc. Am. 105, 3575–3583. 

Johnson, M. P., and Tyack, P. L. 2003. ‘‘A digital acoustic recording tag for 

measuring the response of wild marine mammals to sound,’’ IEEE J. 

Ocean. Eng. 281, 3–12. 

Ketten, D. R., Odell, D. K., and Domning, D. P. 1992. Marine Mammal 

Sensory Systems, edited by J. Thomas Plenum, New York, pp. 77–95. 

Nowacek, S. M., Wells, R. S., Nowacek, D. P., Owen, E. C. G., Speakman, 

T. R., and Flamm, R. O. 2000. ‘‘Manatee behavioral responses to vessel 

approaches,’’ Report No. FWC-00127, 2000. 

Rogers, P. H., and Cox, M. 1988. Sensory Biology of Aquatic Animals, 

edited by J. Atema, A. N. Popper, and R. R. Fay Springer-Verlag, New 

York. 

Schevill, W. E., and Watkins, W. A. 1965. ‘‘Underwater calls of Trichechus 

Manatee,’’ Nature London 2054969, 373–374. 

Sonoda, S., and Takemura, A. 1973. ‘‘Underwater sounds of the manatees, 

Trichechus manatus and T. inunguis Trichechidae,’’ Report of the Institute 

for Breeding Research, Tokyo University of Agriculture, Vol. 4, pp. 


Sousa-Lima, R. S., Paglia, A. P., and Da Fonseca, G. A. B. 2002. ‘‘Signature 

information and individual recognition in the isolation calls of Amazonian 

manatees, Trichechus inunguis Mammalia: Sirenia,’’ Anim. Behav. 


U. S. Marine Mammal Commission 2002. ‘‘Annual Report of the U.S. 

Marine Mammal Commission,’’ U.S. Marine Mammal Commission, 4340 

East West Highway, Suite 905, Bethesda, MD. 

Weigle, B. L., Wright, I. E., and Huff, J. A. 1994. ‘‘Responses of manatees 

to an approaching boat: a pilot study,’’ presented at the First international 

manatee and dugong research conference, Gainesville, FL. 

J. Acoust. Soc. Am., Vol. 114, No. 1, July 2003 Nowacek et al.: Letters to the Editor 

69

Genetica (2011) 139:833–842 

DOI 10.1007/s10709-011-9583-z 

Evidence of two genetic clusters of manatees with low genetic 

diversity in Mexico and implications for their conservation 

Coralie Nourisson • Benjamín Morales-Vela • Janneth Padilla-Saldívar • 

Kimberly Pause Tucker • AnnMarie Clark • Leon David Olivera-Gómez • 

Robert Bonde • Peter McGuire 

Received: 25 February 2011 / Accepted: 18 May 2011 / Published online: 17 June 2011 

Ó Springer Science+Business Media B.V. 2011 

Abstract The Antillean manatee (Trichechus manatus 

manatus) occupies the tropical coastal waters of the 

Greater Antilles and Caribbean, extending from Mexico 

along Central and South America to Brazil. Historically, 

manatees were abundant in Mexico, but hunting during the 

pre-Columbian period, the Spanish colonization and 

throughout the history of Mexico, has resulted in the significantly 

reduced population occupying Mexico today. 

The genetic structure, using microsatellites, shows the 

presence of two populations in Mexico: the Gulf of Mexico 

(GMx) and Chetumal Bay (ChB) on the Caribbean coast, 

with a zone of admixture in between. Both populations 

show low genetic diversity (GMx: NA = 2.69; HE = 0.41 

C. Nourisson (&) B. Morales-Vela J. Padilla-Saldívar 

El Colegio de la Frontera Sur, Av. Centenario Km 5.5, 

77000 Chetumal, Quintana Roo, Mexico 

e-mail: coralie.nourisson@gmail.com 

K. P. Tucker 

Department of Natural Sciences, College of Coastal Georgia, 

3700 Altama Avenue, Brunswick, GA 31520, USA 

A. Clark 

ICBR Genetic Analysis Laboratory, University of Florida, 

2033 Mowry Road, Gainesville, FL 32610, USA 

L. D. Olivera-Gómez 

Division Academica de Ciencias Biologicas, Universidad Juarez 

Autonoma de Tabasco, Km. 0.5 carretera Villahermosa- 

Cárdenas, 86039 Villahermosa, Tabasco, Mexico 

R. Bonde 

US Geological Survey, 2201 NW 40th Terrace, Gainesville, 

FL 32605, USA 

P. McGuire 

University of Florida, 2015 SW 16th Ave, Gainesville, 

FL 32610, USA 

and ChB: NA = 3.0; HE = 0.46). The lower genetic 

diversity found in the GMx, the largest manatee population 

in Mexico, is probably due to a combination of a founder 

effect, as this is the northern range of the sub-species of T. 

m. manatus, and a bottleneck event. The greater genetic 

diversity observed along the Caribbean coast, which also 

has the smallest estimated number of individuals, is possibly 

due to manatees that come from the GMx and Belize. 

There is evidence to support limited or unidirectional gene 

flow between these two important areas. The analyses 

presented here also suggest minimal evidence of a handful 

of individual migrants possibly between Florida and 

Mexico. To address management issues we suggest considering 

two distinct genetic populations in Mexico, one 

along the Caribbean coast and one in the riverine systems 

connected to the GMx. 

Keywords Antillean manatee Microsatellite 

Conservation genetic Genetic structure 

Introduction 

The National Manatee Conservation Program, implemented 

in 2001, divided Mexico’s manatee (Trichechus 

manatus manatus) population into three management units 

(MU) (SEMARNAT 2001) (Fig. 1). These MUs were 

based on the geographic distribution of the manatees, the 

different regional threats, local research capacities, regional 

socio-cultural factors, and similarities in habitat characteristics 

including water quality and availability that has 

led to a protection plan for the region (SEMARNAT 2001). 

An understanding of the manatee population structure and 

diversity in Mexico, based on population genetics, will 

provide a valuable tool to improve the scientific 

123

834 Genetica (2011) 139:833–842 

Fig. 1 Sampling sites, with 

existing manatee management 

units recognized in Mexico. 

Dots represent specific sampling 

sites 

information lending support for management actions, such 

as the new National Manatee Conservation Action Plan for 

Mexico (PACE manati). That plan is expected to be 

adopted this year (2011). In Mexico, manatees have been 

protected since 1922 (Diario Oficial 01/20/1922), listed as 

a threatened species in 1991 under Federal Law (SEDUE 

1991) and since 1994 has been classified as a species at risk 

of extinction by the Mexican Government (SEMARNAT 

2002). At the international level, Antillean manatees were 

classified as vulnerable by the International Union for 

Conservation of Nature (IUCN) Red List from 1982 to 

2007 and endangered since 2008 (Deutsch et al. 2008). 

West Indian manatees have also been listed as an endangered 

species by the Convention on International Trade in 

Endangered Species (CITES 2009) since 1975. 

The Antillean manatee occupies the tropical coastal 

waters of the Greater Antilles and Caribbean, extending from 

Mexico along Central and South America to Brazil (Husar 

1978; Lefebvre et al. 1989, 2001). The distribution of manatees 

in Mexico includes the coastal and wetland systems of 

the Gulf of Mexico (GMx) and the Caribbean coast (Fig. 1). 

The majority of manatees inhabit the wetland systems of 

Veracruz, Tabasco, Chiapas and Campeche states along the 

GMx, where a conservative estimate of population size is 

between 500 and 1,500 manatees (Olivera-Gómez 2006). It 

is estimated that approximately 200 to 250 manatees reside 

in Quintana Roo region (Morales-Vela and Padilla-Saldívar 

123 

2011) and much fewer reside within the Yucatan state 

(Morales-Vela et al. 2003). In Quintana Roo, most manatees 

occur in Chetumal Bay (ChB) with an estimate of about 100 

to 150 manatees (Morales-Vela and Padilla-Saldivar 2009a). 

In Ascencion Bay (AB) the estimate is smaller, with 

approximately 25 manatees counted during a single aerial 

survey in July of 2009 (Landero-Figueroa 2010). ChB and 

AB are located approximately 335 km apart (shore distance). 

North of the Yucatan Peninsula no estimates have 

been provided and manatee abundance is presumed to be 

very low (Morales-Vela et al. 2003). 

Previous genetic studies on the West Indian manatee 

suggest that their mitochondrial DNA (mtDNA) variability 

ranges between one (Florida) to as many as eight haplotypes 

(Colombia) per country (Garcia-Rodriguez et al. 

1998; Vianna et al. 2006). Genetic studies of manatees in 

Mexico, from Tabasco to Quintana Roo indicate differences 

among the populations. The biggest difference is 

between the GMx, where only one haplotype (J) is found, 

and the Caribbean coast where three haplotypes (J, A, A4) 

have been identified (Medrano-González et al. 1997; 

Castañeda-Sortibrán unpublished data). However, the small 

sample size from the GMx (n = 4) at the time of this 

mtDNA study was not sufficient to provide significant 

results. 

Historically, manatees were abundant in Mexico from 

Tamaulipas to the Yucatan Peninsula, but hunting for food

Genetica (2011) 139:833–842 835 

during the pre-Columbian period by Mayans (McKillop 

1985), the Spanish colonization and throughout the history 

of Mexico (Durand 1983), has resulted in the significantly 

reduced population occupying Mexico today. Even as 

recently as 1983, it was reported that manatees were occasionally 

harpooned in the region north of Quintana Roo as a 

source of food (Gallo-Reynoso 1983). Direct hunting is rare 

now in the GMx, but manatees caught in nets are still 

sometimes killed for food, with children reporting that they 

had eaten fresh manatee meat recently (Olivera-Gómez 

2006). Fishermen have also declared that the manatee 

population decline in the Northern and Western coasts of 

the Yucatan Peninsula was caused by a number of factors, 

including hunting for local consumption, entanglement as a 

result of higher net-fishing activities in rivers, and habitat 

destruction and coastal construction due to human population 

growth and hurricane impacts (Morales-Vela et al. 

2003). The last documented manatee hunting activities on 

the Northeast coast of the Yucatan Peninsula occurred in the 

1960–1970s, but since then opportunistic poaching has 

continued into the 1990s (Morales-Vela et al. 2003). In the 

GMx other factors such as natural or artificial closing of 

drainages from freshwater ecosystems have restricted 

manatee access to vegetation, increased water temperature, 

and have resulted in increases in pollution, sedimentation 

and eutrophication due to agricultural and poultry runoff 

(Olivera-Gómez 2006). 

The high level of anthropogenic and habitat destruction 

pressure on the manatee population may have caused a 

population bottleneck, which is known to reduce genetic 

diversity. Typically, habitat loss and degradation increase 

the rate of fragmentation resulting in the isolation of small 

populations and leads to an increased probability for 

inbreeding and unstable demographics (Frankham et al. 

2002). 

Herein, we present a fine-scale population structure of 

manatees in Mexico using analysis of microsatellite DNA 

markers. The genetic diversity and population structure 

were compared to a geographically close conspecific, the 

Florida manatee (Trichechus manatus latirostris), which 

has a larger estimated population size. The results of this 

microsatellite DNA marker study were compared with 

those obtained previously from an unpublished Mexican 

mtDNA study. 

Methods 

Microsatellite DNA amplification and fragment 

analysis 

We analyzed 94 samples from different regions of Mexico 

including the Peninsula of Yucatan MU (ChB: 51, AB: 15), 

the central GMx MU (Tabasco: 15, Chiapas: 5 and Campeche: 

1) and the north of the GMx MU (Veracruz: 7) 

(Fig. 1). Blood or skin tissue from the tail was collected 

from wild manatees captured for health assessment and 

radio tagging studies. Skin tissue was collected from carcasses 

recovered by manatee research projects throughout 

Mexico. Blood from captive manatees was also utilized for 

this study because their original rescue location was 

known. To resolve population structure, we included the 

genotypes of 95 individuals from Florida based on the 

estimated population size in each of the four recognized 

MU’s in that state (Pause 2007). 

Blood and tissue samples were preserved with lysis or 

tissue buffer respectively (lysis buffer: 100 mM Tris–HCl, 

100 mM EDTA, 10 mM NaCl, 1.0% SDS (White and 

Densmore 1992); SED tissue buffer: saturated NaCl; 

250 mM EDTA pH 7.5; 20% DMSO (Amos and Hoelzel 

1991; Proebstel et al. 1993)). DNA extractions, amplifications 

and fragment analysis were performed at the University 

of Florida, ICBR Genetic Analysis Laboratory in 

Gainesville, Florida, USA and at the US Geological Survey, 

Southeast Ecological Science Center Conservation 

Genetics Laboratory in Gainesville, FL, USA. 

DNA extractions were carried out using either a standard 

phenol–chloroform protocol (Hillis et al. 1990) or the 

DNeasy tissue extraction kit (QIAGEN, Valencia, CA, USA). 

Polymerase chain reaction (PCR) amplifications were 

performed for each sample for each of 13 microsatellite 

loci previously designed for manatees: TmaA02, TmaE02, 

TmaE08, TmaE11, TmaE26, TmaF14, TmaM79 (Garcia- 

Rodriguez et al. 2000), TmaSC13, TmaE7, TmaH13, 

TmaE14, TmaK01, TmaJ02 (Pause et al. 2007). Amplifications 

were performed in Biometra UNOII, UNO- 

Thermoblock, T-Gradient thermocyclers (BiometraÒ, 

Göttengen, Germany) or a PTC-200 (MJ Research, Waltham, 

MA) thermocycler using the following conditions: 

95°C for 5 min, 35 cycles of 95°C for 30 s, with the specific 

annealing temperature as listed in the original publication 

for each primer, with the exception of TmaM79 = 

54°C; TmaA02 = 56°C; TmaE02, TmaE11, TmaE26 and 

TmaF14 = 58°C; TmaE08 = 60°C for 30 s, 72°C for 

30 s, and a final extension at 72°C for 10 min. Amplifications 

were performed in a total volume of 15 lL, with 

10 ng target DNA, 19 Sigma PCR Buffer (10 mM Tris– 

HCl, pH 8.3, 50 mM KCl, 0.001% gelatin), MgCl2 as 

indicated in the original publications, 0.2 mM each dNTP, 

0.04 units of Sigma JumpStart Taq polymerase (Sigma– 

Aldrich, St. Louis, MO, USA), 0.25 lM each primer, and 

bovine serum albumin (BSA), where indicated (Garcia- 

Rodriguez et al. 2000; Pause et al. 2007). For fragment 

analysis, the forward primers were labeled with the fluorescent 

dyes HEX or 6-FAM for processing and visualization 

on an ABI 3730xl Automated DNA Analyzer. 

123


Fragment data from the PCR products were collected from 

the ABI 3730xl and analyzed using GENEMARKER 1.5 

(SoftGenetics 2008) to determine allele sizes. Allele sizes 

were standardized using previously analyzed Florida samples 

as the baseline. 

Data analysis 

CONVERT (Glaubitz 2004) was used to convert the data into 

different input file formats. We used STRUCTURE, version 

2.3.1, (Pritchard et al. 2000) to identify possible subpopulation 

designations, without an a priori assignment of the 

overall population structure in Mexico. The data from 

Mexico and Florida were analyzed together. The admixture 

model was used and the number of populations (K) was set 

from 1 to 10 with a burn-in period of 100,000 iterations, 

followed by 1,000,000 Monte Carlo Markov Chain iterations. 

Five independent analyses were simulated for each 

value of K. The value of K with the lowest posterior 

probability was identified as the optimum number of subpopulations, 

as recommended by the STRUCTURE manual. 

GENECLASS2 (Piry 2004) and WHICHRUN version 4.1 (Banks 

and Eichert 2000) were used to test individuals attributed to 

a different population than the geographic location 

assigned by STRUCTURE. GENALEX 6.2 (Peakall and Smouse 

2006) was used to calculate genetic distance between 

individuals which were used on a Principal Coordinate 

Analysis (PCA). 

Estimates of the effective population size were made by 

NEESTIMATOR using the Linkage Disequilibrium algorithm 

(Peel et al. 2004). GENALEX 6.2, GENEPOP 3.4 (Raymond 

and Rousset 1995; Rousset 2008) and ARLEQUIN 3.1 (Excoffier 

et al. 2005) were used to compare and determine the 

genetic diversity and genetic differentiation including 

allelic richness N A and N E, heterozygosity observed (HO) 

and expected (HE), estimate of population subdivision FST 

and RST and inbreeding coefficients (FIS). ARLEQUIN was 

used to check for deviation from Hardy–Weinberg equilibrium. 

GENEPOP webversion was used to examine for 

Linkage Disequilibrium. The presence of null alleles was 

analyzed with MICRO-CHECKER (Oosterhout et al. 2004). The 

presence of a potential bottleneck was estimated using 

BOTTLENECK examining the heterozygosity excess (Cornuet 

and Luikart 1996). 

Results 

Results from the three different software packages (GEN- 

ALEX, GENEPOP, and ARLEQUIN) were compared and similar 

results were observed for genetic diversity and population 

structure as had been previously published. Therefore, only 

the results from GENALEX are presented in Tables 1 and 3. 

123 

Population structure 

Results for the STRUCTURE analysis identified that k = 3 

was the appropriate number of clusters (Fig. 2) based on 

the manual’s recommendation of the lowest posterior 

probability LnP(D). Most individuals were assigned to a 

cluster with Q [ 80%. In all simulations, Florida manatees 

were assigned to a separate population cluster (92.8% 

assignment) and the GMx and ChB populations were 

assigned to a cluster that corresponded to their geography 

(89.0 and 84.6% respectively). Samples collected from AB 

were not as clearly delineated, and were clustered with 

either the GMx (56.1%) or ChB (41.6%). 

The STRUCTURE analysis suggests that there were some 

individuals that may have had mixed ancestry based on this 

analysis. Interestingly, some of the AB individuals with a 

high percentage of ancestry corresponding to the GMx 

cluster do not share the GMx’s unique haplotype. Instead, 

these individuals’ haplotypes corresponded to the AB/ChB 

regions. Four manatees sampled from ChB show high 

percent ancestry with the Florida cluster (between 59% and 

76%). One of them was a female manatee carcass sampled 

in ChB which shared a 59% ancestry with the Florida 

population. This manatee died of natural causes (birthing 

complications) and her calf was not recovered. Another 

was a female juvenile who shared 75.6% ancestry with 

Florida but her haplotype did not correspond with the 

Florida haplotype (Castañeda-Sortibrán pers. comm). One 

male manatee, who was rescued as a calf in March 2002 

and is now in captivity in Veracruz, also shares a high 

percent ancestry with Florida samples (51%). One female 

manatee from Veracruz shares ancestry with the GMx 

samples (44%) and ChB region samples (47%). Two 

manatees from Florida share a high percent ancestry (45 

and 60%) with the GMx individuals. Results from GENE- 

CLASS2 and WHICHRUN analysis corroborate these assignments 

to populations other than their geographic location 

(Table 1). The Veracruz samples have lower ancestry 

values and cannot be totally attributed to Florida or the 

GMx as they appear to be mixtures of both populations on 

GENECLASS2 and WHICHRUN analysis (Table 1). 

The pairwise FST value between ChB and AB is low but 

significant (FST = 0.047), and RST is not significant 

(RST = 0.016) (Table 2). All pairwise FST and RST values 

are presented in Table 2. Significant levels of subdivision 

were observed between the GMx and all other regions with 

FST and RST, and among all regions with FST. All values 

were significant when calculated between the three regions: 

the Caribbean coast (including ChB and AB), the GMx and 

Florida (data not show) but most of RST values were not 

significant when calculated by separating the Caribbean 

coast into two areas: ChB and AB and compared with the 

two other geographic regions: the GMx and Florida


Table 1 Population assignments of some individuals using STRUCTURE, GENECLASS2 and WHICHRUN 

Individual Sampling 

population 

STRUCTURE 

assignment 

(Table 2). A higher level of differentiation (via FST) was 

observed between ChB and the GMx than between ChB 

and Florida. This does not correspond to the STRUCTURE 

analysis, which consistently grouped Florida into its own 

cluster, separate from ChB. A handful of individuals had 

microsatellite genotypes that clustered with Florida, but 

overall, the group is distinct from Florida. This can also be 

STRUCTURE Q value GENECLASS2 results WHICHRUN 

BCh GMx FL Most Score Other Score Other Score 

Attribution 

probable for most population for population pop3 

population probable 

population 

(pop2) pop2 (pop3) 

BCH40 BCH BCh 0.98 0.01 0.02 BCH 100 FL 0 GMx 0 BCh 

BCH13 BCH BCh 0.97 0.02 0.01 BCH 100 GMx 0 FL 0 BCh 

BCH46 BCH FL 0.15 0.09 0.76 FL 81.1 BCH 15.44 GMx 3.46 FL 



N2 BCH FL 0.31 0.1 0.59 FL 76.96 BCH 15.55 GMx 7.49 FL 

TOO2 GMx GMx 0.01 0.98 0.01 GMx 99.96 BCH 0.05 FL 0 GMx 

V2 GMx GMx 0.01 0.98 0.01 GMx 99.73 BCH 0.27 FL 0 GMx 

V3 GMx BCh 0.47 0.43 0.1 GMx 90.13 BCH 9.86 FL 0.01 GMx 

V1 GMx FL 0.04 0.46 0.51 GMx 51.33 FL 47.97 BCH 0.7 GMx 

TM1007 FL FL 0.01 0.01 0.98 FL 100 GMx 0 BCH 0 FL 

TM772 FL FL 0.01 0.01 0.98 FL 100 BCH 0 GMx 0 FL 

TM775 FL FL 0.06 0.17 0.77 FL 79 GMx 18.55 BCH 2.45 FL 

TM925 FL FL 0.28 0.04 0.69 FL 76.06 BCH 23.35 GMx 0.59 FL 

TM523 FL FL 0.17 0.24 0.6 FL 78.25 GMx 15.36 BCH 6.39 GMx (similar 

probability 

for each 

population) 

TM636 FL FL 0.02 0.24 0.73 FL 86.96 GMx 12.14 BCH 0.9 FL 

TM993 FL GMx 0.05 0.64 0.31 GMx 57.76 FL 41.08 BCH 1.16 GMx 

TM641 FL FL 0.1 0.42 0.48 FL 63.68 GMx 27.06 BCH 9.26 FL 

Values generated by STRUCTURE in italics are individuals that have higher ancestry percentage associations when compared to other populations, 

relative to where the sample was collected. Underlined results indicate higher association to a population other than their original sampling 

location population. Results not in italics indicate two samples assigned to their geographic population for comparison 

Fig. 2 Proportions of ancestry for individuals were assessed without 

a priori information using Bayesian clustering via STRUCTURE. This 

graphic represents the best fit of the data, where three population 

clusters are clearly distinguished (K = 3). Manatees from Florida 

consistently grouped separately from the manatees from Mexico. 

Manatees from the Chetumal Bay (ChB) cluster together and those 

from the Gulf of Mexico (GMx) river systems clustered together. 

Samples from Ascencion Bay (AB) suggest it may be a mixing zone 

for the Mexican manatee populations 

observed in the PCA from genetic distance that shows 

separate clusters for Florida and Mexico (Fig. 3). The null 

hypothesis tested for heterozygosity excess using the 

Wilcoxon test, with BOTTLENECK software, provided 

(P = 0.0004 and P = 0.07) probabilities under Two-Phase 

mutation (TPM) and Step-wise mutation (SMM) respectively, 

with a normal L-shaped distribution for ChB 

123


Table 2 Pairwise F ST and R ST values comparing the Mexican manatee 

populations defined as Chetumal Bay (ChB), Ascencion Bay 

(AB) and the Gulf of Mexico (GMx), as well as the Florida manatee 

population, generated by GenAlEx 6.2 

ChB AB GMx Florida 

ChB – 0.016 0.114* 0.025 

AB 0.047* – 0.087* 0.014 

GMx 0.131* 0.088* – 0.089* 

Florida 0.096* 0.094* 0.106* – 

* Significant values 

The FST values are presented below the diagonal, and RST values are 

above diagonal 

Fig. 3 PCA study from genetic distance using GENALEX. On the left 

is the Mexican population with individuals from the Caribbean and 

the Gulf of Mexico coasts. An admixture zone is apparent between 

these two areas. The population on the right corresponds to the 

Florida population 

population. For the GMx and AB populations the Wilcoxon 

test indicates a probability of 0.40 (TPM) and 0.17 (SMM) 

with a shifted mode distribution for the GMx and 0.046 

(TPM) and 0.10 (SMM) with a shifted mode distribution 

for AB. For Florida, the Wilcoxon test shows a probability 

of 0.02 (TPM) and 0.55 (SMM) with a normal L-shaped 

distribution. 

Genetic diversity 

No evidence of null alleles was identified in either the 

Mexico or Florida populations. After 78 comparisons and a 

sequential Bonferroni correction, no linkage disequilibrium 

was observed (overall a = 0.05). All loci were in Hardy– 

Weinberg equilibrium (HWE) after a sequential Bonferroni 

correction for all Mexican populations but TmaE02 was 

not within HWE for Florida. The error rate was determined 

by re-genotyping 12% of the samples. No errors were 

detected. Estimates of the mean number of alleles, effective 

number of alleles, and heterozygosity expected and 

observed, FIS, estimated population size and effective size 

for each determinate population (ChB, AB, the GMx and 

Florida) are presented in Table 3. Private alleles were 

found in Florida (n = 16), ChB (n = 2) and AB (n = 4). 

Discussion 

The GMx, with extended riverine and lagoon systems in 

Tabasco, Veracruz, Chiapas and Campeche, is a very 

favourable habitat for manatees. It has abundant vegetation, 

fresh water and areas where manatees can evade 

hunters. The Caribbean coast also represents very suitable 

habitat, especially ChB and AB, which are protected areas. 

ChB is the largest marine protected area at the state level in 

Mexico and is shared with Belize. AB is part of the Biosphere 

Reserve of Sian Ka’án, one of the largest Federal 

marine reserves in Mexico. 

Table 3 Diversity statistics over the 13 microsatellite loci examined for manatees from Mexico and Florida 

Population ChB AB GMx Florida 

Number of samples 51 15 28 95 

NA 3.00 ± 0.32 3.00 ± 0.32 2.62 ± 0.24 3.62 ± 0.48 

NE 1.99 ± 0.17 2.00 ± 0.22 1.84 ± 0.17 2.04 ± 0.16 

HE 0.46 ± 0.04 0.43 ± 0.05 0.41 ± 0.05 0.47 ± 0.04 

HO 0.47 ± 0.05 0.45 ± 0.07 0.44 ± 0.05 0.47 ± 0.04 

FIS -0.059 -0.035 -0.056 -0.006 

LD Abs Abs Abs Abs 

Null alleles Abs Abs Abs Abs 

Estimated population 100–150 23 (aerial survey) 500–1,500 5,000 

Effective population size 32.7 (23.9–47.4) 4.9 (4.0–6.2) 27.6 (18.0–49.4) 424.3 (208.3–6,816.5) 

The mean number of alleles (N A), effective number of alleles (N E), observed and expected heterozygosity (H O and H E, respectively), inbreeding 

coefficient (F IS), linkage disequilibrium after sequential Bonferroni correction (LD), null alleles, estimated population size, and effective 

population size for each population examined: Chetumal Bay (ChB), Ascencion Bay (AB), the Gulf of Mexico (GMx) and Florida for 

comparison 

123


Manatees are known to travel long distances along 

coastlines with suitable habitat (e.g. a Florida manatee was 

observed as far north as Rhode Island), as well as infrequent 

travel across open ocean (Alvarez-Alemán et al. 

2010; Deutsch et al. 2003; Fertl et al. 2005; Reep and 

Bonde 2006). Using existing tools, genetic analyses of 

Florida manatees have suggested little population structure 

throughout Florida (McClenaghan and O’Shea 1988; Garcia-Rodriguez 

et al. 1998; Pause pers. com.). Although 

manatees are capable of travelling along the shoreline 

between the GMx and the Caribbean coast, seasonal 

migration in response to cold weather is not necessary for 

survival in Mexico as it is in Florida. 

Radio tagging studies in ChB illustrated movement by 

five males and one female along the shoreline between 

discrete manatee habitats in ChB and Belize (Morales-Vela 

et al. 2007). One of these males was also observed participating 

in a mating group in Belize (Auil-Gomez pers. 

comm). The movement pattern from ChB to Belize was very 

similar as manatees made directed, continuous moves along 

the shoreline between discrete manatee habitats (Morales- 

Vela et al. 2007). None of the 19 manatees tagged with 

Argos-linked GPS radio tags, either from ChB or AB 

showed movements north of the initial tagging site (Morales-Vela 

and Padilla-Saldívar 2009b). The natural morphological 

features of ChB, oriented in the south of Mexico, 

easily connect ChB with both the Caribbean Sea and coastal 

Belize. An extensive coral reef barrier forms a natural 

marine corridor that may promote easier movement of the 

manatees between ChB to the south along the coast of 

Belize, than to the north of the Yucatan Peninsula. The 

Caribbean group is represented by ChB and AB, with a 

significant but low FST between these two locations. AB 

appears as a mixture of the southern portion of the Caribbean 

coast (ChB) and the GMx manatees, which is why the F ST 

between ChB and AB was significant but low (Fig. 2). It 

seems that migrants from the GMx breed in AB and do not 

continue south towards ChB. Mothers and calves are often 

observed in AB, which hosts suitable and abundant habitat 

for manatees. The mixture found in AB with the presence of 

individuals with both ancestral roots was not observed in the 

GMx region. The higher genetic diversity found in the 

Caribbean coast when compared to the GMx are consistent 

with results from the mtDNA data. Analyses of mtDNA 

analysis identified three haplotypes along the Caribbean 

coast, one common to Florida, another in common with 

Belize and the last shared a haplotype unique to the GMx 

(Castañeda-Sortibrán unpublished data). The Caribbean 

Cluster is geographically closer to Florida (approximately 

800 km) than to the GMx (approximately 1,150 km). 

A high level of genetic diversity in a population is 

thought to increase the probability of surviving a catastrophic 

event (Frankham et al. 2002). In this study, the 

mean number of observed alleles was very low and corresponds 

to less than what is predicted for wildlife populations 

that have been hunted or have been significantly fragmented 

(DiBattista 2008). However, these data describing low 

variability are consistent with other West Indian manatee 

populations throughout their range (Hunter et al. 2010, 

Pause pers. comm.). The lower genetic diversity, based on 

the number of alleles and heterozygosity found in the GMx, 

is probably due to a combination of a founder effect and a 

bottleneck event. This is likely due to manatees occupying 

the northern range of the subspecies and the extensive historical 

exploitation experienced during and since the pre- 

Columbian period up to the 1960–1970s. That depletion of 

manatee stocks resulted in the reduced population numbers 

observed today (Durand 1983; McKillop 1985; Medrano- 

González et al. 1997). The population with the greatest 

genetic diversity observed along the Caribbean coast also 

has the smallest estimated number of individuals (Table 3). 

This is possibly due to manatees that come from the GMx 

and Belize. Some breeding contribution of manatees from 

Belize is suggested by recent radio tagging data (Morales- 

Vela and Padilla-Saldívar 2009b) and by the presence of 

shared mtDNA haplotypes (Vianna et al. 2006). The proximity 

of the large Belize manatee population, only 

200–300 km south of ChB, may explain the dispersal route 

of the Caribbean coast manatees. Having a large population 

close by with an easy access route, makes it easier for the 

manatees to travel south than to try to make the longer 

journey to the GMx. There is evidence from radio tagging 

studies where some male manatees move from ChB to south 

Belize and return (Morales-Vela et al. 2007). However 

mtDNA shows different matrilineal trends in haplotype 

dispersal patterns in Belize and Mexico (Vianna et al. 2006) 

indicating that ChB and the Belize populations are not one 

well mixed population but have persisted independently 

over time. The genetic diversity along the Caribbean coast 

may have been recently influenced by potential migration 

from the growing manatee population in Florida as suggested 

by the few individuals that share remote ancestry 

with the Florida population. 

The Belize population shows a stronger separation from 

Florida (FST = 0.141) (Hunter et al. 2010) than the Mexican 

populations, with FST = 0.096 between the Mexican 

Caribbean coast and Florida and F ST = 0.106 between the 

GMx population and Florida. Belize and the Caribbean 

coast show a different pattern of haplotype distribution 

with two haplotypes in common and one private haplotype. 

The Florida haplotype, which is absent in Belize, yet is 

present in Mexico, confirms the closer relationship between 

Florida and Mexico than between Florida and Belize as 

confirmed by microsatellite data. 

Current collaborative studies utilizing samples from 

Mexico, Belize, Puerto Rico, Florida and other Caribbean 

123


countries will be completed in 2011–2012 to further assess 

the phylogeography and dispersal patterns of West Indian 

manatees. The effective population size is lower than the 

estimated population size for manatees in Mexico, which 

may be a reflection of the reduction in population size due 

to prior hunting pressure. The low Ne of the manatee 

population in the GMx may be due to a founder effect 

resulting in low genetic diversity, recent bottleneck events, 

and migratory limitations due to climate change and glacial 

periods. This could also be an artefact of the small sample 

size for the GMx. More samples are urgently needed from 

this area. 

Manatees in the GMx population tend to stay within the 

inland river systems, not in the coastal waters, and the 

group is likely fragmented by urban and agricultural 

development. An area of 140 km in the northeastern region 

of the Yucatan Peninsula is unsuitable habitat for manatees 

due to urban development, and the lack of vegetation and 

fresh water sources, resulting in a likely barrier to gene 

flow between the GMx and Caribbean coast (Medrano- 

González et al. 1997; Morales-Vela et al. 2003). Close to 

this zone, there are also significant coastal fishing activities 

and poaching (Morales-Vela et al. 2003). Examination of 

oceanographic structures shows a differentiation between 

the GMx and the Yucatan Peninsula (Laura Carrillo, pers. 

comm.; Merino 1997). This barrier may explain the low 

gene flow between the GMx and the Caribbean coast. 

Nevertheless, a group of six large manatees were observed 

in 2006 along the northeast coast of the Yucatan Peninsula 

(Reyes-Mendoza and Morales-Vela 2007). It is not known 

if these manatees were transient or resident. 

The analyses presented here suggest minimal evidence 

of a handful of individual migrants possibly between 

Florida and Mexico. One Florida manatee and six potential 

second generation migrants from Florida were detected in 

Mexico, which raises the question of whether migration or 

breeding occurs between the two subspecies located in 

Florida and Mexico. Two manatees from Florida share a 

high percent ancestry (45 and 60%) with the GMx individuals 

suggesting individuals may be second generation 

migrants. One of these manatees was a female with a 

known record of Florida maternal lineage from photoidentification. 

She was born in the Naples, FL area in 1995 

and captured in Port of the Islands, FL in February 2001. 

The other was the carcass of a male calf found in August 

1997 in the Banana River on the east coast of Florida 

(Beck, USGS, pers. comm.). One possibility is that 

migrants could be from Cuban waters; however, no genetic 

data are currently available from manatees in Cuba. Major 

currents go from Mexico to Florida and travel close to 

Cuba. Events such as tropical storms and hurricanes can 

change the currents and can separate manatees from the 

coast, taking them offshore and subject to drift (Langtimm 

123 

and Beck 2003). In that way, currents may also allow 

manatees to travel to Mexico from Florida. Manatees are 

able to survive short open water travels, and adults have no 

major natural predators so they will be able to survive 

incidental open sea travel. For example a known long-term 

resident female from the Florida manatee photo-identification 

catalog was sighted in Cuba in 2007 (Alvarez-Alemán 

et al. 2010). This manatee successfully travelled 

across open sea illustrating potential for population 

expansion. Reports of Florida manatees in the northern 

GMx indicate that they also can travel as far west as the 

southern Texas coast following the shoreline (Laguna 

Madre and Rio Grande) (Fertl et al. 2005). Historical distribution 

of manatees in Tamaulipas, Mexico which is 

north of the GMx shows a possible link that may exist 

between the GMx and Florida for manatees to travel 

(Lazcano-Barrero and Packard 1989). This leads to the 

question of successful reproduction between the two subspecies 

(T. m. manatus and T. m. latirostris) and the possible 

positive (increased variability, heterosis) or negative 

consequences (outbreeding depression) of breeding. 

Conclusion/conservation application 

The genetic structure of manatees in Mexico indicates two 

clusters with gene flow from the GMx to the Caribbean 

coast with no migration from the Caribbean back towards 

the GMx. This movement pattern could not be detected 

using mitochondrial DNA as there is only one haplotype 

(J) present in the GMx which is also present in the 

Caribbean. The three haplotypes found in the Caribbean are 

also found in the GMx, Florida and Belize. The individuals 

from AB appear as a mixture of the populations from ChB 

and the GMx. Additional evidence should be collected to 

determine the connectivity of other Central American 

populations of T. m. manatus, as well as the connectivity 

between the two subspecies. 

To address management issues, we suggest considering 

two distinct genetic populations in Mexico, one along the 

Caribbean coast and one in the riverine systems connected 

to the GMx. There is evidence to support unidirectional or 

limited gene flow between these two important areas. 

Special attention for conservation in the AB population 

would result in a healthier genetic stock, as this region is a 

source for potential mixture between the two primary 

genetic clusters. 

Based on this information it is important to maintain the 

natural migration routes of manatees from the GMx to the 

Caribbean area. This can be accomplished by conserving 

suitable manatee habitat along the north and east coasts of 

the Yucatan Peninsula, enforcing protection, reducing 

poaching and helping local initiatives that increase public


education. Ongoing tourism and urban development projects 

along those coasts are a major issue of concern. 

All of the captive manatees in Mexico were from the 

GMx region where they were originally rescued. However, 

most of them are in facilities located along the Caribbean 

coast. In the event of their release, returning them to the 

GMx would help maintain distinct populations. Also, if 

these facilities continue breeding manatees in captivity, a 

program that minimizes inbreeding and prevents inbred 

individuals or manatees with parents from different genetic 

populations from being released into the wild population 

must be considered. Genetic tools to assess lineages are 

currently being evaluated (Nourisson 2011). 

Acknowledgments This study is part of the doctoral dissertation 

research of the first author (CN), who was funded by a grant from the 

Secretaria de Relaciones Exteriores de México and by the Ministère 

des Affaires Etrangères Française—EGIDE. Financial support for 

training in Florida was provided by the Marine Mammal Commission. 

The project was funded by SEMARNAT/CONACYT (Project 

2002-C01-1128) and Dolphin Discovery for manatee captures and 

genetic analysis, as well as the US Geological Survey-Sirenia Project 

for genetic analysis. Mexican Government Research Permits and 

sample collection authorizations were obtained from DGVS # 03144; 

04513; 03670 and 03675. Samples were collected under scientific 

collection permits NUM/SGPA/DGVS/03144, NUM/SGPA/DGVS/ 

04513, NUM/SGPA/DGVS/03670/06, SGPA/DGVS/04060/06; 

SGPA/DGVS/01103/07, SEDUM/SSMA/DGPPE/0191/2004 and 

RBSK OFICIO CUN 037/04. Samples were transported to the 

research laboratories in the US under CITES export permits 

MX22523, MX24463, MX28578, MX26485, MX38416, MX34645, 

MX31591 and CITES import permits 06US808447/9 and 

07US808447/9. Samples were processed in Florida under authority of 

USFWS wildlife research permit MA791721 issued to the USGS 

Sirenia Project. All sample collection was done under approval of 

IACUC standards. Samples from the Gulf of Mexico area came from 

various projects and facilities: Dolphin Discovery, Veracruz Aquarium, 

Xcaret, ViaDelphi and Universidad Juárez Autónoma de 

Tabasco. We thank Dr. Margaret Hunter of the USGS Southeast 

Ecological Science Center for advice and help in the laboratory with 

various software packages. Any use of trade, product, or firm names is 

for descriptive purposes only and does not imply endorsement by the 

US Government. 

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Fish Sci (2011) 77:795–798 

DOI 10.1007/s12562-011-0388-x 

ORIGINAL ARTICLE Biology 

The differences in behavioral responses to a net obstacle 

between day and night in captive manatees; does entanglement 

happen at night? 

Mumi Kikuchi • Miwa Suzuki • Keiichi Ueda • 

Hirokazu Miyahara • Senzo Uchida 

Received: 23 March 2011 / Accepted: 27 June 2011 / Published online: 23 July 2011 

Ó The Japanese Society of Fisheries Science 2011 

Abstract Entanglement in fishing gear occurs in endangered 

manatees and may result in serious injury or death. 

Such incidents may happen more frequently at night when 

the animal’s visual sense is limited. In this study, we 

examined the differences in behavioral response of captive 

manatees to a net obstacle during light (day) and dark 

(night) periods. We used a plastic net as the obstacle, and 

video-recorded the manatees’ behavior. The experiments 

showed that captive manatees avoided the obstacle during 

the day more frequently than at night, which suggests that 

the manatees can perceive the obstacle more readily during 

light periods. However, there was no difference in the 

frequency of bumping or actively touching the obstacle 

between light and dark periods. The results suggest that the 

manatees can recognize the net obstacle even at night by 

purposely touching it, but they avoid it less frequently, and 

M. Kikuchi (&) 

Laboratory of Fisheries Biology, Graduate School 

of Agricultural and Life Science, University of Tokyo, 

1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan 

e-mail: mumi@cocoa.plala.or.jp 

M. Suzuki 

Department of Marine Science and Resources, College 

of Bioresource Sciences, Nihon University, 1866 Kameino, 

Fujisawa, Kanagawa 252-0880, Japan 

e-mail: miwa@brs.nihon-u.ac.jp 

K. Ueda H. Miyahara S. Uchida 

Okinawa Churaumi Aquarium, 424 Ishikawa, Motobu, 

Okinawa 905-0206, Japan 

e-mail: k_ueda@kaiyouhaku.or.jp 

H. Miyahara 

e-mail: h_miyahara@kaiyouhaku.or.jp 

S. Uchida 

e-mail: s_uchida@kaiyouhaku.or.jp 

that entanglement during light periods may occur during 

accidental bumping, rather than from a failure to recognize 

it altogether. 

Keywords Obstacle Behavior Trichechus manatus 

Introduction 

The greatest threat to many marine mammals is incidental 

entanglement and mortality in a fishing net, or bycatch [1]. 

The three species of manatees are aquatic mammals of the 

order Sirenia, and are known as generalist aquatic herbivores 

with no apparent natural predators. However, there 

are conservation concerns for all three species because of 

collisions with boats, entanglement in fishing nets, hunting 

and habitat degradation. In Florida, collisions of the manatee 

Trichechus manatus latirostris with watercraft are the 

primary cause of human-contact-related manatee mortality, 

but other preventable deaths result from entrapment in 

water control structures and entanglement in fishing gear 

[2]. The Antillean manatee Trichechus manatus manatus is 

primarily threatened by entanglement in fishing nets [3, 4]. 

The intensity of boat traffic throughout its range is relatively 

low in the areas used by Antillean manatees, and 

may not be a significant threat [3]. In the West African 

manatee Trichechus senegalensis, subsistence hunters have 

heavily exploited this species [5]; however, at present, 

incidental entanglement seems to be the most significant 

threat [6]. Even when manatees survive such encounters, 

entanglement may still result in serious injury, the loss of 

part of a pectoral flipper, and even death later on [5, 7, 8]. 

A high degree of sensitivity for brightness discrimination 

has been observed in West Indian manatees, which is 

comparable to some piscivorous predators, such as fur seals 

123

796 Fish Sci (2011) 77:795–798 

[9]. Furthermore, manatees have dichromatic color vision 

that is most sensitive in the blue and green region of the 

spectrum [10, 11]. Color vision greatly enhances pattern 

recognition and may compensate for some deficiencies in 

resolution, at least in comparison to cetaceans with 

monochromatic vision [12]. Hartman [7] concluded that 

vision is the preferred means of exploring their surroundings 

in manatees. Therefore, we might safely assume that 

manatee entanglement happens more frequently at night 

when their visual sense may be more limited. In order to 

test this assumption, any possible difference in cognitive 

performance needs to be assessed between light and dark 

periods. In this study, we examined the difference in 

behavioral responses of captive manatees to a net obstacle 

between day and night periods, in order to better understand 

the apparent causes of manatee entanglement. 


Experiments were conducted with four captive Antillean 

manatees Trichechus manatus manatus from June to September 

2004 at the Okinawa Churaumi Aquarium, Japan 

(Table 1). The manatees were kept in two indoor pools 

with the sexes separated. The first pool, containing two 

males, was 8.0 m long, 4.9 m wide and 3.0 m deep; the 

second pool, containing two females, was 8.0 m long, 

10.8 m wide and 3.0 m deep. The indoor facility has large 

windows that allow natural sunlight into the pools. 

Experiments were carried out randomly in the morning 

(0730 hours) and at night (1900–2000 hours). All experiments 

were conducted outside of regular business hours to 

minimize potential human interference. A total of eight and 

nine independent trials were conducted during the daytime 

and nighttime, respectively. In each trial, the subject’s 

behaviors were recorded for one hour with a video camera 

(FV40/FV300, Canon, Japan). During nighttime trials, a 

night-vision scope (WV-BP50, Panasonic, Japan) was also 

used to observe the subject’s behavior. Illumination 

intensity was recorded near the surface of the water using 

a digital luxmeter (LX-1332, Custom Co., Japan) at the 

beginning and end of each trial. 

Table 1 Name, standard body length (SL), body mass (BM), age 

(estimated for all except Yuma), and sex of each manatee used in the 

current study (data from 2004) 

ID Name SL (m) BM (kg) Age (year) Sex 

1 Yukatan 2.7 302 26 Male 

2 Ryu 2.7 317 14 Male 

3 Maya 2.8 412 17 Female 

4 Yuma No data No data 3 a 

Female 

a Yuma was born at the aquarium 

123 

Fig. 1 Photo of the black plastic net obstacle used in this study. The 

obstacle was constructed from PVC pipe and plastic netting, with 

weights attached to the bottom 

In order to examine the manatee’s behavioral response 

to the obstacle, a plastic net with no danger of entanglement 

was used. The obstacle (150 9 160 cm, black) was 

constructed from PVC tubing and plastic netting (1.5 9 

1.5 cm mesh size, 0.2 cm width, Takiron Co., Ltd.), with 

weights attached to the lower part of the obstacle to submerge 

it perpendicularly in the water (Fig. 1). The obstacle 

was placed in the pool such that the manatees had sufficient 

space to pass around it with no interference. The position 

of the obstacle was changed for each trial. To analyze the 

behavioral response to the obstacle, each individual’s 

behavior was classified into three categories: avoiding, 

bumping, or active touching with their snout or pectoral fin. 

The number of times these behaviors were observed and 

the duration of active touching were recorded. In addition, 

the number and durations of events of inactive behavior at 

the surface or on the bottom were calculated in order to 

compare with their active behaviors between day and night. 

To confirm the difference in illumination intensity 

between day and night, a generalized linear mixed model 

(GLMM) was analyzed with gamma errors, with each trial 

considered a random factor, and day–night differences 

treated as explanatory variables. To test the effect of the 

day–night difference on the number and duration of each 

recorded behavior, a GLMM was used with Poisson and 

gamma errors, respectively, and each individual manatee

Fish Sci (2011) 77:795–798 797 

was included as a random factor. The most parsimonious 

model was selected based on the Akaike information criterion 

(AIC). For all statistical analyses, we used the 

software R, and the GLMM was analyzed using the 

package lme4 and the function lmer. 

Results 

The GLMM for illumination intensity including the day– 

night difference as an explanatory variable was the best 

model, with the lowest AIC. The model had an AIC value 

that was 578.2 lower than the second best model, which 

included random effects only. This suggests that illumination 

intensity clearly differed between day and night 

(GLMM: day–night, estimated value during the day: 

1161.0 ± 63.5 SE, night: 1.1 ± 63.5 SE). 

The GLMM for the number of events of avoiding 

behavior that included the day–night difference as an 

explanatory variable was the best model, with the lowest 

AIC (Table 2). This model had an AIC value that was 31.1 

lower than the second best model, which included random 

effects only. These results suggest that the number of 

events of avoiding behavior differed between the day and 

night: these subjects showed a greater number of events of 

obstacle avoidance behavior during the day than at night 

(GLMM: day–night, estimated value during the day: 

1.7 ± 3.5 SE, at night: 0.8 ± 1.1 SE). 

The model with the lowest AIC value with respect to 

the number of events of bumping or active touching 

included random effects only (Table 2). The model had an 

AIC value of 0.8 and 1.7 lower than the second best 

model, which included the day–night difference. The 

GLMM for the number of events of bumping (GLMM: 

random effects only, 0.9 ± 1.3 SE) and active touching 

(GLMM: random effects only, 7.2 ± 2.1 SE) revealed 

that it was not related to the day–night difference. The 

GLMM for the duration of active touching, including 

random effects only, was the best model with the lowest 

AIC. The AIC value was 2.0 lower than the second best 

model, which included the day–night difference. These 

results suggest that the duration of active touching was not 

different between day and night (GLMM: random effects 

only, 49.8 ± 12.8 SE). 

The GLMM for the number or duration of events of 

inactive behavior, including random effects only, was the 

best model with the lowest AIC. The model had an AIC 

value of 0.7 and 0.8 lower than the second best model, 

which included day–night. These results indicate that the 

number (GLMM: random effects only, 1.3 ± 1.5 SE) and 

duration (GLMM: random effects only, 104.4 ± 10.7 SE) 

of events of inactive behavior were not related to the day– 

night difference. 

Discussion 

In this study, the number and duration of events of 

inactive behavior did not differ between day and night. 

Therefore, we concluded that our subjects’ activities did 

not differ between day and night, and that it did not affect 

their behavioral responses to the obstacle during the 

experiments. 

Focusing on the differences in behavioral responses to a 

net obstacle between day and night, we found that captive 

manatees show a greater number of avoidance behaviors 

during the day than at night. These results suggest that 

manatees can recognize the obstacle more easily during 

light periods. However, there was no difference in the 

number of bumping events between light and dark periods. 

Therefore, accidental bumping may be expected to occur 

regardless of the level of illumination and manatee’s higher 

degree of associated recognition. 

All sirenian species have sparse hairs on their bodies and 

orofacial that are of the sinus type, and typically tactile in 

function [13–18]. In fact, it has been specifically reported 

that a manatee’s orofacial hairs are used for tactile exploration 

and discrimination [13–16, 18]. In the current study, 

the number and the duration of active touching behavioral 

events did not differ between day and night. These results 

indicate that manatees heavily rely on their tactile senses to 

recognize an obstacle, even during light periods that 

facilitate purely visual recognition. In field studies, when 

wild Antillean manatees are caught by encircling them with 

Table 2 The GLMM models for the number of events of each behavioral response to the obstacle (avoidance, active touching, and bumping of 

the obstacle) along with AIC and delta AIC (DAIC) values 

Model The number of events of each behavioral response to the obstacle 

Avoidance Active touching Bumping 

AIC DAIC AIC DAIC AIC DAIC 

Random effects only 200.7 31.1 180.8 0.0 48.8 0.0 

Day–night 169.6 0.0 182.5 1.7 49.6 0.8 

Favoured models (bold type) were evaluated on the basis of the lowest AIC 

123

798 Fish Sci (2011) 77:795–798 

nets, the animals often explore the ‘‘weak areas’’ of the net 

via tactile contact in order to escape (Olivera-Gomez LD, 

2011, pers. comm.). They tend to descend to the bottom of 

the net and pull it up with its snout. There are many reports 

of these escape behaviors by local fishermen. Wild Antillean 

manatees can escape from the net in this way, and this 

more often occurs at deeper depths, where the net is more 

vertical (Olivera-Gomez LD, 2011, pers. comm.). In shallow 

depths, where the net forms a bag, manatees enter the 

fold of the net and are more easily caught on it (Olivera- 

Gomez LD, 2011, pers. comm.). In addition, entanglement 

often occurs with larger mesh size nets, which are used to 

catch large fishes (Olivera-Gomez LD, 2011, pers. comm.). 

Therefore, we further recommend examining the position 

of the net relative to the depth and the effect of the mesh 

size in order to clarify the causes of manatee entanglement. 

Acknowledgments We would like to thank all of the staff at the 

Okinawa Churaumi Aquarium for their assistance in conducting these 

experiments. We would like to thank K. Asahina at Nihon University, 

H. Kato at Tokyo University of Marine Science and Technology, L. 

D. Olivera-Gomez at the Autonomous University Juarez of Tabasco, 

and D. Gonzalez-Socoloske at Duke University for their discussions 

and insightful comments on previous drafts. We also thank J. 

A. Mobley and D. Gonzalez-Socoloske for correcting the English 

manuscript. The present study was supported by the Fisheries 

Research Agency, National Research Institute of Far Seas Fisheries. 

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Low genetic variation and evidence of limited dispersal in 

the regionally important Belize manatee 

M. E. Hunter 1,2 , N. E. Auil-Gomez 3,4 , K. P. Tucker 5 , R. K. Bonde 1,2 , J. Powell 4 & P. M. McGuire 2 

1 Sirenia Project, Southeast Ecological Science Center, U.S. Geological Survey, Gainesville, FL, USA 

2 Department of Physiological Sciences, College of Veterinary Medicine, University of Florida,Gainesville, FL, USA 

3 Wildlife Trust, Belize City, Belize 

4 Sea to Shore Alliance, St Petersburg, FL, USA 

5 College of Marine Science, University of South Florida, St. Petersburg, FL, USA 

Keywords 

conservation genetics; low diversity; 

microsatellite; mitochondria; marine 

mammal; West Indian manatee. 

Correspondence 

Margaret E. Hunter, Sirenia Project, 

Southeast Ecological Science Center, US 

Geological Survey, 2201 NW 40th Terrace, 

Gainesville, FL 32605, USA. Tel: +1 352 

264 3484; Fax: +1 352 378 4956 

Email: mkellogg@usgs.gov 

Received 26 October 2009; accepted 13 June 

2010 

doi:10.1111/j.1469-1795.2010.00383.x 

Introduction 

Abstract 

The West Indian manatee Trichechus manatus is a threatened 

aquatic mammal found throughout the south-eastern United 

States, Central and South America and the Caribbean. The 

Florida manatee Trichechus manatus latirostris and Antillean 

manatee Trichechus manatus manatus are the two recognized 

subspecies of the West Indian manatee. A low reproductive 

rate, environmental impacts and direct threats from the human 

population have historically limited manatee population 

growth. In 1982, the International Union for Conservation of 

Nature classified all West Indian manatee populations as 

vulnerable to extinction (IUCN, 2007). 

During the 17th through 19th centuries, the Spaniards in 

Belize and throughout the region severely exploited the 

592 

Animal Conservation. Print ISSN 1367-9430 

The Antillean subspecies of the West Indian manatee Trichechus manatus is found 

throughout Central and South America and the Caribbean. Because of severe 

hunting pressure during the 17th through 19th centuries, only small populations of 

the once widespread aquatic mammal remain. Fortunately, protections in Belize 

reduced hunting in the 1930s and allowed the country’s manatee population to 

become the largest breeding population in the Wider Caribbean. However, 

increasing and emerging anthropogenic threats such as coastal development, 

pollution, watercraft collision and net entanglement represent challenges to this 

ecologically important population. To inform conservation and management 

decisions, a comprehensive molecular investigation of the genetic diversity, 

relatedness and population structure of the Belize manatee population was 

conducted using mitochondrial and microsatellite DNA. Compared with other 

mammal populations, a low degree of genetic diversity was detected (HE=0.455; 

N A=3.4), corresponding to the small population size and long-term exploitation. 

Manatees from the Belize City Cayes and Southern Lagoon system were genetically 

different, with microsatellite and mitochondrial FST values of 0.029 and 

0.078, respectively (P 0.05). This, along with the distinct habitats and threats, 

indicates that separate protection of these two groups would best preserve the 

region’s diversity. The Belize population and Florida subspecies appear to be 

unrelated with microsatellite and mitochondrial F ST values of 0.141 and 0.63, 

respectively (P 0.001), supporting the subspecies designations and suggesting 

low vagility throughout the northern Caribbean habitat. Further monitoring and 

protection may allow an increase in the Belize manatee genetic diversity and 

population size. A large and expanding Belize population could potentially assist 

in the recovery of other threatened or functionally extinct Central American 

Antillean manatee populations. 

Antillean subspecies for sustenance (Lefebvre et al., 2001). 

By 1936, the population decline was so severe in Belize that 

Manatee Protection Ordinances were introduced to preserve 

the population (McCarthy, 1986). Today, the Belize manatee 

is listed as endangered by the Belize Wildlife Protection 

Act of 1981, Part II, Section 3(a) (Auil, 1998, 2004). A 

Manatee Recovery Plan was also proposed requesting 

information on habitat use and movement patterns to aid 

the development of conservation policies for the protection 

of the Belize manatee (Auil, 1998). 

While studying Caribbean manatee populations, O’Shea 

& Salisbury (1991) concluded that ‘Belize remains one of the 

last strongholds for the species in this part of the world.’ 

From 1977 to 1991, the Belize manatee population size 

appeared stable, however, an overall negative trend in 

Animal Conservation 13 (2010) 592–602 c 2010 The Authors. Animal Conservation c 2010 The Zoological Society of London

M. E. Hunter et al. 

numbers was detected from 1997 to 2002 (Auil, 2004). 

Although today Belize is considered the largest breeding 

Antillean population, it is still under pressure from anthropogenic 

threats and the census size of 1000 individuals is 

well below that recommended for the long-term genetic 

sustainability of a population (Frankham, Ballou & Briscoe, 

2002; Quintana-Rizzo & Reynolds III, 2007). 

Little is known of the abundance or distribution of 

manatees in the other Central American populations, 

although they are considered elusive and thought to be rare 

(Quintana-Rizzo & Reynolds III, 2007). However, supplementation 

from Belize or Mexico manatees in concert with 

coordinated regional efforts could potentially assist in the 

recovery of the Guatemala populations and those further 

the south. The large Mexico population is also protected 

Reduced Belize manatee dispersal and genetic variation 

Figure 1 Geographic map of Belize with the 

three study sites inset, Belize City Cayes 

(north), Northern & Southern Lagoons (center), 

and Placencia Lagoon (south). 

and manatees from Mexico have been documented traveling 

to Belize and even participating in a mating herd (Auil et al., 

2007; Morales-Vela et al., 2007). Quintana-Rizzo & Reynolds 

III (2007) suggest that safeguarding the Belize and 

Mexico populations as a resource of regional importance 

should be a high conservation priority. 

Long-term exploitation and small population sizes 

can lower genetic diversity and decrease fitness-related 

traits, such as fecundity and survival (Hoelzel et al., 1993; 

Frankham et al., 2002; Dixon et al., 2007). Genetic variation 

often acts in concert with demographic stochasticity in 

small populations. Loss of diversity can ultimately lead to 

an ‘extinction vortex,’ or a cyclic reduction in population 

size, resulting in loss of the population (Gilpin & Soulé, 

1986). 

Animal Conservation 13 (2010) 592–602 c 2010 The Authors. Animal Conservation c 2010 The Zoological Society of London 593

Reduced Belize manatee dispersal and genetic variation M. E. Hunter et al. 

A previous mitochondrial DNA (mtDNA) study identified 

three haplotypes (A03, A04 and J01) in 43 animals in Belize 

(Vianna et al., 2006). The resultant haplotype parameters 

included 28 polymorphic sites and nucleotide substitutions 

with h=0.558 and p=0.037. The distribution and genetic 

structure of the mtDNA haplotypes was not addressed, but 

could provide valuable information on the population structure, 

especially coupled with biparentally inherited nuclear 

data. Presented here are mitochondrial and nuclear microsatellite 

DNA studies addressing the genetic diversity, 

relatedness and population structure in Belize manatees. 

The Antillean Belize population is also compared with 

T. m. latirostris to provide information on the extent of West 

Indian manatee migration and relatedness. 


Sample collection and DNA extraction 

Manatee epidermis tissue and/or white blood cells were 

collected from recovered carcasses or during wild manatee 

health assessments in Belize from 1997 to 2007. Genetic 

samples were collected from a total of 118 unique animals 

in 213 health assessments (50% female and 50% male; Auil 

et al., 2007) and 12 carcass samples. Genomic DNA was 

isolated using Qiagen’s DNeasy blood and tissue kits 

(Valencia, CA, USA). Within the Florida dataset, 96 genotypes 

were randomly chosen, proportionally representing 

the four demographically defined management units 

(K.P. Tucker et al., unpubl. data). 

Study locations 

The Belize City Cayes (BCC), including the near shore and 

outlying cayes, are utilized by the tourist industry and experience 

heavy boat traffic and recreational activities from Belize 

City, the largest port in the country (Fig. 1). Manatee tours are 

largely conducted around Swallow Caye within the BCC. 

The Southern Lagoon system (SLS) consists of the Southern 

and Northern Lagoons and has the highest recorded 

number of manatees, with 55 individuals sighted in a single 

aerial survey (O’Shea & Salisbury, 1991). While the population 

is not heavily affected by watercraft, it is potentially 

impacted by salinity changes due to increased rainfall, 

influencing the abundance of aquatic vegetation, the primary 

food source for manatees. 

Placencia Lagoon (PL) is located 75 miles south of the 

SLS (Fig. 1). Placencia Village is a popular tourist destination, 

with a large amount of coastal development and 

agricultural runoff severely altering the environment and 

aquatic vegetation. Nitrification from shrimp farm effluent 

causes extensive algae blooms that can compromise the 

quality and growth of seagrass (Thornton, Shanahan & 

Shanahan, 2003). Nitrification also provides a food source 

for a marine snail, thought to be an intermediate host of a 

respiratory fluke Pulmonicola cochleotrema (Blair, 2005), 

which is known to parasitize manatee lungs (Beck & 

Forrester, 1988). Manatees in PL present at necropsy with 

594 

large loads of P. cochleotrema and copious mucoid discharge 

that could hinder respiration (Auil et al., 2007). 

The carcass samples utilized here were recovered from 

Corazol (n=1), Stan Creek (n=1), the Belize River mouth 

in Belize City (an area of high watercraft activity), or south of 

the river, possibly caught in the ocean current (n=10). The 

northern most manatee reserve in Belize is a section of 

Chetumal Bay, which continues into Mexico (Fig. 1). Samples 

collected in Chetumal Bay are not included in this study. 

Laboratory procedures 

Mitochondrial DNA analysis 

Primers CR-4 and CR-5 from García-Rodríguez et al. 

(1998) amplified a 410 bp portion of the mtDNA control 

region displacement loop for 113 individuals; 101 live 

captures and 12 carcasses. All PCR amplifications were 

carried out on a PTC-200 thermal cycler (MJ Research, 

Waltham, MA, USA). The PCR reaction conditions followed 

Kellogg (2008). Representatives from each haplotype 

and any ambiguous sequences were sequenced in both 

directions to ensure the accuracy of nucleotide designations. 

Microsatellite DNA analysis 

A panel of 16 polymorphic microsatellite primers (García- 

Rodríguez et al., 2000; Pause et al., 2007) was PCR amplified 

using 118 individuals. The study included 88 individuals 

from the SLS system (12 Northern Lagoon and 76 Southern 

Lagoon), 21 from BCC, two from PL and seven amplifiable 

carcass samples. PCR conditions followed Kellogg (2008; 

Table 1). MgCl2 concentrations were 3 mM, except for 

TmaH13, TmaKb60 and TmaSC5, which required 2 mM. 

Fragment analysis was performed on an Applied Biosystems 

(Foster City, CA, USA) ABI 3730 Genetic Analyzer. All 

individuals amplified at 14 or more loci. The Florida data 

were kindly provided for use in this paper (K.P. Tucker 

et al., unpubl. data). 

Statistical analysis 


The degree of differentiation, F ST and F ST, betweentheBCC 

and SLS and between Belize and Florida was calculated using 

ARLEQUIN 3.1 (Excoffier, Laval & Schneider, 2005). Comparisons 

with PL were not conducted due to the small sample size. 

Estimates of sequence divergence used the Kimura twoparameter 

genetic distance model (Kimura, 1980; Jin & Nei, 

1990). Lastly, Tajima’s D of selective neutrality, genetic 

diversity (h), nucleotide diversity (p), number of polymorphic 

sites (S) and number of nucleotide substitutions (NS) were 

calculated (Nei, 1987; Tajima, 1993). 


The level of polymorphism was estimated by the observed 

(HO) and expected heterozygosity (HE) and the average 



Table 1 Characteristics and PCR conditions for the 16 microsatellite loci implemented in the Belize manatee samples 

Locus name Tm ( 1C) BSA NA HO HE PIC NE TmaA02 56 2 0.310 0.349 0.534 1.537 

TmaE1 60 + 4 0.615 0.619 1.121 2.622 

TmaE02 55 2 0.265 0.300 0.477 1.429 

TmaE7 62 + 4 0.299 0.323 0.627 1.477 

TmaE08 58 3 0.701 0.657 1.084 2.917 

TmaE11 56 5 0.761 0.757 1.488 4.123 

TmaE14 62 + 4 0.564 0.573 1.035 2.340 

TmaE26 60 4 0.381 0.341 0.622 1.518 

TmaF14 58 2 0.390 0.403 0.593 1.675 

TmaH13 58 + 2 0.359 0.355 0.540 1.550 

TmaJ02 60 2 0.504 0.482 0.675 1.932 

TmaK01 54 2 0.530 0.390 0.578 1.638 

TmaKb60 56 5 0.416 0.483 0.782 1.935 

TmaM79 56 + 3 0.627 0.593 0.974 2.454 

TmaSC5 58 3 0.410 0.366 0.663 1.577 

TmaSC13 58 2 0.162 0.230 0.391 1.298 

Mean 3.1 0.456 0.451 0.762 2.001 

The optimized annealing temperature (T m), BSA requirement of 0.4 mg mL 1 , number of alleles (N A), the observed and expected heterozygosity 

(H O and H E), polymorphic information content (PIC), and effective number of alleles (N E). 

number of alleles per locus (NA) using GenAlEx 6.2 (Peakall 

& Smouse, 2006). Departures from linkage disequilibrium 

and Hardy–Weinberg equilibrium (HWE) were tested (dememorization 

10 000, batches 100, iterations per batch 

5000) in GENEPOP 4.0 (Raymond & Rousset, 1995) and 

Bonferroni’s corrections were applied for multiple comparisons. 

To assess overall genetic differentiation at the population 

level, GenAlEx 6.2 calculated F ST using the infinite 

alleles model and RST using the stepwise mutation model 

through an AMOVA. Comparisons included SLS, BCC and 

recovered carcasses, and Belize and Florida. 

GENECAP (Wilberg & Dreher, 2004) calculated the unbiased 

probability of identity (PID), which is the probability that two 

individuals drawn at random from a population will have the 

same genotype at the assessed loci (Paetkau & Strobeck, 1994) 

and P(ID)sib, a related more conservative statistic for calculating 

PID among siblings (Evett & Weir, 1998). The program 

additionally searched for duplicate genotypes. GenAlEx 6.2 

was used to estimate the shadow effect and P(ID)observed to 

determine whether unbiased P(ID) or P(ID)sib is the more 

accurate probability (Mills et al., 2000; Waits, Luikart & 

Taberlet, 2001) following Hunter et al. (2010). 

The relationship between genetic and geographic distance 

was evaluated to test for isolation by distance within Belize 

and for Belize and Florida based on 10 000 randomizations 

in GenAlEx 6.2. BOTTLENECK 1.2.02 evaluated heterozygote 

excess under the two-phased model using the Wilcoxon signranked 

test (Piry, Luikart & Cornuet, 1999). The M-ratio 

test used M_P_Val.ex to measure the proportion of unoccupied 

allelic states, which is lowered during a population 

reduction (Garza & Williamson, 2001). Input values included 

a mutation rate of 5 10 4 and y=0.274; and the 

recommended values of Dg=3.5 and ps=0.9. Datasets 

using seven or more loci and the appropriate mutation 

model can be assumed to have experienced a reduction in 


population size with an Mo0.68. The coefficient of genetic 

relatedness, r xy (Queller & Goodnight, 1989), was used to 

test the genetic variability within Belize using 95% confidence 

intervals in GenAlEx 6.2. Intra-populational relatedness 

should be significantly higher in populations that have 

undergone bottlenecks or founding events. 

To test the distribution of rxy between all pairs of 

individuals, KINGROUP 2 simulated expected unrelated and 

full-sib pairwise relatedness (10 000 pairs) from observed 

allele frequencies and the rxy values were plotted to compare 

the distribution (Konovalov, Manning & Manning, 2004). 

A deviation from random expectation could result from 

nonrandom mating among related individuals and/or overrepresentation 

from a few families, suggesting an excess of 

inbred individuals in the population. 

The program STRUCTURE 2.3.2 was used to identify the 

genetic subdivision within Belize and the genetic relationship 

and ancestral source populations of Belize and Florida 

manatees (Pritchard, Stephens & Donnelly, 2000). The most 

probable number of populations, K, was determined by 

evaluating the likelihood of the posterior probability [L(K); 

Pritchard, Wen & Falush, 2007] and by calculating DK, an 

ad hoc quantity related to the change in posterior probabilities 

between runs of different K values (Evanno, Regnaut & 

Goudet, 2005) in STRUCTURE HARVESTER (Earl, 2009). Simulations 

were conducted using the admixture model of 

K=1–10 with 10 000 repetitions of MCMC, following the 

burn-in period of 10 000 iterations with and without a priori 

‘population’ information using the admixture model. The 

LOCPRIOR setting was used to detect cryptic structure by 

providing priors for the Bayesian assignment process based 

on the sample location. The LOCPRIOR model allows structure 

to be detected with lower levels of divergence and is not 

biased towards detecting structure when it is not present 

(Hubisz et al., 2009). Individual assignment success was 



recorded as the likelihood of assignment (Q). Individuals 

were assigned to a cluster with QZ60%. 

Results 


The Belize samples contained three haplotypes (A03, A04 and 

J01). The BCC samples were comprised of the A04 (n=4) and 

J01 (n=15) haplotypes. The SLS individuals contained the A04 

(n=52), J01 (n=22) and A03 (n=6) haplotypes. A04 (n=1) 

and J01 (n=1) were identified in the PL samples. Recovered 

carcasses contained the A04 (n=6) and J01 (n=6)haplotypes. 

MtDNA sequence divergence estimates were h=0.534 0.025 

and p=0.031 0.015. Within Belize, Tajima’s D was large and 

positive (D=4.118) consistent with a population bottleneck, 

however it was not significant (Po1.000); therefore the 

null hypothesis of selective neutrality cannot be rejected. 

Genetic differentiation estimates between BCC and SLS 

were FST=0.078 (Po0.045 0.015) and FST= 0.036 

(Po0.712 0.052). Twenty-eight variable sites and nucleotide 

substitutions (6.8%) were identified in the three haplotypes. 

Within Florida, one haplotype was observed (A01, p=0.000; 

unpubl. data; Garc´ ıa-Rodríguez et al., 1998). Belize and Florida 

mtDNA sequence divergence estimates were FST=0.626 (Po0.00001 0.0) and FST=0.302(Po0.00001 0.0). 


The 16 nuclear microsatellite markers had lower levels of 

variation [HE=0.453 (0.230–0.757); HO=0.456 (0.162– 

0.761), N A=3.1 (2–5); Table 1] than the Florida population 

over 14 loci (K.P. Tucker et al., unpubl. data). In Belize, 

TmaKb60 and TmaSC13 had evidence of null alleles due to a 

heterozyogote deficiency. Deviation from HWE was found 

for TmaKb60 and TmaK01, even after a sequential Bonferroni 

adjustment (Po0.001). After 120 comparisons, linkage 

disequilibrium was observed between TmaE1 and TmaE14 

(Po0.05). FIS was 0.012 overall, suggesting slight inbreeding 

in the population. The error rate was determined by 

re-genotyping 11% of the individuals; no errors or duplicate 

genotypes were detected. 

Genetic differentiation between the BCC, SLS and recovered 

carcass samples was significant (Po0.05), although low 

(Table 2). The majority of private alleles were detected in 

SLS (n=5) as compared with BCC (n=1). The genetic 

distances showed a positive relationship with geographical 

distances between the BCC and SLS [r=0.20, (Po0.001)] 

and Belize and Florida [(r=0.48, (Po0.001)]. Pairwise F ST 

and R ST values for Belize and Florida were 0.141 and 0.082 

(Po0.001), respectively, supporting the subspecies distinction. 

Private alleles were detected for Florida (n=17) and 

Belize (n=1). 

The loci produced an unbiased P(ID) estimate of 

4.55E 08 and a P(ID)sib estimate of 3.60E 04, in which 

unrelated individuals could be identified in a population 

size of 4.7E+03 and 53, respectively, with a shadow 

effect of 1.00. Calculations in GenAlEx determined that 

P (ID)observed was nearly identical to that of unbiased P (ID), 

demonstrating that relatedness in this population is unlikely 

to affect match probability, because the population is 

o4.7E+03. 

The BCC and SLS Mantel test was positive and significant 

(Po0.001). All mutation model heterozygosity excess tests 

were significant (P 0.05), with low heterozygosity deficiency 

to excess ratios, SMM (4:12), IAM (2:14) and TPM (3:13). 

However, the mode shift test was L-shaped with no distortion 

of allele frequencies. The M-ratio was 0.54, indicative 

of a recent reduction in population size. The Belize intrapopulational 

pairwise relatedness was rxy=0.184 (95% 

CI=0.174–0.185), and fell above of the 95% CI ( 0.022– 

0.015) for permutations assuming random mating. 

The empirical distribution of pairwise relatedness values 

was low (mean=0.002, range=0.852–0.815), but not significantly 

different from the simulated distribution under 

random mating (mean=0.144; Mann–Whitney U-test, 

Table 2 Genetic differentiation and haplotype proportions of Belize manatees in the Southern Lagoon System (SLS), Belize City Cayes (BCC), and 

recovered carcasses (CAR) 

Geographic region 

(a) Genetic differentiation 

SLS BCC CAR 

SLS – 0.031 0.045 

BCC 0.041 – 0.025 

CAR 0.215 0.033 – 

(b) Haplotype proportions 

F ST values (above diagonal) and R ST values (below diagonal) generated from a survey of 16 microsatellite loci. Statistically significant values are in 

italics (P 0.01). 

Pie charts indicating the haplotype proportions of the A03 (black), A04 (dark gray), and J01 (light gray) in the SLS (n=80), BCC (n=19) and CAR 

(n=12) samples. 

596 



P40.05) or the full-sib distribution (Mann–Whitney U-test, 

P40.05; Fig. 2). However, the full-sib pairwise relatedness 

indicated a full-sib detection threshold of 0.21 with 19.9% of 

the pairs potentially representing full-sibs under this criterion, 

suggesting a strong representation of a few families in 

the population. 

The Bayesian and resulting Evanno et al. (2005) analyses 

strongly supported two genetic clusters (P 1; Fig. 3a and c). 

Belize (QAVE=98.5%) and Florida (QAVE=98.6%) had no 

admixture and strong assignment of individuals to their 

respective populations. When Belize was analyzed alone 

without a priori ‘population’ information, one population 

was supported (P 1). Alternatively, under the LOCPRIOR 

model, K=2 was supported (P 1; Fig. 3b) and a single 

genetic cluster or more than two were rejected (P 0, K=1, 

3–10). DK=2 also had weak support as the largest modal 

Figure 2 Distributions of pairwise relatedness values r xy (Queller & 

Goodnight, 1989) for the Belize manatee population (gray bars). 

Simulated unrelated (solid line) and full-sib (dashed line) curves are 

based on 10 000 iterations. 

value (Fig. 3d). The two clusters corresponded closely with 

the sampled geographic regions, the BCC (95% correct 

assignment, QAVE=91.6%) and SLS (86% correct assignment, 

QAVE=81.0%). 

Discussion 

Genetic diversity 


Trichechus manatus manatus is believed to have inhabited 

the majority of the coastal habitat of Central and South 

America historically, although no specific census size estimates 

are available (Husar, 1978; IUCN, 2007). A few 

thousand manatees were estimated in the 18th century in 

Belize (Auil, 1998). Today, the subspecies is severely reduced, 

rare, or absent in many areas where manatees were 

previously identified as abundant (Husar, 1978). Current 

population estimates place the Antillean manatee subspecies 

at o2500 mature individuals (IUCN, 2007) and Belize at 

approximately 1000 individuals after recovering from a 

severe decline (Quintana-Rizzo & Reynolds III, 2007). The 

low levels of haplotype diversity, microsatellite heterozygosity 

and allelic variation found in the Belize manatee 

population are characteristic of small, isolated populations 

enduring bottlenecks or long-term persecution (Jamieson, 

Wallis & Briskie, 2006). 

Belize manatees have lower levels of diversity than other 

endangered or bottlenecked populations (Gebremedhin 

et al., 2009), including a koala population on French Island, 

Australia, which was colonized by three animals (HE=0.48, 

N A=3.8, 15 loci; Cristescu et al., 2009), the Wanglang giant 

panda (HE=0.68, NA=6.2, 13 loci; He et al., 2008), and the 

East African cheetah (HE=0.47, NA=3.55, 82 loci; 

Figure 3 Plot of mean and standard deviation of the posterior probabilities, L(K), among STRUCTURE 2.3.3 runs for each value of K (1–10) for (a) 

Florida and Belize and (b) Belize alone. Plot of DK versus K for (c) Florida and Belize and (d) Belize alone. 



Driscoll et al., 2002). Examples of species with lower 

diversity than the Belize manatee include the Mediterranean 

monk seal (HE=0.41, NA=2.3, 15 loci; Paster et al., 2004) 

and the critically endangered Amur leopard (H E=0.37, 

NA=2.6, 25 loci; Uphyrkina et al., 2002). 

The Belize population was also found to have reduced 

variation compared with other marine mammal populations. 

Trichechus manatus latirostris currently has greater diversity 

and a quickly recovering large population, possibly owing to 

a shorter and/or less intense bottleneck period. Hunting of 

other marine mammal populations, such as the large cetaceans, 

occurred for a similar duration and intensity as for the 

Antillean manatee, and also resulted in the commercial 

extinction of many populations in the 1800s or 1900s. 

Populations with intense hunting and smaller historical 

sizes, such as the North Atlantic right whale (NARW), appear 

to have lost much of their diversity. The NARW was hunted 

for an extended period (11th–20th century) and was reduced 

from 12 000 individuals to the low hundreds, where it 

remains today (Waldick et al., 2002). The NARW genetic 

diversity reflects the extended and severe bottleneck the 

population has endured (NA=4.1, HE=0.46, 11 polymorphic 

loci). Alternatively, the related South Atlantic right 

whale population experienced less intense whaling that allowed 

the population to remain in the thousands and has 

higher genetic diversity (Waldick et al., 2002). Genetic studies 

have found large diversity, pre-whaling population estimates 

and recovered population sizes for fin (Berube et al., 1998), 

minke (Pastene, Goto & Kanda, 2009) and humpbacks whales 

(Garrigue et al., 2004), and suggest that the cessation of 

hunting in the early 20th century, allowed these populations 

to remain above 1000 individuals (Roman & Palumbi, 2003). 

Though it is reported as once being abundant in the 

Caribbean, T. m. manatus historical population sizes were 

not likely as large as some whale populations (Husar, 1977, 

1978). Further, a protracted period of severe hunting reduced 

the regional populations to o1000 individuals and in 

598 

Figure 4 Plot of posterior probability of assignment 

for individuals (vertical lines) based 

on Bayesian analysis of variation at 16 microsatellite 

loci. Individuals are grouped by population, 

(a) Belize and Florida and (b) the Belize 

City Cayes and Southern Lagoon System. Red 

indicates genetic cluster 1 and green indicates 

genetic cluster 2 in each plot. 

some cases to effective extinction (O’Shea & Salisbury, 1991; 

UNEP/CEP, 1995). This population contraction could have 

reduced the genetic diversity in Belize, which is below even 

that of the critically endangered NARW. However, lower 

dispersal and immigration capabilities in manatees may 

limit the exchange and development of inherent diversity in 

the taxa. 

The detected heterozygosity excess, mean pairwise values, 

and recent reduction in the population size suggests that a 

bottleneck/founder event, inbreeding, genetic drift and/or a 

reproductive skew has increased the relatedness among 

Belize manatees. Because diversity is considered necessary 

for adaptation to diseases and environmental changes, 

erosion of the currently low variation could negatively affect 

the population in the future (Reusch & Wood, 2007). 

Populations characterized by low diversity and past inbreeding 

are at risk for further losses and those not intensely 

monitored can become inbred with little warning (Frankham, 

1995; Bijlsma, Bundgaard & Boerema, 2000). Alternatively, 

inbreeding accumulating gradually in populations 

can provide the opportunity for natural selection to remove 

deleterious alleles. To date, there are no indications of 

decreased fitness due to inbreeding depression in the Belize 

population. However, further reduction of population size 

could increase inbreeding above the ‘inbreeding threshold,’ 

resulting in loss of fitness and risk of extinction (Frankham, 

1995). Further monitoring could help to detect inbreeding 

depression or declines in population size (Schwartz, Luikart 

& Waples, 2007). 

The immigration of genetically distinct individuals can 

substantially reduce the deleterious effects of inbreeding 

(Frankham et al., 2002). However, the enhancement of 

diversity through this mechanism is limited since many 

manatee populations are small, isolated and movement is 

restricted by their dependence on fresh water. Manatees 

prefer near-shore habitat, have limited coastal ranges and 

infrequently move long distances, highlighting the need for 



detection and management of genetically isolated populations 

(Lefebvre et al., 2001; Vianna et al., 2006; Quintana- 

Rizzo & Reynolds III, 2007). 

Genetic population structure 

Genetic differentiation, private alleles and a strong discrepancy 

in haplotype proportions indicate restricted admixture 

between the BCC and SLS regions (Table 2). A 

significant Mantel test suggests a potential barrier to gene 

flow and isolation by distance. The BCC and SLS had 

disparate proportions of haplotypes, J01 (79%) and A04 

(65%), respectively, and greater mtDNA FST values than 

microsatellite FST values, indicating female philopatry and 

male-biased gene flow. These data also suggest a larger 

number of individuals moving from SLS to BCC. Limiting 

human activity in the Bar River and Belize River corridors 

might encourage movement and breeding between the SLS 

and BCC, leading to greater genetic diversity. 

Mitochondrial DNA haplotypes have been analyzed 

throughout the manatee range and the A03 haplotype has 

been found exclusively in the SLS (presented here; Vianna 

et al., 2006), suggesting that A03 females remain isolated, 

although further analyses of samples from the region are 

needed. Reduced movement has also been observed in manatees 

tracked using VHF, GPS or UHF transmitters. The 

majority of manatees tagged had strong site fidelity, many 

remaining within a 15 mile radius of the tagging location (Auil 

et al., 2007). The distinct habitats and lack of movement and 

admixture indicate that protection and preservation of the 

population as at least two genetic populations would best 

protect the discrete diversity in each region. 

The increasing incidence of boat strike near Belize City 

could quickly erode the BCC population size and diversity 

(O’Shea & Salisbury, 1991; Auil, 1998, 2007). The recovered 

carcasses from the Belize River mouth or to the south were 

not statistically different from the BCC samples. The identified 

cause of death in the carcasses was boat strike or 

undetermined due to decomposition, corresponding to the 

high boat traffic near the mouth of the Belize River. 

Phylogeographic relationships 

Recently, known Florida manatees have been documented 

traveling great distances from Florida, including, Cuba, the 

Bahamas and Rhode Island (Reid, 2000; Deutsch et al., 

2003; Alvarez-Alemán, Powell & Beck, 2007). Florida 

manatees could potentially travel to Mexico along the Gulf 

of Mexico coast or by way of the Yucatán Peninsula. In fact, 

Mexico and Florida manatees share the A01 mitochondrial 

haplotype, possibly relating the two populations. However, 

although gene flow between Florida and Belize through 

Mexico is possible, the nuclear and mitochondrial DNA 

data do not support admixture, indicating possible barriers 

to gene flow (Domning & Hayek, 1986). 

Radio-tracking technologies have documented manatees 

traveling between Mexico and Belize (Auil et al., 2007; 

Morales-Vela et al., 2007). Although these movements have 

been tracked and the populations share two haplotypes, each 

country also contains a private haplotype (A01 and A03, 

respectively; Vianna et al., 2006), suggesting a paucity of 

female gene flow and incomplete genetic mixing. The limited 

relatedness of the three West Indian populations illustrates the 

historically low vagility and genetic exchange of the species. 

Future directions 

Quantifying the degree of migration and diversity in the 

Wider Caribbean using genetic tools is recommended to 

clarify the current and future role Belize may play in 

maintaining the Antillean subspecies in the region. Additionally, 

a more thorough examination of genetic connectedness 

among West Indian manatee populations 

throughout the range will assist in determining breeding 

populations and appropriate units of management for conservation. 

Further nuclear studies are anticipated to provide 

more detail on the genetic relationships. Identification of 

isolated or fragmented populations is important as lack of 

gene flow has significant deleterious effects on inbreeding, 

fitness and population sustainability (Frankham, 1995; 

Frankham et al., 2002). The growth and expansion of the 

Belize manatee population could also assist in the repopulation 

of small or functionally extinct Antillean manatee 

populations throughout the Wider Caribbean region 

(O’Shea & Salisbury, 1991; Bonde & Potter, 1995). 


This work was conducted under the USFWS Wildlife Research 

Permit MA791721, issued to the USGS, Sirenia Project. 

Funding for this project was provided by the USGS, and 

the University of Florida College of Veterinary Medicine 

Aquatic Animal Health Program. We would like to thank 

the Belize Manatee Project that provided access to genetic 

samples, logistical support and permission to collaboratively 

work under their Belize Forestry Department scientific collection 

and research permits CD/72/02 and CD/60/3/03 with 

subsequent amendments issued to N. Auil-Gomez and J.A. 

Powell. Additionally, Ginger Clark with the UF ICBR and 

Sean McCann provided critical technical assistance and 

Martha Sudholt and Susana Caballero provided helpful 

editorial recommendations. Any use of trade, product, or firm 

names is for descriptive purposes only and does not imply 

endorsement by the US Government. 

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Tourism and wildlife habituation: Reduced population fitness 

or cessation of impact? 

J.E.S. Higham *, E.J. Shelton 

Department of Tourism, School of Business, University of Otago, P.O. Box 56, Dunedin, New Zealand 

article info 

Article history: 

Received 17 August 2010 

Accepted 15 December 2010 

Keywords: 

Tourism 

Wildlife 

Habituation 

Stimulus control 

Tolerance 

Sensitisation 

Management 

1. Introduction 

abstract 

The concept of wildlife habituation traditionally has been treated 

uncritically within the field of nature-based tourism (Edington & 

Edington, 1986; Shelton & Higham, 2007). Typically the concept of 

habituation is accepted as a unitary phenomenon that is a negative 

possible consequence of tourist interactions with animals in the wild 

(Higginbottom, 2004; Newsome et al., 2005; Shackley, 1996). This 

global and stable behavioural descriptor, habituation, is an unhelpful 

way to formulate most observed lack-of-wildlife-response to 

human interactions. A more fine-grained behavioural and temporal 

approach to understanding wildlife habituation may be of considerable 

relevance to the optimal management of tourist interactions 

with wild animals. 

This paper attempts two points of departure from established 

discourses on wildlife habituation. The first challenges the contrast 

between the use of habituation in zoological studies (e.g. to mitigate 

researcher impacts), and the treatment of habituation in tourism 

management as entirely undesirable (Seddon, Ellenberg, & van 

Heezik, in press). Second, it asks if in some instances habituation 

* Corresponding author. 

E-mail addresses: james.higham@otago.ac.nz, jhigham@business.otago.ac.nz 

(J.E.S. Higham), eric.shelton@otago.ac.nz (E.J. Shelton). 

0261-5177/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. 

doi:10.1016/j.tourman.2010.12.006 

Tourism Management 32 (2011) 1290e1298 

Contents lists available at ScienceDirect 

Tourism Management 

journal homepage: www.elsevier.com/locate/tourman 

Habituation typically is viewed as a negative consequence of human interactions with wildlife 

(Higginbottom, 2004; Newsome, Dowling, & Moore, 2005; Shackley, 1996). While animal habituation 

commonly is used in the laboratory and field-based zoology studies, attempts to consider deliberate 

habituation specifically in a tourism management context (Shelton, Higham, & Seddon, 2004) has been 

received unsympathetically by biological scientists and wildlife managers on the grounds that habituation, 

by definition, is undesirable. This paper puts forward the case that the global and stable behavioural 

descriptor, habituation, is not the most useful way to formulate most observed lack-of-wildlife-response to 

visitor approach and observation. It presents an applied behaviour analysis of wildlife habituation that is 

situated within learning theory. This analysis differentiates between avoidance/approach behaviours, 

tolerance, habituation and sensitisation. This provides a formulative framework for humanewildlife 

interactions, that is then considered specifically in terms of tourism businesses seeking to provide 

sustainable visitor interactions with wild animals. A tourism management model derived from this critique 

of habituation is presented and discussed. 

Ó 2011 Elsevier Ltd. All rights reserved. 

may be deployed as a deliberate tourism management strategy in 

pursuit of cessation of visitor impacts upon focal animals (Nisbet, 

2000). These discussions draw upon three sources; thousands of 

unstructured personal observations on the part of the authors 

derived from employment as wildlife tour guides in New Zealand; 

extensive in situ personal observations of humanewildlife encounters 

in New Zealand including New Zealand’s sub-Antarctic Islands, 

and Ross Sea Dependency (Antarctica); and key empirical literature 

(e.g. Bejder, Samuels, Whitehead, Finn, & Allen, 2009; Ellenberg, 

Mattern, Seddon, & Jorquera, 2006; Johns, 1996; Knight, 2009; 

Romero & Wikelsi, 2002). The discussions that follow draw upon 

person observations unless indicated otherwise through reference 

citation. 

2. Ecotourism and wildlife encounters 

Wildlife viewing, once the domain of dedicated enthusiasts, or 

‘specialists’ (Duffus & Dearden, 1990), has moved into the mainstream 

of commercial tourism (Knight, 2009). With this has come 

a proliferation and diversification of opportunities to encounter 

wildlife (Higham, Lusseau, & Hendry, 2008). This course of development 

has occurred despite an inescapable tension. Knight (2009: 

p. 167) identifies a fundamental contradiction in wildlife viewing in 

that “wild animals are generally human-averse; they avoid humans

and respond to human encounters by fleeing and retreating to 

cover”. A gradual reduction of such avoidance commonly is labelled 

habituation. However humanewildlife encounters represent 

a complexity of interaction stimuli that render the unitary term 

habituation problematic (Bejder et al., 2009). With this point in 

mind, it is surprising that wildlife habituation continues to be 

treated uncritically within the context of nature-based tourism and 

sustainable tourism management. 

Successful commercial wildlife viewing requires that visitors are 

concentrated in well-defined locations where interactions with 

wild animals are predictable and constant (Whittaker, 1997). 

Usually, viewing wildlife takes place where sightings are most 

consistent, focal animals can be viewed in abundance or, where 

spectacular behaviours may be predictably observed and experienced 

(e.g. courtship and socialising behaviours). The critical nature 

of these sites, in terms of site ecology and wildlife behaviours, raises 

two important points; (1) That the behavioural state of wild animals 

varies significantly over time (e.g. across times of day, through 

different stages of the breeding cycle and across life course) and (2) 

that animal responses to external stimuli (e.g. the presence of 

tourists) is likely to vary over time, as influenced by these temporal 

determinants. 

These points raise the challenge of understanding and 

responding to the potential adverse impacts of humanewildlife 

interactions, not only for the sake of the focal animals, but also from 

an experiential standpoint with the aim of (1) reducing avoidance, 

flight or retreat responses and (2) mitigating adverse impacts on 

animals that may otherwise discontinue critical, site-specific 

behaviours e.g. by instigating site abandonment. Furthermore, 

increasingly tourists seek to be assured that their mere presence at 

wildlife viewing sites (and their associated behaviours) are not to 

the detriment of the animals that they seek to experience first hand, 

either in terms of the welfare of individual animals or wider population 

fitness (Higham & Lusseau, 2004; Muloin, 1998). 

Such concerns on the part of tourists (and site managers) are well 

founded. Knight (2009) critiques the dichotomy between wildlife 

viewing and wildlife hunting as non-consumptive and consumptive 

respectively, highlighting that viewing and hunting wildlife have 

some fundamental similarities. First, both engage in locating and 

identifying target wild animals, which are generally “wary of human 

presence and reluctant to expose themselves to human eyes” 

(Knight, 2009: p. 169). Such wariness may be expressed through 

anti-predatory adaptations, both physical (e.g. camouflage colouration) 

and behavioural (e.g. concealment) to avoid detection. The 

directed, intensive and sustained tourist gaze offers a second 

parallel with hunting (and predation more generally), which also is 

likely to trigger alarm and anti-predatory responses in individual 

animals or groups of animals. 

Tourist satisfaction is commonly associated with close-up, 

unconstrained and prolonged interactions with wild animals, the 

experience of critical behaviours (e.g. hunting, feeding, socialising 

and courtship) and, in some cases, immediate proximity extending 

to touch (e.g. Muloin, 1998). Although there are some exceptions to 

this rule (Orams, 2000), the importance of managing ‘humane 

wildlife viewing interactions’ (as opposed to ‘non-consumptive 

viewing’ e given the consumptive nature of pursuit, intensive gaze 

and proximal interaction) is evident. Knight (2009: p. 173) proposes 

that “there appear to be three main ways in which wild animals can 

be made available for human viewing: capture and confinement; 

habituation and attraction.” 

The first, capture and confinement, brings with it behavioural 

diminution associated with wild animals being physically removed 

from their natural ecosystem. Also, in many cases, the capture and 

confinement of ‘charismatic’ wild animals is illegal. The last, attraction, 

through interventions such as provisioning (i.e. feeding) is 

J.E.S. Higham, E.J. Shelton / Tourism Management 32 (2011) 1290e1298 1291 

equally unpalatable due to its association with manipulated wildlife 

distributions, compromised feeding (e.g. predatoreprey) relationships, 

increased probability of aggressive behaviour (both towards 

animals and people) and consequential diminished behaviours 

(Orams, 1995). Attraction of animals through supplemental feeding, 

while affording close and enduring viewing opportunities, also 

compromises the notion of wild, creating indistinct dividing lines 

between animals that are wild and those that are confined, tamed or 

domesticated (Knight, 2009). Of the three approaches to making 

wild animals viewable, this leaves habituation. 

Habituation has been defined as “a decrease in the strength of 

a response after repeated presentations of a stimulus that elicits that 

response” (Mazur, 2006). As such, habituation typically is viewed as 

a negative consequence of human interactions with wildlife due to 

the likely consequential reduction of population fitness arising from 

reduced danger flight response. However, habituation has been 

actively applied by zoological scientists in their field studies (i.e. in 

the wild), having been pioneered by primatologists such as Jane 

Goodall (Tanzania) working with chimpanzees (Pan troglodytes) and 

Dian Fossey (Rwanda) with gorillas (Gorilla gorilla) (Knight, 2009). 

Interestingly, Fossey’s habituation of Gorillas made possible the 

development of Gorilla tourism as an alternative to Gorilla poaching 

(Shackley, 1995). Yet habituation has never been treated critically in 

the specific context of sustainable commercial wildlife viewing 

(Nisbet, 2000). 

The relationship between tourists and wild animals is extremely 

complex (Bejder et al., 2009). Duffus and Dearden (1990) contend 

that this complexity arises from the interplay of three key components 

of the wildlife experience; site users, focal wildlife species 

(both individual animals and local animal populations) and the wider 

ecology of the viewing site. Given these components, considerations 

of habituation in ecotourism can be contemplated only in terms of 

site users (e.g. visitor management, guiding practice), the focal 

wildlife population (i.e. species-level variables and characteristics of 

individual animals) and the wider ecology of the focal species (e.g. 

spatio-temporal ecology) (Higham et al., 2008). Duffus and Dearden 

(1990) highlight also the temporal dimension in so far as tourist 

interactions with wildlife animals vary within diurnal, seasonal and 

life course timeframes, a point that has been inadequately addressed 

in academic discussions of habituation (Bejder et al., 2009). 

Following Duffus and Dearden (1990) then, some species of wild 

animals, and some individual animals, demonstrate a well-established 

response of inquisitiveness to humans or signs of human 

activity. Others are intensely private, remain concealed from 

onlookers, and flee readily from human interaction. In terms of 

inquisitiveness and active interaction, gulls are a ubiquitous example 

but rarely are gulls the focal species of interest to ecotourism operators 

and their visitors (Shelton & Higham, 2007). Useful approaches 

to the task of analysing the behaviour of species that are of tourist 

interest should, however, prove to be of considerable value. 

Applied behaviour analysis, based on the notion of stimulus 

control and situated within learning theory, is well suited to provide 

a formulative framework for those humanewildlife interactions that 

are of interest to commercial tourism operators. In this respect, the 

term habituation has been described as any situation where wildlife 

come to tolerate the presence of humans without any obvious signs 

of physiological or behavioural response (Shackley, 1996). Under this 

definition, habituation may be considered a mitigation or cessation 

of impact. The use of the term habituation in tourism and recreation 

has been applied also when animals approach people, or scavenge 

for food (Newsome et al., 2005). Park managers in North America 

attempt to educate the public not to engage in behaviours that will 

merge habituation and approach-for-food, particularly in the case of 

deer (The National Park Service, 2006a, 2006b) and bears (Davis, 

Wellwood, & Ciarniello, 2002).

1292 

To be as useful as possible, habituation must be distinguished 

from foraging or increased approach behaviour, even though the 

three phenomena regularly occur together (Davis et al., 2002). The 

starting point for such an undertaking is a critical behavioural 

analysis of wildlife habituation. In response to this need, a critical 

discussion of animal responses to human presence in presented, in 

order to achieve a more fine-grained understanding of habituation 

in all of its complexity. This critique provides a platform from which 

then to consider habituation within the context of sustainable 

wildlife tourism management. 

3. A behavioural formulation of wildlife habituation 

A behavioural formulation of wildlife habituation should begin 

by acknowledging the poor fit between observable animal behaviour 

and internal state (Ellenberg et al., 2006). In other words, the 

apparent tolerance of some wildlife species to approach and 

observation may not necessarily mean that these wild animals are 

not being impacted. Bejder et al. (2009) explain that wildlife tolerance 

of human stimuli may arise from various factors including: 

(1) Displacement: e.g. less tolerant individual animals may be 

displaced, resulting in a bias towards more tolerant animals 

that remain at a given site. 

(2) Physiology: e.g. reduced responsiveness to human stimuli due 

to physiological impairment. 

(3) Ecology: e.g. lack of suitable adjacent habitat to which animals 

may otherwise relocate. 

This poor fit has been demonstrated in the case of penguins 

(Ellenberg et al., 2006) where artificial eggs placed under incubating 

birds record elevated heart rate in birds that outwardly appeared to 

be unaffected when approached (Nimon, Schroter, & Stonehouse, 

1995). An understanding of habituation must acknowledge both 

the presence and absence of specific behaviours, and that impacts of 

significance at both the individual and species level may arise from 

both behavioural classes. The presence or absence of behaviours 

may vary at different scales of analysis, from individual animals to 

Table 1 

A critical behavioural formulation of the unitary term habituation. 

J.E.S. Higham, E.J. Shelton / Tourism Management 32 (2011) 1290e1298 

entire populations (Bejder et al., 2006; Lusseau, 2003; Shelton & 

Higham, 2007), and is dynamic over time. Following Bejder et al. 

(2009), a behavioural formulation of habituation in the specific 

context of wildlife-based tourism may be presented in four parts; 1. 

Avoidance/approach behaviours, 2. Tolerance, 3. Habituation and 4. 

Sensitisation (Table 1). 

3.1. Avoidance/approach behaviour 

An important starting point for any critical discussion of habituation 

is an understanding of the complexity of avoidance and 

approach behaviours. The avoidance behaviours of cetaceans when 

engaged in interactions with tourist vessels have been particularly 

well researched (Baker, Perry, & Vequist, 1988; Corkeron, 1995; 

Lusseau, 2003; Salden, 1988; ). Although responses to boat traffic 

vary between species, some show signs of active avoidance, ranging 

from altered movement patterns (Bejder, Dawson, & Harraway,1999; 

Campagna, Rivarola, Greene, & Tagliorette, 1995; Edds & MacFarlane, 

1987; Nowacek, Wells, & Solow, 2001; Salvado, Kleiber, & Dizon, 

1992), increases in dive intervals (Baker & Herman, 1989; Baker 

et al., 1988; Blane, 1990; Janik & Thompson, 1996; MacGibbon, 

1991) and increases in swimming speed (Blane & Jaakson, 1995; 

Williams, Trites, & Bain, 2002). Avoidance behaviours in Bottlenose 

dolphins (Tursiops truncatus) have been shown to vary at an individual 

level (Lusseau, 2003), where male animals show a greater 

propensity to avoid boat traffic than females with calves (see Higham 

& Lusseau, 2004). 

These studies present clear evidence of animal avoidance 

behaviours, not only as a result of the presence of boats, but also 

arising from the manoeuvring of boats, including sudden changes 

in vessel speed and rapid approaches (Constantine, 2001; Gordon, 

Leaper, Hartley, & Chappell, 1992; MacGibbon, 1991). In 2006, the 

International Whaling Commission reached agreement that “there 

is compelling evidence that the fitness of individual odontocetes 

repeatedly exposed to whale-watching vessel traffic can be 

compromised and that this can lead to population-level effects” 

(IWC, 2006). This consensus has been reached in light of recent 

studies that suggest avoidance responses from cetaceans when 

Concept Variables Cases 

1. Avoidance/approach Avoidance response (e.g. pre-emptive avoidance) Male Bottlenose dolphins (Tursiops truncatus) 

behaviour 

Response behaviours (e.g. generalised vigilance, concealment, 

discontinuation of critical behaviours) 

Male Bottlenose dolphins (Tursiops truncatus) 

Stimulus control (i.e. group and individual behaviours) Adele penguins (Pygoscelie adeliae); Little penguins 

(Eudyptula minor); Bottlenose dolphins (Tursiops truncatus) 

Exploratory approach behaviour Elephant seal (Mirounga leonine) 

Opportunistic approach behaviour Buller’s mollymawk (Diomedea bulleri); Giant petrel 

(Macronectes giganteus) 

Discriminative stimulus Fantail/piwakawaka (Rhipidura fuliginosa); Southern Royal albatross 

(Diomedea epomophora) 

2. Tolerance Intrinsic tolerance Little penguins (Eudyptula minor); Spotted shags 

(Stictocarbo punctatus); Stewart Island shags 

(Leucocarbo chalconotus); Little shags (Phalacrocorax melanoleucos) 

Selective tolerance New Zealand sea lion (Phocarctos hookeri) 

Seasonal tolerance New Zealand wood pigeon/kereru (Hemiphaga novaseelandiae) 

3. Habituation Approach habituation New Zealand dabchick (Poliocephalus rufopectus) 

Spatio-temporally bound habituation Colonial breeding female New Zealand fur seal (Arctocephalus forsteri). 

Socially acquired absence of avoidance behaviour New Zealand fur seal (Arctocephalus forsteri) neonates 

Socially acquired habituation Female New Zealand fur seal (Arctocephalus forsteri) 

(e.g. new colony recruits) 

Reduced physiological arousal Northern Royal albatross (Diomedea epomophora sanfordi) 

Reduced avoidance behaviour Yellow-eyed penguin (Megadyptes antipodes) 

4. Sensitisation Sensitisation Stoats(Mustela erminea) (i.e. in the laboratory) 

Paradoxical sensitisation Galapagos marine iguana (Mblyrhynchus cristatus)

tourist vessels are present, and that those responses disrupt the 

behavioural budgets of affected animals. Repeated disturbance can 

then lead to displacement from preferred habitat and reduced 

fitness at the population level (Bejder et al., 2006) as opposed to 

any evidence of habituation. 

3.1.1. Stimulus control 

The presence or absence of avoidance/approach behaviours 

might usefully begin with the treatment of stimulus control. This 

term may be used to describe naturally-occurring wild animal 

behaviours that are resistant to modification. Adele penguins 

(Pygoscelie adeliae) launching from an Antarctic ice floe engage in 

grouping and rushing behaviours, presumably to reduce the likelihood 

of fatal attack by predators such as Leopard seals (Hydrurga 

leptonyx). The same stimulus control applies to Little penguins 

(Eudyptula minor) at tourist sites such as the Philip Island Penguin 

Parade (Victoria, Australia) and Oamaru Blue Penguin Colony (New 

Zealand). In this instance proximity to the landing site and 

grouping induces a rushing response which is unchanged despite 

millions of unchallenged landings over many generations of birds 

(Houston & Russell, 2000). This failure to habituate to coastline 

proximity has no obvious evolutionary cost to the species. The 

lighting, public address systems and grandstands full of visitors at 

these sites do not deter the birds from landing where they have, in 

recent history, always landed. This lack of avoidance response has 

not changed over time and is uniquely characteristic of this species 

of penguin which does not demonstrate habituation of approach or 

avoidance behaviour. 

Another relevant case involves cetaceans. Lusseau’s (2003) 

study of Bottlenose dolphins (Tursiops truncatus) in Doubtful 

Sound (Fiordland, New Zealand) found that these marine mammals 

entertained visitors on tour boats with their bowriding and leaping 

out of the water, such that it might be assumed that dolphins 

engage in this behaviour by choice. Power boats, though, act as 

a stimulus for dolphins not to rest; that is, bowriding and leaping 

are more likely to be under stimulus control and therefore not the 

result of choice. There are clear potential negative impacts of 

decreased resting on this species, including a disrupted energy 

budget and likely compromised reproductive success (Lusseau & 

Higham, 2004). 

Repeated exposure to tourist vessels does not seem to reduce 

the strength of the dolphins’ approach responses and this situation 

clearly demonstrates the difficulties inherent in referring to stable 

or increasing approach behaviour as habituation. Lusseau and 

Higham (2004) suggest the spatial segregation of non-permitted 

boats and Bottlenose dolphins through multi-level zoning. An 

additional management strategy could, in this case, include 

inducing habituation via stimulus mitigation; that is, reducing the 

dolphin’s responsiveness to the presence of tourist vessels through 

the close management of key stimuli (e.g. boat speed and noise) so 

as to counter the stimulus control that these animals appear to act 

under. 

3.1.2. Exploratory approach behaviour 

A further manifestation of approach/avoidance behaviour, with 

an apparent temporal (i.e. life course) dimension may be termed 

exploratory approach behaviour. Elephant seals (Mirounga leonine) 

on sub-Antarctic Campbell Island may be exposed fleetingly to two 

or three groups of visitors per year at North West Bay (and not at all 

elsewhere on Campbell Island). Juvenile Elephant seals will 

approach and investigate tour parties at close range. The lack of 

similar interest on the part of adult Elephant seals very probably 

reflects a decreasing exploratory behaviour as a consequence of 

maturation rather than through habituation (i.e. repeated exposure 

to humans) where tourist encounters are so uncommon. 


This change in responsiveness raises important questions 

around the naturally-occurring contingencies and physiological 

processes that operate to reduce exploratory behaviour during 

maturation from neonate through juvenile to adult. Repeated nonconsequential 

exposure to a range of human behaviours should be 

situated somewhere in this process. On mainland New Zealand, 

where tourist encounters are more common, adult Elephant seals 

will rest ashore, selecting where possible confined and inaccessible 

resting sites, and demonstrating complete indifference to approach, 

based on a confidence of remaining unmolested. This indifference 

may be understood as reduced exploratory approach behaviour 

rather than habituation. 

3.1.3. Opportunistic approach behaviour 

The term opportunistic approach behaviour may be used to 

address approach stimuli linked to an individual’s energy budget. 

Offshore boat-based tourist encounters with some seabird species 

such as Buller’s mollymawk (Diomedea cauta eremita) may result in 

close but fleeting observations of birds derived from what may be 

descried as ‘investigatory fly past’. Opportunistic approach behaviour 

may be a generalisation from the birds’ habit of following fishing 

boats whose crews routinely engage in gutting offshore. Giant 

petrels (Macronectes giganteus) also will engage in this behaviour. 

Distinct from provisioning and scavenging, these birds approach in 

response to a specific stimulus. Despite daily exposure to the tourist 

boat, and never having been fed, this exploratory approach behaviour 

persists over time. Due no doubt to a failure to distinguish 

between tourist vessels and fishing boats, and with so little energy 

required to complete an investigation, these birds, as an optimal 

feeding strategy, casually and routinely approach every boat. 

3.1.4. Discriminative stimuli 

Related to this, approach behaviours may be further differentiated 

from habituation via an understanding of discriminative 

stimuli. The behaviour of fantails/piwakawaka (Rhipidura fuliginosa) 

is typically misleading. Visitors often encounter the situation where 

they are walking along a bush track and suddenly numerous 

fantails appear and flutter tantalisingly close-by. Many may incorrectly 

assume that it is their presence that has attracted the birds 

which are attracted to human presence. Rather, the birds are 

attracted to small flies that have risen from the leaf litter as a result 

of human disturbance. The attraction to visitors in the bush is 

indirect. People in this case act as a discriminative stimulus for 

a likely disturbed forest floor, and consequently available prey. 

Similarly, Southern Royal albatrosses treat private boats as 

discriminative stimuli for fish being scaled and gutted and land in 

their wakes. These examples only serve to further confirm the poor 

fit between observable behaviour and internal state in terms of 

understanding animal behaviours in the wild. 

3.2. Tolerance 

3.2.1. Intrinsic tolerance 

Within investigations of humanewildlife interactions the 

apparent tolerance of wild animals to human approach has 

remained almost entirely undifferentiated from habituation. The 

exception is Bejder et al. (2009: p. 181) who define tolerance as the 

“intensity of disturbance that an individual. tolerates without 

responding in a defined way”. Tolerance may readily be confused 

with the complete absence of tourist impact. Indeed Higham 

(1998:529), in reference to viewing Northern Royal albatrosses 

(Diomedea epomophora sanfordi), warned that “tolerance should not 

disguise the fact that serious impacts may still take place”. The 

manifestations of disturbance in the case of these outwardly 

tolerant birds have been revealed only by long-term monitoring and

1294 

analysis (Higham et al., 2008). A more critical treatment of tolerance 

allows, in the first instance, for consideration of intrinsic tolerance, 

which varies both between individual animals and species. 

Many species of seabirds will demonstrate intrinsic tolerance to 

boat approach, seemingly oblivious to engine vibration and noise 

(both mechanical and human). Little penguins (Eudyptula minor) 

demonstrate intrinsic tolerance of boat engine vibration and noise, 

which indicates that they clearly are able to ignore human presence 

across settings (i.e. coastal landing zones and open water). Various 

species of New Zealand shag (cormorant) also demonstrate 

intrinsic tolerance to human approach (e.g. Spotted shags (Stictocarbo 

punctatus), Stewart Island shags (Leucocarbo chalconotus) and 

Little shags (Phalacrocorax melanoleucos)) (Shelton & Higham, 

2007). However tolerance inevitably is behaviour (stimulus) 

specific. Supporting Knight’s (2009) treatment of the tourist gaze is 

the fact that an intense and prolonged stare is sufficient to cause 

some individual birds (e.g. Spotted shags) to abandon their perches. 

3.2.2. Selective tolerance 

Tolerance, like habituation, has a spatio-temporal component. 

Solitary adult male New Zealand sea lions (Phocarctos hookeri) 

demonstrate various responses to human approach which may be 

termed selective tolerance (or intolerance). Some adult male New 

Zealand sea lions will, when in the water in the autumn months, 

respond intolerantly (e.g. aggressive approach, charging and biting) 

to the passing kayaks of a commercial operator. Repeated exposure 

to kayakers, at this time of year, does not decrease the likelihood of 

aggressive behaviour. At other times of the day when hauled out on 

a nearby beach the same individual animals will tolerate close 

approaches by visitors (Shelton & Higham, 2007). The sharp 

contrasts between agonistic and indifferent responses (which 

clearly vary on a spatio-diurnal basis) are almost certainly linked to 

specific spatio-ecological (i.e. territorial dominance) and temporal 

(i.e. reproduction) elements. 

3.2.3. Seasonal tolerance 

A variation of selective tolerance is seasonal tolerance. The New 

Zealand wood pigeon/kereru (Hemiphaga novaseelandiae) frequents 

some urban areas in New Zealand and can appear to be indifferent 

to everyday human activity. Closer analysis reveals seasonal variations 

in the species’ tolerance of human stimuli depending on food 

availability (Shelton & Higham, 2007). As the season progresses, 

and food becomes more abundant, kereru increasingly favour 

branches higher up in trees, and seasonal responses to human 

activity appear to change. 

In this case, it is clearly necessary to elucidate precisely what 

role people are playing as discriminative stimuli. People minding 

their own business, presumably measured by their unmodified 

patterns of movement, uninterrupted chatter and non-birddirected 

gaze, act as discriminative stimuli for approach tolerance. 

A sudden silence, ceasing walking, or bird-directed gaze act as 

stimuli for flight. The paradox for the commercial wildlife tourism 

operator who intends that visitors experience pigeons close-up is 

that the best advice to be given is to ignore them. Natural settings 

do not offer the frequency of close contact that would be required 

to attempt deliberately to manipulate the birds’ existing responses. 

These two examples illustrate a more general concern with how 

humans can best interact with multiple species of birds in urban 

areas (Blumstein, Fernandez-Juricic, Zollner, & Garity, 2005). 

3.3. Habituation 

3.3.1. Approach behaviour 

Bejder et al. (2009: p. 181) define habituation as the “relative 

persistent waning of a response as a result of repeated stimulation 


which is not followed by any kind of reinforcement”. Shackley 

(1996) observes that wildlife may habituate to the presence of 

humans, showing no obvious signs of physiological or behavioural 

response. If so, such a lack of response may fruitfully be explored 

within the context of sustainable wildlife tourism and cessation of 

impact. However, habituation can be assumed to have important 

spatio-temporal dimensions. New Zealand dabchick (Poliocephalus 

rufopectus) may become habituated to human approach following 

multiple exposures (Bright, Reynolds, Innes, & Waas, 2003). Similarly 

diurnal or seasonal habituation may take place in some species 

of wild animals under certain circumstances. Non-breeding male 

New Zealand fur seals (Arctocephalus forsteri) may be placid on 

land, where they demonstrate a decreased gross behaviour 

response to human approach. The same animals may be aggressive 

to swimmers in the water, which acts against describing any individual 

animals as being habituated. Nearby breeding colonies of 

female New Zealand fur seals that are exposed to regular stimuli 

may become unresponsive to approach. 

3.3.2. Socially acquired habituation 

Furthermore, there is evidence to suggest that the absence of 

response behaviours may be socially acquired or learnt (Bejder 

et al., 2009) by wild animals. Early exposure, in the presence of 

an unresponsive mother, may result in seal pups that have never 

perceived tourist approach as a stimulus for flight. Seal pups do 

vary in their post-weaning exploratory audacity and some, having 

moved around the site once in the presence of humans with no illeffects, 

begin to include indifference in their behavioural repertoire. 

Each uneventful visit further reduces the discriminative value of 

humans. Those adult females who had been born at the colony 

could conceivably retain their neonate indifference but those 

recruited from other colonies, where avoidance response to less 

frequent human approach takes place, may demonstrate socially 

acquired habituation through their peers modelling indifference. 

Such complexities of seal habituation to human approach, 

including the confounding effect of probable previous exposure, 

has been investigated by van Polanen Petel (2005) who suggests 

a species-specific approach is required in order to manage 

humaneseal interactions optimally. 

3.3.3. Reduced physiological arousal 

Habituation in the form of complete indifference may be 

usefully differentiated from reduced physiological arousal, in which 

behavioural responses remain evident, but with reduced energy 

expenditure and arousal. At Taiaroa Head (Dunedin, New Zealand) 

Northern Royal albatross (Diomedea epomophora sanfordi) are 

closely monitored (Higham, 1998) and tourists are confined to 

a soundproof hide glazed with reflective glass. Throughout the 

breeding season all individual birds in the colony are exposed to 

close contact and attention from conservation staff, including 

weekly handling during weighing and measuring. These birds do 

not abandon their nests but do continue the defencive use of their 

beaks, as do Northern Royal albatrosses on the remote Campbell 

Island. Despite having been handled periodically over the years 

since their hatching these birds did not seem to have habituated to 

this particular human behaviour. However, although there had 

been no apparent change in the gross motor component of the 

birds’ defence rituals, there may well have been reductions in 

human-induced physiological arousal. Thus, the defence behaviour 

persists, but with reduced determination or persistence. 

3.3.4. Reduced avoidance behaviour 

A fourth manifestation of habituation may be termed reduced 

avoidance behaviour. This arises in cases where approach/avoidance 

is at the discretion of individual animals. While it is conceivable

that approach behaviour may be habituated the more likely case in 

wild animal populations is that avoidance behaviour may decrease 

over time. This appears to be the case in Yellow-eyed penguin 

(Megadyptes antipodes) colonies that are exposed to increasing 

tourist interactions, where established members of the colony may 

become less timid over time, but there may be a simultaneous 

reduction in the recruitment of prospecting birds. The impact of 

humans on this most phlegmatic but inquisitive of penguins is the 

subject of ongoing study (Seddon, Smith, Dunlop, & Mathieu, 2004). 

This work is predicated on the fact that measuring penguin habituation 

using only approach/avoidance behaviour is inappropriate 

since physiological arousal fluctuates independently of observable 

behaviour (Ellenberg & Mattern, 2004) and the relationship varies 

both between individual penguins of the same species and different 

penguin species (Ellenberg et al., 2006). 

3.4. Sensitisation 

Finally, it is important to attempt to differentiate between 

sensitisation and habituation. Usually, sensitisation refers to an 

increase in the strength of a response upon repeated or ongoing 

exposure to a stimulus that has significant consequences (Bejder 

et al., 2009). However, it is noteworthy that repeated exposure to 

tourists appeared to lower the production of corticosterone, 

commonly a stress hormone, in Galapagos marine iguana (Romero & 

Wikelsi, 2002). Lower corticosterone production in response to 

human interaction, compared with animals who have no human 

interaction, seems to demonstrate sensitisation, the opposite of 

habituation, but in this case the lowering of corticosterone production, 

although demonstrating sensitisation, may legitimately be 

labelled paradoxical sensitisation. Of course one study is inconclusive 


but it does raise an intriguing possibility. If robust, this finding 

implies that chronic sub-optimal physiological processes may be 

a naturally-occurring phenomenon in some species of wild animals. 

4. Wildlife habituation and sustainable nature-based 

tourism: a management model 

This discussion addresses the proposition that ecotourism 

operators who are committed to providing a sustainable naturebased 

product will be interested to know how their activities may 

be influencing the environments in which they do business. The 

inherent tensions between business practice and sustainability in 

nature-based tourism have been well described (Fennell, 2003; 

McKercher, 1993a, 1993b, 1998; Newsome et al., 2005). The 

preceding discussions allow for the development of a management 

model for sustainable wildlife tourism interactions (Fig. 1) based on 

a critical behavioural formulation of habituation. 

Following Duffus and Dearden (1990) Fig. 1 is constituted 

principally by three key elements; site users, focal animals (individuals 

or local populations) and the wider ecology of the wild 

animals engaged with human approach and observation. Such 

a representation recognises that any humanewildlife interactions 

are spatially bound; that is, human interactions with individual 

wild animals can take place in a variety of settings that vary across 

a range of habitats where different behaviours (e.g. migration, 

feeding, resting, socialising, breeding, raising neonates etc.) take 

place. Animal responses to human approach and interaction inevitably 

vary between settings. 

The model recognises also the temporal variation that exists in 

terms both of site users (e.g. timing and duration of visit, and 

seasonal context), and focal animals (e.g. diurnal, seasonal and life 

Fig. 1. Management model for sustainable wildlife tourism interactions based on a critical behavioural formulation of the term habituation.

1296 

course), which influence the outcomes of humaneanimal interactions. 

Avoidance/approach behaviours, tolerance, habituation and 

sensitisation can fruitfully be considered within this context. 

A critical understanding of spatio-temporal ecology and the interactions 

of tourists and focal animals can then be applied in terms of 

tourism management planning and consideration of conscious 

management interventions (Fig. 1). This would require a critical 

understanding of the unitary term habituation, which is attempted 

in this article. It would also necessitate a mixed (biological and 

social) science platform of research to inform an integrated and 

adaptive management approach (Higham, Bejder, & Lusseau, 2009). 

5. Discussion 

As nature-based products are offered in more and more remote 

places (i.e. previously unexploited ecosystems) it becomes 

increasingly likely that any given individual animal will encounter 

humans, engaged in particular behaviours, at some stage of its life. 

The animal may approach the human, as neonates and juveniles of 

many species do. If, on repeated exposure to these particular 

human behaviours, this approach behaviour decreases, and is not 

replaced by escape/avoidance behaviour, then the animal may 

accurately be described as being habituated to the human behaviours 

to which it has been exposed, in a particular spatio-temporal 

setting. 

Any habituation/sensitisation process is dynamic, and may 

reflect the hormonal state of the individual animal at the time of 

exposure to the particular human behaviour. If the individual 

animal demonstrated indifference to the human behaviour right 

from the start then habituation is not the best term to use to 

describe the situation; tolerance or resilience may be more useful. 

Similarly, animals may respond to human activity through 

increases in physiological processes, commonly grouped under the 

term arousal. Decreasing physiological arousal upon repeated 

exposure indicates habituation, increased arousal indicates sensitisation. 

The unusual situation where an initially high level of 

arousal may be reduced by exposure to human activity may be 

tentatively labelled paradoxical sensitisation. It is possible also for 

wildlife to decrease one response to human presence, for example 

fleeing, but to increase another response. Chimpanzees’ activity 

rates in Kibale Forest, Uganda, habituate to the presence of 

increasing numbers of observers but vocalisation increases (Johns, 

1996). 

It is useful at this point to address two issues. Firstly, why is it 

important to specify to what human behaviours, in what settings 

and at what times do individual animals habituate, and to avoid the 

simpler descriptor; habituation to humans? Habituation to 

humans, by definition, involves decreased vigilance in response to 

human presence, decreased communication of alarm upon coming 

across humans and/or decreased avoidance of, or fleeing from, 

humans. The argument then is that habituated animals are made 

vulnerable in that habituation to one potential predator, Homo 

sapiens will induce a generalised reduction of predator-preparedness 

(Beale & Monaghan, 2004). 

We argue that this concern evaporates when habituation is 

more usefully formulated. If habituation is related to spatially and 

temporally constrained specific human behaviours, rather than 

simply to human presence, then it is reasonable to hypothesise that 

individual animals will retain predator-preparedness outside of 

these parameters. Discriminating between human behaviours is 

consistent with laboratory-based enquiry that has demonstrated 

that many species have the ability to discriminate even between 

individual human beings performing the same behaviours (Davis, 

2002). Predator-preparedness training in birds, in common with 

exploratory behaviours (Huber, Rechberger, & Taborsky, 2001), can 


occur through social learning. For example adult Sandhill cranes 

teach predator-preparedness by modelling vigilance and predatorresponse 

even to unrelated captive-reared conspecific chicks 

(Heatley, 1995). There is debate about how possible habituation to 

human activity acquired while in captivity, for example in a rehabilitation 

facility, should be managed. A fine-grained analysis is 

available addressing the issue of how much deliberate training-forrelease 

should take place, what such training should comprise, and 

exactly how humans should be involved in its delivery (Bauer, 

2005). 

It is reasonable to suppose that habituation can be socially learnt 

also in natural settings, and be passed on in a sophisticated rather 

than generalised way. Different species teach their offspring 

different sensitivities. For cliff-dwelling birds visited by tourists, 

size-of-party has been reported to have species-specific effects 

(Beale & Monaghan, 2005). It is not unreasonable to suggest that 

certain species may teach their young not to respond to a particular 

wildlife guide, acting within certain behavioural limits. In such 

cases it is critical that individual animals are the unit of analysis in 

rigorous longitudinal studies (Bejder et al., 2009). 

The second issue that needs to be addressed is one of 

management. If, as suggested here, some or all of the behaviours of 

many wild species can be brought under stimulus control, then 

what happens to the wild in wildlife? The application of stimulus 

control techniques to the management of human behaviour is 

widely reported in the Applied Behaviour Analysis literature. Using 

the nuanced approach to habituation outlined here it is conceivable 

that wildlife managers and visitor managers could co-operate to 

apply behavioural technologies to structure almost completely the 

nature of humanewildlife interactions site-by-site, species-byspecies, 

and in some cases to the level of individual animals, taking 

into account time of day and time of year. This level of management, 

although common in zoos and other captive settings, if 

applied to natural settings would challenge directly the motivation 

for visiting such sites in the first place. Nonetheless, in certain cases 

the conservation outcomes available using such an approach may 

be justified. 

6. Conclusion 

This article highlights the wide variability of wild animal 

responses to human approach and interaction. In doing so, it begs 

the question; which individual animals or groups of animals 

respond in what fashion to what kind of tourist behaviour in what 

contexts? Clearly individual (or groups of) animals that respond 

passively in one setting, may in other settings not be so sanguine. 

For example, where a particular set of contingencies operate to 

induce decreasing gross behavioural responsiveness, on land, to 

a fairly narrow set of visitor behaviours, in a group of seals who 

shared non-breeding status, evidence of spatially and temporally 

bounded habituation may exist. The responsiveness of physiological 

processes within individual seals, the role of developmental 

maturation and the influence of vicarious or social learning through 

the observation of calm conspecifics remain largely unexamined, 

although available for formulation. 

Clearly, a fine-grained behavioural approach is required to 

overcome the poor fit between observable wildlife behaviour in the 

presence of humans and individuals’ internal states, and to 

accommodate the fact that habituation is spatially and temporally 

bounded. Given that such a poor fit is unhelpful to individual, 

species or whole-of-ecosystem management, it seems desirable 

that ecotourism operators actively address likely habituation or 

other conditioning to humans as part of their business plan 

or concession application. As such, wildlife managers and visitor 

managers could co-operate to apply behavioural technologies

to structure almost completely the nature of humanewildlife 

interactions. A tourism management model that accommodates 

a nuanced understanding of wildlife habituation is presented, 

building upon a formulative framework for humanewildlife interactions. 

The development of empirical case studies to inform and 

monitor tour operator best practices is a valuable avenue of future 

research. 

Knight (2009) presents three approaches to making wildlife 

viewable; capture and confinement, habituation, and attraction. 

While of the three, habituation is the least likely to be associated 

with diminished behaviours, the question of diminished wildness 

remains unanswered. Exploring this question will, no doubt, reveal 

a trade off between using habituation as a tourism management 

tool and the potential evolutionary costs to focal animal populations, 

not only in terms of physiological and behavioural 

responses, but also in terms of exposure to disease (Bejder et al., 

2009). One provocative approach, integrated with the field of 

neurobiology, will be designer wild species, specifically habituated 

for viewing. Alternatively, Knight (2009) observes that learnt 

animal behaviours can be unlearnt, giving rise to the notion of the 

reversal of habituation. AsKnight (2009: p. 180) comments, “In an 

age when our visual appetite for wildlife has never been greater, 

there may be good reasons for keeping this appetite in check and 

acting to make viewable wild animals unviewable again”. Before 

further contemplating the reversal of habituation, a more critical 

understanding of habituation itself is required. This amplifies the 

need for “studies (that) adopt a long-term experimental design 

involving sequential sampling of the same individuals at different 

levels of exposure to a disturbance” (Bejder et al., 2009: p. 181). In 

the meantime, these thoughts pose intriguing questions that are 

available for scholars to debate and research. 

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MARINE MAMMAL SCIENCE, 27(3): 606–621 (July 2011) 

C○ 2011 by the Society for Marine Mammalogy 

DOI: 10.1111/j.1748-7692.2010.00435.x 

Using distance sampling techniques to estimate 

bottlenose dolphin (Tursiops truncatus) abundance 

at Turneffe Atoll, Belize 

DOROTHY M. DICK 1 

ELLEN M. HINES 

Department of Geography and Human Environmental Studies, 

San Francisco State University, 

1600 Holloway Avenue, 

HSS Room 279, 

San Francisco, California 94132, U.S.A. 

E-mail: doridick14@gmail.com 

ABSTRACT 

Reliable abundance estimates are critical for management and conservation of 

coastal small cetaceans. This is particularly important in developing countries 

where coastal human populations are increasing, the impacts of anthropogenic 

activities are often unknown, and the resources necessary to assess coastal cetaceans 

are limited. We adapted ship-based line transect methods to small-boat surveys 

to estimate the abundance of bottlenose dolphins (Tursiops truncatus) at Turneffe 

Atoll, Belize. Using a systematic survey design with random start and uniform 

coverage, 34 dolphin clusters were sighted during small-boat line transect surveys 

conducted in 2005–2006. Distance sampling methods estimated abundance at 216 

individuals (CV = 27.7%, 95% CI = 126–370). Due to species rarity in the 

Atoll, small sample size, and potential violations in line transect assumptions, the 

estimate should be considered preliminary. Nevertheless, it provides up-to-date 

information on the status of a regional population in an area under increasing threat 

of habitat loss and prey depletion via uncontrolled development and unsustainable 

fishing. This information will be useful as Belize develops a new conservation 

initiative to create a comprehensive and resilient marine protected area system. 

Our study illustrates the application of distance sampling methods to small-boat 

surveys to obtain abundance estimates of coastal cetaceans in a region lacking 

resources. 

Key words: survey design, small-boat surveys, distance sampling, line transects, 

Distance 5.0, abundance, bottlenose dolphin, Tursiops truncatus, Turneffe Atoll, 

Belize. 

1 Also affiliated with: Oceanic Society, Fort Mason Quarters 35, San Francisco, California 94123, 

U.S.A. Current address: Department of Geosciences, Geography Program, Oregon State University, 104 

Wilkinson Hall, Corvallis, Oregon 97331, U.S.A. 

606

DICK AND HINES: BOTTLENOSE DOLPHIN ABUNDANCE 607 

Although the common bottlenose dolphin (Tursiops truncatus) is well studied and 

widespread across various marine habitats in temperate and tropical waters (Wells 

and Scott 1999), its worldwide status is unknown. In the IUCN 2008 Red List of 

Threatened Species update, T. truncatus was classified as Species of Least Concern and 

listed habitat destruction and degradation, disturbance and harassment, prey depletion, 

pollution, and direct/indirect takes as specific threats of concern (Hammond 

et al. 2008). While these threats apply to the species as a whole, any one may impact 

certain regional populations more than others as seen in the Mediterranean (Bearzi 

and Fortuna 2006, Bearzi et al. 2008), Moray Firth, Scotland (Wilson et al. 1997, Sini 

et al. 2005), and Peru (Van Waerebeek et al. 1997). Declines in regional populations 

of apex predators, such as bottlenose dolphins, could have far reaching effects on 

the community structure of an ecosystem (Currey et al. 2009), as seen in western 

Alaska when increased killer whale predation on sea otters lead to a dramatic rise 

in sea urchins and subsequent decreases in kelp forests (Estes et al. 1998). For these 

reasons, coastal bottlenose dolphin populations should be assessed on a regional scale 

when evaluating status, managing threats, and implementing conservation measures 

(Reeves et al. 2003, Currey et al. 2009). 

The effects of anthropogenic activities on coastal bottlenose dolphin populations 

are of particular concern as human populations continue to grow along coastlines, 

especially in developing countries (Aragones et al. 1997, Dawson et al. 2008). The 

extent of these activities, however, is generally unknown and the data needed to 

substantiate the impacts are rarely available. Without adequate knowledge about 

the status and life history of these populations future management actions are limited. 

Consequently, there is a strong need to conduct population assessment studies 

on coastal marine mammal populations in underdeveloped countries (Vidal 1993, 

Aragones et al. 1997, Hines et al. 2005, Dawson et al. 2008). 

Line transect surveys using distance sampling protocols are a common method 

used to assess marine mammal populations (Buckland et al. 2001). Surveys of this 

type typically use large ships or fixed-wing aircraft, sophisticated equipment (high 

powered binoculars, navigational tools, e.g., radar and electronic charts), and may traverse 

sizeable ocean expanses (Barlow 1988, 1995; Barlow et al. 1988; Calambokidis 

and Barlow 2004; Forcada et al. 2004; Mullin and Fulling 2004; Zerbini et al. 2007). 

As a result they are prohibitively expensive and inaccessible to developing countries 

with limited budgets and expertise and shallow coastal regions (Dawson et al. 2008). 

Adapting ship-based line transect methods to small-boat surveys (Vidal et al. 1997; 

Dawson et al. 2004; Williams and Thomas 2007, 2009) may be the best option to 

estimate coastal marine mammal populations in less affluent nations. 

Turneffe Atoll (Fig. 1), located in Belize, Central America, is the largest most 

biologically diverse of the nation’s three atolls (Stoddart 1962) and the only one 

without long-term ecological protection. Turneffe Atoll provides year-round habitat 

to a small population of coastal bottlenose dolphins (Grigg and Markowitz 1997, 

Campbell et al. 2002). Photo-identification studies from the 1990s estimated a 

population of less than 90 individuals (Campbell et al. 2002). More than a decade 

later there have been no new abundance estimates. Protected from import/export, 

wildlife trade, and hunting by Belize’s 1981 Wildlife Protection Act, threats from 

human induced mortality are currently minimal. However, unsustainable fishing 

(overfishing and illegal fishing) and rapid coastal development (mangrove clearing, 

dredging, and overdevelopment) have been identified as severe threats to the ecological 

integrity of Turneffe Atoll (World Resources Institute 2005, Granek 2006). 

There is a high probability that the small dolphin population could be threatened by


Figure 1. The location of Turneffe Atoll, Belize, the survey design, and the bottlenose 

dolphin sighting locations during small-boat surveys conducted in 2005–2006. The survey 

was created with the automated survey design function in Program Distance 5.0 release 2 

using two substrata, the lagoon area and the western area between the mangrove cays and the 

fringing reef. 

habitat degradation, prey depletion, vessel traffic, and pollution as the atoll’s human 

population increases (Wells and Scott 1999). Obtaining an up-to-date abundance 

estimate for the population before further anthropogenic impacts occur is imperative 

to provide the baseline information necessary to guide future management and 

conservation actions.


We sought to (1) develop and implement a repeatable and economically feasible 

systematic survey for use on bottlenose dolphins at Turneffe Atoll, (2) provide the 

first non-mark-recapture quantitative estimates of dolphin abundance in the study 

area, and (3) develop survey methods potentially applicable for other small cetacean 

coastal surveys in underdeveloped countries. This project is part of a long-term 

social and behavioral ecology research program of bottlenose dolphins conducted at 

Turneffe Atoll. 


Study Area 

Located 50 km east of mainland Belize and 18 km beyond the Mesoamerican Barrier 

Reef in the western Caribbean Sea, Turneffe Atoll is roughly 50 km long, 16 km 

wide at its widest point (average width 8–10 km), and encompasses approximately 

531 km2 (Fig. 1) (Stoddart 1962). The atoll contains >200 mangrove cays (islands), 

incorporates three shallow (


Survey Procedures/Field Work 

Using the GPS unit to guide the boat along each transect line, surveys were 

conducted from either an 8.2 m skiff with two 85 hp outboard motors or a 6.4 m 

boat equipped with one 150 hp outboard motor. Boat speed was kept constant 

between 12 and 15 km/h and surveys were only conducted in Beaufort sea states of 

≤3 and wave heights


one outlier at around 200 m, allowing better model fit (Buckland et al. 2001). 

Distance 5.0 release 2 (Thomas et al. 2010) was used to estimate detection probability 

using Conventional Distance Sampling (CDC) and Multiple Covariate Distance 

Sampling (MCDS) (Buckland et al. 2001, 2004). Unlike CDC, which assumes the 

detection of an object is the sole function of its distance from the line, MCDS allows 

for the inclusion of additional variables that are likely to impact the detection 

probability. For cetacean surveys, Beaufort sea state is a common covariate (Palka 

1996, Barlow et al. 2001) and was used here. Following Buckland et al. (2001), 

several standard detection function models in CDS and MCDS were fitted to the 

data. The Kolmogorov–Smirnov goodness-of-fit test for each model was used to examine 

the absolute fit of the model (Buckland et al. 2004). Estimates from the model 

with the lowest Akaike’s Information Criterion (AIC) were selected (Buckland et al. 

2001). 

Results from a size-biased regression (the default method in Distance) indicated 

weak evidence of dependence between cluster size and distance (rs = 0.19, P = 

0.14). Mean sample cluster size (¯s ) was considered an unbiased estimator of the 

estimated mean cluster size of the population ( Ê (s )) (or Ê (s ) = ¯s ) (Buckland et al. 

2001). Bottlenose dolphin abundance ( ˆ N) within the survey area was estimated using 

(Buckland et al. 2001, Marques and Buckland 2003): 

ˆN = A · 

n · ¯s 

c · 2L · , 

where ˆ N is the estimated abundance, A the size of the study area, n the number of 

clusters seen, ¯s the mean sample cluster size, c the constant (or multiplier) indicating 

the number of times each line was surveyed, L the total length of transect line, and 

the effective strip half-width. 

The coefficient of variations (CV) for n, , and ¯s were each calculated individually. 

Empirical estimation of CV(n), as recommended by Buckland et al. (2001), plus an 

adjustment for multiple visits to transect lines followed: 

where var(n) = 

CV(n) = 

TL 

var(n) 

n 2 

k 

ti · li · (n i/(ti · li) − n/TL) 2 

i=1 

k − 1 

TL is the total line length traveled, represented by, TL = k 

i=1 ti · li, ti the number 

of times a line was traveled, li the length of transect line i, ni the number 

of detections on line i, k the number of transect lines. CV() and CV(¯s ) were 

each calculated by dividing the standard error of the estimator by itself. Individual 

CVs were used to compute the abundance estimate CV using (Buckland et al. 

2001): 

CV( ˆ N) = [CV(n)] 2 + [CV()] 2 + [CV(¯s )] 2 . 

,


RESULTS 

Survey Design 

The total planned survey effort was 220.54 km across 310.25 km2 . Due to shallow 

areas inaccessible to the boat, the realized survey effort was 175.21 km across 

298.5 km2 (about 80% of planned) for a set of transect lines. Six survey sets were 

completed, totaling 1,051.26 km of effort over 471.7 h during the rainy seasons of 

2005 (November–December) and 2006 (June–August and October–December) and 

during a two-week period (March–April) in the 2006 dry season. 

Abundance Estimation 

Thirty-four dolphin clusters, totaling 97 animals, were sighted on-effort (Fig. 1). 

Small sample size (n = 33 after truncation) precluded stratification by season; ungrouped 

perpendicular distances were pooled across all survey sets for analysis. Cluster 

size ranged from 1 to 12, with a mean cluster size of 2.61 (CV = 17%, 95% CI = 

1.85–3.68). The majority of sightings (84.5%) were of clusters ≤3 dolphins. 

Model results and the best fitting plotted detection function are presented in 

Table 1 and Figure 2. Estimated abundance and density for the study area was 

216 dolphins (CV = 27.7%, 95% CI = 126–370) and 0.749 dolphins/km2 (CV = 

27.7%, 95% CI = 0.437–1.282), respectively. A detection probability of 0.50 (CV = 

15%, 95% CI = 0.372–0.681) occurred within the study area. 

DISCUSSION 

Our study produced a new abundance estimate for a species of conservation concern 

in a region where such estimates are scarce and without governmental financial 

support. Only two prior studies from the 1990s, both using photo-identification, 

Figure 2. Histogram of perpendicular sighting distances truncated at 90 m and the fitted 

detection function for the best fitting model, MCDS half-normal model (no adjustment 

parameters) with sea state as a covariate. One sighting at 200 m was truncated.


Table 1. Model results for each of the tested models. Data were ungrouped, pooled across all surveys sets, and truncated at 90 m (n = 33). 

No. of parameters 

Model 

(Key + Adjustment) Key Adjustments AIC Ns 

ˆ CV(%) Dˆ CV(%) Ds 

ˆ CV(%) P CV(%) K-S p 

CDS 

Uniform + cosine 0 1 287.75 220 25.6 0.763 25.6 0.306 21.2 0.57 10.0 0.195 

Uniform + simple polynomial 0 1 288.04 204 25.0 0.707 25.0 0.272 20.5 0.64 9.0 0.153 

Half-normal + cosine 1 0 287.35 227 27.0 0.785 27.0 0.317 22.8 0.55 13.0 0.210 

Half-normal + hermite 1 0 287.35 227 27.0 0.785 27.0 0.317 22.8 0.55 13.0 0.210 

MCDS with Beaufort sea state as a covariate 

Half-normal + cosine 1 0 285.05 216 27.7 0.749 27.7 0.347 23.8 0.50 15.0 0.246 

Half-normal + hermite 1 0 285.05 216 27.7 0.749 27.7 0.347 23.8 0.50 15.0 0.246 

Hazard-rate + cosine 2 0 291.05 216 28.0 0.749 28.0 0.347 24.1 0.52 15.0 0.243 

Note: AIC = Akaike Information Criterion; ˆ Ns = abundance estimate for survey area; ˆ D = estimated density of dolphins/km 2 ; ˆ Ds = estimated 

density of clusters/km 2 ; P = detection probability; CV = coefficient of variation; K-S p = Kolmogorov–Smirnov goodness-of-fit p-value.


report abundance estimates for regional bottlenose dolphin populations in Belize: 

Campbell et al. (2002) estimated 82–86 individuals at Turneffe Atoll and Kerr 

et al. (2005) reported 122 individuals in the Drowned Cayes, located 16 km west 

of Turneffe within the Mesoamerican Barrier Reef. The different dolphin abundance 

estimates for Turneffe is not surprising, primarily because the two methods measure 

slightly different things and are therefore, not directly comparable. Mark-recapture 

sampling estimates the abundance of the overall biological population whether or 

not all individuals are present at a moment in time, while line transect sampling 

estimates the size of the population within the study area during the survey interval 

(Calambokidis and Barlow 2004). Nevertheless, the abundance estimates for 

this region are small and suggest the population cannot withstand high levels of 

mortality. 

To our knowledge there are no reports of hunting, fisheries bycatch, or boat strikes 

of dolphins at Turneffe, and Campbell et al. (2002) reported an absence of crescentshaped 

scars indicative of shark predation. Moreover, bottlenose dolphins are fully 

protected under Belize’s 1981 Wildlife Protection Act. This would suggest threats to 

the dolphins at Turneffe are currently minimal. However, mounting evidence indicates 

that continued unsustainable fishing (overfishing and illegal fishing) and rapid 

development are impacting the ecological integrity of the Atoll (World Resources 

Institute 2005, Granek 2006). Within Belize, fisheries are primarily artisanal; ongoing 

commercial fisheries heavily and unsustainably exploit Caribbean spiny lobster 

and queen conch, and a small-scale fishery targets snapper, grouper, and other fish 

species (Gillet 2003, FAO 2005). Coblentz (1997) demonstrated artisanal fisheries 

to be unsustainable and can quickly alter reef communities. Furthermore, gill nets, 

recognized as a leading cause of cetacean mortality worldwide (Read et al. 2006), 

are one of several techniques used in this fishery, often by illegal Guatemalan and 

Honduran fishers (Gillet 2003, FAO 2005, Perez 2009). The threat of entanglement 

in gill nets is cause for concern to bottlenose dolphin populations in Turneffe and 

the rest of Belize. 

Removal of mangroves and dredging of seagrass beds for private and commercial 

development are increasing at Turneffe. As important nursery areas for reef fish 

(e.g., snappers, grunts, and parrotfish), elimination of either habitat type can have 

significant impacts to adjacent reef fish communities and may lead to cascading 

effects at higher trophic levels (Nagelkerken et al. 2002, Mumby et al. 2004, Manson 

et al. 2005). Although quantitative diet studies for Turneffe dolphins do not yet 

exist, if unsustainable fisheries and development are left unchecked, changes to 

the atoll’s ecosystem could potentially lead to prey depletion. This is especially 

concerning because females with neonatal and older, but presumed nursing, calves 

are sighted year-round suggesting the atoll may be an important calving area (Grigg 

and Markowitz 1997, Campbell et al. 2002). Prey depletion could have negative 

ramifications on reproductive success since lactating females have much higher energy 

requirements than non nursing individuals (Oftedal 1984, Cheal and Gales 1991). 

On a larger scale, site fidelity patterns indicate a high proportion of dolphins 

are transient and use a much larger area than Turneffe (Campbell et al. 2002). 

Belize is a small western Caribbean country and the dolphins observed at Turneffe 

could move beyond the country’s borders. Extensive gill net use occurs in Mexican, 

Honduran, and Guatemalan artisanal fisheries and bottlenose dolphins have been 

historically found entangled or dead in these nets (Vidal et al. 1994, FAO 2000). 

To better understand the impacts of these threats on Turneffe dolphins, surveys 

should continue at the atoll in conjunction with studies that focus on dolphin


movement beyond the atoll, including a Belize-wide bottlenose dolphin population 

assessment, and the development of a method for monitoring and reporting fisheries 

interactions. 

Potential Violations of Line Transect Assumptions and Considerations for Future Surveys 

Survey design—Although it is possible to design a survey based on the amount 

of effort required to attain a certain level of precision (Buckland et al. 2001), often 

practical considerations will dictate the survey design, as was the case in this study. 

This is the first rigorous systematic survey conducted at Turneffe and its use is 

expected to continue. The choice of an equally spaced zig-zag design, with a few 

minor adjustments (see further), was considered successful. 

One particular issue arose during field surveys that required additional consideration. 

The full length of most transects between the mangrove shoreline and the 

fringing reef on the western side and several areas within the lagoons could not be 

surveyed; coral heads and shallow sand bars made these areas inaccessible. Instead, 

the areas were scanned for dolphins from the closest point that could be reached 

by the boat. Thomas et al. (2007) reported a similar experience and suggested this 

problem may be avoided by using high-resolution maps during the survey design 

process; however, such items are not available for this region. The issue was resolved 

by excluding the unsurveyed areas from the total line length traveled during analysis 

(Thomas et al. 2007). Because unsurveyed areas often occurred at the apexes of the 

zigzags, exclusion of these areas had the added benefit of further improving even 

coverage probability (Dawson et al. 2008). 

Abundance estimation—Visibility bias or incomplete detection at distance zero 

(g(0) < 1) can be problematic in marine mammal surveys and cause negatively 

biased estimates. This bias is classified in two ways: (1) animals may not be available 

to be seen by observers (availability bias) because they are not at the water’s surface 

where they can be seen (e.g., during diving), and (2) animals may potentially be 

visible to an observer but are not detected (perception bias) because of factors such as 

environmental conditions (e.g., sea state) (Marsh and Sinclair 1989). Consequently, 

species with longer dive times or found in smaller clusters are more likely to be 

missed by observers, thereby impacting the assumption g(0) = 1 (Dawson et al. 

2008). Bottlenose dolphins have relatively short dive durations in shallow areas. For 

example, along Florida’s Gulf Coast in areas with depths ranging between 1 and 5 m, 

average dive times for this species were recorded to be 20–25 s off Sanibel Island 

(Shane 1990), 30–40 s in Sarasota Bay (Irvine et al. 1981), and 28.5 s in Tampa Bay 

(Mate et al. 1995). Similar environmental conditions, including shallow waters, sand 

flats, and seagrass beds, occur at Turneffe Atoll; therefore dive times are likely to be 

comparable to those recorded in Florida. This short dive duration makes it unlikely 

that dolphins missed detection on the transect line because of being underwater. In 

addition, despite the small mean observed cluster size, almost 85% of the sightings 

were of clusters with ≤3 dolphins indicating smaller group sizes were not being 

missed. Introduction of significant bias to the abundance and density estimates from 

the assumption g(0) = 1 is, therefore, not expected. 

Responsive animal movement either toward or away from the survey vessel prior 

to detection will introduce bias (Turncock and Quinn 1991, Palka and Hammond 

2001). Bottlenose dolphins are known to bow-ride, and in at least 15% of the 

sightings, dolphins were first detected as they were quickly approaching the boat


and just prior to bow-riding. Attraction to vessels is seen in other small cetacean 

species including Dall’s porpoise (Phocoenoides dalli, Turncock and Quinn 1991), 

Pacific white-sided dolphins (Lagenorhynchus obliquidens, Williams and Thomas 2007), 

and white-beaked dolphins (Lagenorhynchus albirostris, Palka and Hammond 2001). 

Lemon et al. (2006) noted behavioral changes by Indo-Pacific bottlenose dolphins 

(T. aduncus) to an approaching boat at 100 m. Calculated distances from this study 

found all but one sighting occurred at ≤90 m, suggesting that the presence of the 

boat may have already attracted dolphins to the boat prior to detection. During future 

surveys, every effort should be made to ensure dolphins are sighted as far ahead of 

the vessel as possible. Correction factors, to account for attractive movement and 

positively biased estimates, should be developed through the collection of animal 

orientation data (Palka and Hammond 2001). 

Measurement accuracy also influences estimates and can be problematic regardless 

of survey platform type, although it can be exacerbated in small-boat surveys. Estimation 

of distances and angles is common (Vidal et al. 1997, Hammond et al. 2002); 

however, it may lead to measurement rounding and biased estimates. For this reason, 

estimation is not recommended unless observers are well trained and continually 

tested throughout the survey or correction factors are developed (Buckland et al. 

2001, Dawson et al. 2008). Lerczak and Hobbs (1998) and Buckland et al. (2001) 

describe several acceptable methods for acquiring measurements using tools such as 

angle boards and binoculars with reticles and/or compasses. An angle board was used 

to measure sighting angles and it helped to avoid angle rounding. A nonstandard 

method was used to determine sighting distances due to site-specific limitations, 

primarily that the horizon was rarely visible due to the enclosed nature of the atoll. 

A clinometer was chosen, as it is self-leveling and does not require the horizon as a 

reference point. However, declination angles

DICK AND HINES: BOTTLENOSE DOLPHIN ABUNDANCE 617 

other small cetacean abundance studies (e.g., 27.9% short-beaked common dolphin 

(Delphinus delphis), 48.1% bottlenose dolphin (Barlow 1995); 15.7% Hector’s dolphin 

(Cephalorhynchus hectori) (Dawson et al. 2004); 29.2% Dall’s porpoise, 35.3% Pacific 

white-sided dolphin (Williams and Thomas 2007), the abundance (216 dolphins, 

CV = 27.7%) and density (0.749 dolphins/km 2 ,CV= 27.7%) reported here for 

Turneffe Atoll are the best estimates given the conditions and should be considered 

preliminary. The development of correction factors to help account for potential 

line transect analysis violations is strongly recommended. Future surveys would also 

benefit from a higher observation platform and the consistent use of binoculars; 

however, this should only be done after careful thought as protocol modification after 

six survey sets will impact the ability to detect trends. 

Being able to obtain reliable abundance estimates and identify critical habitats 

are vital to the creation and success of marine protected areas for cetaceans (Hoyt 

2005). Our results provide an up-to-date population assessment for the area and 

should serve as a baseline as Belize moves forward with the development of a new 

conservation initiative to create a comprehensive and resilient marine protected area 

system. The year-round presence of dolphins, including mom/calf pairs (Grigg and 

Markowitz 1997, Campbell et al. 2002), suggests this area may be an important 

calving/nursery site and should be a priority for protection. Moreover, the high 

frequency of sightings near mangrove shorelines and atoll openings, 2 suggests these 

areas are important habitat features to the dolphins and should remain undeveloped. 

This and other recent studies (Vidal et al. 1997; Dawson et al. 2004, 2008; Williams 

and Thomas 2009) have shown that line transect surveys can be successfully modified 

for small-boats, provided the survey design is well planned and field methods are 

designed to address the main assumptions of line transect analysis. As coastal human 

populations continue to grow and the threats to small cetacean species increase, the 

reduction in cost and the improved accessibility to shallow areas through the use 

of small-boats will provide more opportunities for underdeveloped nations to assess 

their coastal marine mammal populations. 


We thank L. Thomas for providing helpful guidance during the survey design phase, 

S. G. Allen, B. Holzman, and H. Edwards for their reviews of earlier drafts of this paper, 

M. Christman, C. Keller, and P. Kubilis for their statistical advice, and R. Williams and an 

anonymous reviewer for comments on the manuscript. We are grateful to the many Oceanic 

Society and Elderhostel volunteers who helped in the field. Financial and logistical support 

was provided by Oceanic Society Expeditions. D. Dick received financial support from San 

Francisco State University’s Department of Geography and the College of Behavioral and 

Social Sciences Graduate Stipend. All research was approved by the Office for the Protection 

of Human and Animal Subjects at SFSU and conducted under a research permit issued to the 

Oceanic Society from the Ministry of Natural Resources Forest Department, Belize. 


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July 2009.


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Received: 3 August 2009 

Accepted: 16 July 2010

Journal of Zoology 

The lesser of two evils: seasonal migrations of Amazonian 

manatees in the Western Amazon 

E. M. Arraut 1,2 , M. Marmontel 3 , J. E. Mantovani 4 , E. M.L.M. Novo 1 , D. W. Macdonald 2 & R. E. Kenward 5 

1 Earth Observation General Coordination, Remote Sensing Division, National Institute for Space Research, São José dos Campos, São Paulo, SP, 

Brazil 

2 Wildlife Conservation Research Unit, Zoology Department, The Recanati-Kaplan Centre, University of Oxford, Tubney, Oxfordshire, UK 

3 Mamirauá Sustainable Development Institute, Tefé, AM, Brazil 

4 National Institute for Space Research, Natal Regional Center, Natal, RN, Brazil 

5 Centre for Ecology and Hydrology, Wallingford, Oxfordshire, UK 

Keywords 

Trichechus inunguis; habitat selection; 

remote sensing; geographical information 

system; Sirenia; migration. 

Correspondence 

Eduardo Moraes Arraut, Earth Observation 

General Coordination, Remote Sensing 

Division, National Institute for Space 

Research, Avenida dos Astronautas, 1 758, 

Jardim da Granja, PO Box 515, CEP 12227- 

101, São José dos Campos, SP, Brazil. Tel: 

55 12 3945 6486; Fax: 55 12 3945 6488 

Email: arraut@dsr.inpe.br or 

arraut@gmail.com 

Editor: Andrew Kitchener 

Received 9 March 2009; revised 28 August 

2009; accepted 13 September 2009 

doi:10.1111/j.1469-7998.2009.00655.x 

Introduction 

Abstract 

Migrationisanadaptationtoenvironmentsinwhichhabitat 

quality in different regions changes asynchronously in space 

and/or time (Dingle & Drake, 2007). This implies that habitat 

quality in the destination will be better than that at the origin, 

but not necessarily that it must be good. Here, we show that 

Amazonian manatees that live in the region of the Mamirauá 

and Amana˜ Sustainable Development Reserves (RDSM and 

RDSA, respectively) are subject to challenging habitat conditions 

during part of the year, and that they migrate into an 

area that is their best option under difficult circumstances. 

Journal of Zoology. Print ISSN 0952-8369 

We investigated the paradox of why Amazonian manatees Trichechus inunguis 

undergo seasonal migrations to a habitat where they apparently fast. Ten males 

were tracked using VHF telemetry between 1994 and 2006 in the Mamirauá and 

Amana˜ Sustainable Development Reserves, constituting the only long-term 

dataset on Amazonian manatee movements in the wild. Their habitat was 

characterized by analysing aquatic space and macrophyte coverage dynamics 

associated with the annual flood-pulse cycle of the River Solimo˜es. Habitat 

information came from fieldwork, two hydrographs, a three-dimensional model 

of the water bodies and classifications of Landsat-TM/ETM + images. We show 

that during high-water season (mid-May to end-June), males stay in várzea lakes in 

association with macrophytes, which they select. We then show that, during lowwater 

(October–November), the drastic reduction in aquatic space in the várzea 

leads to the risk of their habitat drying out and increases the manatees’ 

vulnerability to predators such as caimans, jaguars and humans. This explains 

why males migrate to Ria Amana˜. Based on data on illegal hunting, we argue that 

this habitat variability influences females to migrate too. We then use published 

knowledge of the environment’s dynamics to argue that when water levels are high, 

the habitats that can support the largest manatee populations are the várzeas of 

white-water rivers, and we conjecture that rias are the species’ main low-water 

refuges throughout Western Amazonia. Finally, we warn that the species may be 

at greater risk than previously thought, because migration and low-water levels 

make manatees particularly vulnerable to hunters. Moreover, because the flooding 

regime of Amazonian rivers is strongly related to large-scale climatic phenomena, 

there might be a perilous connection between climate change and the future 

prospects for the species. Our experience reveals that the success of research and 

conservation of wild Amazonian manatees depends on close working relationships 

with local inhabitants. 

We studied the influence of seasonal habitat variation on 

the migration of the Amazonian manatee Trichechus inunguis, 

which is the only member of the order Sirenia that lives 

exclusively in freshwater (Bertram & Bertram, 1973). Its 

distribution spans the Amazon basin, from Ecuador (Timm, 

Albuja & Clauson, 1986) and Peru (Reeves et al., 1996) to 

the Atlantic coast of Brazil (Best, 1984). Phylogenetic 

studies suggest that manatees from the mid-Solimo˜es, midand 

low-Amazonas form a single panmictic population 

(Cantanhede et al., 2005). 

Amazonian manatees are herbivores that in the RDSM 

and RDSA have been reported to feed on 63 species of 

Journal of Zoology 280 (2010) 247–256 c 2009 The Authors. Journal compilation c 2009 The Zoological Society of London 247

Seasonal migration of Amazonian manatees E. M. Arraut et al. 

aquatic macrophytes (annual freshwater plants) (Guterres & 

Marmontel, 2008). Adults reach up to 3 m in length and 

450 kg in weight (Caldwell & Caldwell, 1985), and consume 

about 8% of their body weight in aquatic macrophytes per 

day (Rosas, 1994). Because of strong habitat seasonality (see 

‘Materials and methods’), Amazonian manatees face an 

annual period of food shortage, which may last 7 months, 

during which they apparently fast (Best, 1983). 

The first tracking of an Amazonian manatee was carried 

out by Montgomery, Best & Yamakoshi (1981). A juvenile 

male was captured in the wild, kept in captivity for 

20 months (approximately half its life) and then released 

during the rising-water period in a várzea (a floodplain of a 

river with nutrient-rich and high-silt content water) near 

Manaus (a different region from where it had been captured). 

The manatee was tracked for 20 days, during which it 

spent most of its time feeding on aquatic macrophytes, and 

moved at a similar rate by day and by night. 

The Amazonian manatee’s migration was first reported 

by Marmontel et al. (2002), who tracked five adult males 

during a period of four and a half years. This showed that 

individuals migrated each year between várzea lakes, where 

they spent the high-water period, and Ria Amanã (a ria is 

long narrow lake formed by the partial submergence of a 

river valley), where they spent the low-water period (see 

‘Materials and methods’). Here, we extend the initial sample 

to 10 radio-tagged manatees to show (1) new migratory 

routes and (2) that the migration pattern remains consistent. 

We also indicate associations between Amazonian manatee 

248 

migratory movements and (3) availability of preferred food 

and (4) aquatic space reduction and predator aggregation. 

On that basis, we propose that the migratory behaviour, 

which is paradoxical insofar as animals travel to a place 

where, seemingly, they cannot eat, is a balance of feeding 

and predator avoidance. Finally, in the light of our results, 

we discuss the next steps for the species’ conservation. 


Study site 

The study region comprises just over 1 million hectares and 

lies within RDSM and RDSA, mid-River Solimo˜es region, 

Amazonas, Brazil (Fig. 1). The region was chosen because 

there were previous data on radio-tracked manatees (Marmontel 

et al., 2002), and the RDSM infrastructure facilitated 

fieldwork and the development of relationships with 

local communities. Its 120 km longitudinal extent 

(W65103 0 43.60 00 –W63151 0 49.80 00 ) encompassed all locations 

of the tracked manatees, and its 70 km latitudinal extent 

(S02114 0 39.34 00 –S03137 0 45.74) is bounded by várzea and by 

the Ria Amanã. 

In the várzea study region, water levels fluctuate annually 

over a range of 16 m, while in Ria Amana˜ annual variation is 

about 10 m (Fig. 2a). This variation in water level is caused 

by a flood pulse in the River Solimo˜es, and this pulse is the 

principal determinant of the extent and depth of flooding 

(Fig. 2b) and of the water’s physical chemistry (Junk, Bayley 

Figure 1 Study region showing in: small quadrant, 

location in relation to South America; large 

quadrant, band 4 of Landsat-TM image overlaid 

by migration routes of male Amazonian manatees 

Trichechus inunguis. Thin white lines are 

routes reported by Marmontel et al., (2002), 

thicker white lines are routes of manatees 

tracked later; thicker lines end at Lake Castanho 

so as not to mask previously detected 

routes, but all routes lead to or depart from Ria 

Amanã. Also shown are location of gauges 

(white squares) and of local human communities 

(white crosses). 

Journal of Zoology 280 (2010) 247–256 c 2009 The Authors. Journal compilation c 2009 The Zoological Society of London

E. M. Arraut et al. 

& Sparks, 1989). As a result of this large variation in water 

level, and because of the irregular geomorphology of many 

lakes and channels, water depth is the principal determinant 

of the connectivity between water bodies. The differences of 

geomorphology and of water level variation explain, for 

example, why although Lake Mamirauá and Ria Amana˜ 

have similar depths during high-water, the former might 

become isolated during low-water while the latter remains 

deeper, connected to adjacent water bodies and with more 

aquatic space (Arraut, 2008). Based on this habitat seasonality, 

we distinguish between periods of lowering-water 

(July–August), low-water (September–November), risingwater 

(December–April) and high-water (May–June), defined 

on the basis of the water level and its speed of vertical 

change (Arraut, 2008). 

Manatee tracking 

Seasonal migration of Amazonian manatees 

Figure 2 (a) Water-level variation as a result of 

River Solimões’s flood pulse measured by 

gauges positioned in the channel of Lake 

Mamirauá and in Ria Amanã (see Fig. 1). The 

gauges are not inter-calibrated, so hydrographs 

are only comparable with respect to time and 

water-level variation. (b) Habitats vary depending 

on flooding duration and flood pulse phase. 

When water levels are high, lakes, rivers 

and flooded forest are all passable for the 

manatee. When levels are low, lakes may loose 

connectivity. 

From 1994 to 2006 (excepting 2004), 10 males were radiotracked 

with an Advanced Telemetry Systems (ATS) transmitter 

(Advanced Telemetry Systems Inc., Isanti, MN, 

USA) on the 164 MHz band using a three-element Yagi 

antenna. They were caught under government permit by 

research teams, sometimes aided by local hunters, mostly 

using a wide mesh net. Attempts were made to locate each 

individual once a day. Although hunting of Brazilian native 

fauna is illegal (Castello-Branco & Gomes, 1967), hunters 

eventually killed six out of our 10 tracked Amazonian 

manatees. We also captured three females, but we lost track 

of two on the following day and one was found dead 2 days 

later (Table 1). On some occasions, individuals were tracked 



Table 1 Information about tracked Amazonian manatees 

ID Gender 

Capture 

Location Water season 

but no GPS coordinate was associated to the location (Table 

1); in these instances, the geographical location is recorded 

as the name of the place (lake or part of lake) where the 

individuals were active and, for analysis, subsequently given 

coordinates at the centre of that location. As a result, for 

this subsample of the data, all locations of all manatees that 

had been recorded as being from that place were allocated 

the same coordinates. Thus, for example, individual seven 

was located 168 times, and these sites are allocated, for 

analysis, to only 12 GPS positions. 

Estimation of manatee locations 

We triangulated using the Best bi-angulation algorithm of 

the software LOCATION OF A SIGNAL (LOAS) 4.0b (ESS, 2006). 

Magnetic bearing corrections were calculated using the 

software DECLINAçaÕ MAGNÉTICA 2.0 (LEEE, 2003). Field 

experiments in which manatee tracking conditions were 

simulated at distances up to 2 km gave a mean positional 

error of 140 m (Arraut, 2008); we used a tracking resolution 

of 300 m, which was much smaller than either the range size 

or the dimensions of the habitat fragments. 

Migration detection and home-range 

calculations 

We first separated ranging from migratory movements using 

the dispersal detector algorithm in the software RANGES8 

(Kenward et al., 2008). We detected that all the eight 

manatees that we tracked for more than one flood-pulse 

period had migrated. Then, because in the scale of our 

analysis the habitat showed annual seasonality, (e.g. macro- 

Tracking period 

Seasonal 

ranges 

N_locs used for 

range estimate 

1 M L. Mamirauá High 4 years A 36 1289 

B 18 518 

2 M L. Mamirauá High 3 years 4 months A 170 794 

B 150 1952 

3 M L. Mamirauá High 4 years 4 months A 58 727 

B 50 1031 

4 M R. Amanã Lowering 1 year 4 month A 92 394 

B 61 2664 

5 M R. Amanã Low 5 months A 9 3474 

B 6 234 

6 M P. do Castanho Low 3 years A 85 308 

7 M L. Mamirauá High 2 years 2 months A 156 250 

8 M R. Amanã Lowering 3 months B 55 1186 

9 M R. Amanã Lowering 3 months B 43 2117 

10 M R. Amanã Low 6 months B 19 748 

11 F P. do Castanho Lowering Not tracked – – – 

12 F P. do Castanho Lowering Not tracked – – – 

13 F R. Amanã Low Not tracked – – – 

phyte cover and flooding were similar in high-water periods 

of different years), we pooled locations of each individual in 

the same geographic area and flood-pulse period. Home 

ranges were estimated using 95% kernels with fixed-smoothing 

parameter (Kenward et al., 2008). This model was 

especially appropriate because of variability in positional 

accuracy and owing to the small number of locations in 

some ranges (mean=59, range=6–170, n=15): kernels 

with fixed smoothing can give maximum range area estimates 

with as few as 12–15 locations (Kenward, 2001) (all 

but one animal had at least 12 locations); fixed smoothing 

also generates better overall surface estimates than adaptive 

smoothing (Seaman & Powell, 1996). Five individuals had 

two seasonal home ranges, whereas for the five other 

individuals, we could only calculate one home range. 

Habitat characterization 

95% kernel 

range size (ha) 

Number of locations used to calculate each of the seasonal home ranges is shown. Letter ‘A’ identifies high-water ranges in várzea lakes and 

letter ‘B’ identifies lowering-water ranges in River Japurá and low-water ranges in Ria Amanã (see ‘Habitat Analysis’ section). 

L., lake; P., paraná; M, male; F, female; ID, individual identification. 

250 

To analyse the spatial–temporal corollaries of manatee 

movement we considered: (1) water-level variation, measured 

daily from gauges with 1 cm interval positioned at 

Lake Mamirauá (since 1992) and Ria Amana˜ (since 2001); 

(2) the bottom topography and depths of water bodies, 

based on a bathymetric model from the field survey and 

geographical information system modelling; (3) the growth 

cycle and spatial distribution of macrophytes combined with 

the flooding dynamics in the area, from classifications of 11 

Landsat-TM and ETM+ images acquired between 1995 

and 2005 (three of the high-water, four of the loweringwater, 

two of the low-water and two of the rising-water). 

The total of 5 months of fieldwork was distributed throughout 

all four flood-pulse periods. 



Frequent cloud cover over the Amazon limited the availability 

of good-quality satellite images. Previous studies, 

however, suggest that on a broad scale, the environment 

shows annual seasonality with regard to the flooding extent, 

water physical chemistry and macrophyte cover dynamics 

(Junk et al., 1989; Junk & Piedade, 1993; Barbosa, 2005; 

Arraut, 2008). Thus, when images from the same dates as 

the tracking data were not available, we used images from a 

different year but same flood pulse period. 

In the classifications, we distinguished six habitat 

classes: (1) macrophytes on water; (2) flooded forest; (3) 

open-water; (4) macrophytes on non-flooded land; (5) nonflooded 

forest; (6) non-flooded land. The first three occurred 

during high-water and the last three, plus open-water, 

during the low-water. Classification assessment was 

based on a confusion matrix (Congalton & Green, 2008), 

which indicated accuracies above 90%. Further details of 

the habitat characterization process are given in Arraut 

(2008). 

Habitat analysis 

Habitat analysis addressed three questions: 

Question 1: Selective use of habitat 

Are males selective in their use of habitats, and specifically 

of aquatic macrophytes? 

Question 2: Proportion of forage within home ranges 

during high-water 

During the high-water, was there proportionally more 

forage in manatee home ranges within várzea lakes than if 

they had remained in River Japur a´ or Ria Amana˜? 

Question 3: Seasonal reduction in flooded area within 

home ranges 

Did the proportional seasonal reduction in the aquatic 

area within home ranges differ between manatees in várzea 

lakes and those in River Japurá or Ria Amana˜? 

Selective use of habitat (question 1) was assessed using 

compositional analysis (CA) on log ratios of used and 

available habitats (Aebischer, Robertson & Kenward, 

1993). To answer questions 2 and 3, we separated the 15 

home ranges occupied by the 10 manatees into two 

categories: ranges in várzea lakes during the high-water 

(category A) and ranges in River Japurá during the lowering-water 

or in Ria Amana˜ during the low-water 

(category B). Ranges in River Japur a´ and Ria Amana˜ were 

grouped into one category because the objective was to 

discover, with quantitative evidence, why male manatees 

remained in várzea lakes during high-water, and why they 

did not remain there during low-water (i.e. why they 

migrated); this grouping also increased sample size for 

statistical analyses. 

We carried out analyses of variance (ANOVA) by means 

of general linear models (GLM) using MINITAB v15.1.1 

(Minitab, 2007). For question 2, the response variable in 

the GLM was the ‘proportion of the home range covered by 

aquatic macrophytes’ (arcsine root transformed), and for 

question 3, it was the ‘proportional seasonal reduction in the 

flooded area’ (arcsine root transformed). Although there 

were too few ranges to test for inclusion of multiple 

predictor variables, we included individual identification 

(ID) and location number in each home range (N_locs) in 

the GLMs with category variable A/B to exclude the 

possibility that relationships with the response variable 

depended on differences between individuals and sampling 

characteristics. 

Results 

Seasonal habitat use and migration 

Males remained in várzea lakes from the middle of the rising 

to the beginning of the lowering-water period (approximately 

from February to the beginning of August), when 

flooding facilitated unconstrained access to all lakes, rivers 

and flooded forest. During the lowering-water, they left 

várzea lakes and migrated to Ria Amanã, where they stayed 

during the low-water. Then, during the rising-water, males 

migrated back to várzea lakes, thus closing the annual 

migratory cycle. The three females captured were either at 

(during low-water) or migrating to (during lowering-water) 

Ria Amana˜, thus, moving in accordance with what was 

observed for the radio-tracked males. 

Habitat analysis 

Selective use of habitat 


CA revealed aquatic macrophytes as the only preferred 

habitat class during high-water, and ranked the three 

habitat classes: (2) macrophytes, (1) open-water and (0) 

flooded forest [F (2, 5 d.f.)=7.56, P=0.04]. 

Proportion of forage within home ranges during 

high-water 

During high-water, home ranges in várzea lakes (category 

A) encompassed almost sevenfold the area of aquatic 

macrophytes that occurred within home ranges in River 

Japurá or Ria Amana˜ (A: mean=0.27, SE=0.13; B: 

Figure 3 Macrophyte proportion in the home ranges of individuals 

was greater when in várzea lakes (^) than when in River JapuráorRia 

Amanã (’). ID, individual identification. 



mean=0.04, SE=0.04) (Fig. 3). In the GLM, the category 

A/B variable explained the most variance in the response 

variable, and continued to do so with the inclusion of ID 

and N_locs (Table 2). Model residuals showed no trend, 

indicating that the model was appropriate. Thus, the proportion 

of the home range classified as macrophyte habitat 

was greatest for males while they were in várzea lakes. 

Seasonal reduction in flooded area within home 

ranges 

Reduction in the flooded area in várzea lakes was over 4.5 

times greater than in River Japur a´ or Ria Amana˜ (A: 

mean=0.98, SE=0.01; B: mean=0.21, SE=0.07) (Fig. 4). 

In the GLM, variable A/B explained most of the variance in 

the response variable, and continued to do so with inclusion of 

ID and N_locs (Table 3). Analysis of full model residuals 

showed no particular trend, indicating the model was appropriate. 

Areas within high-water ranges practically dried out 

during low-water, while areas where manatees had low-water 

ranges suffered much smaller reduction in the aquatic space. 

After leaving Mamirauá while the water was lowering in 

1996, individuals one, two and three remained for a few days 

in an area of River Japur a. ´ They then disappeared during 

the low-water, only to return in the next rising-water. On the 

other hand, individuals captured at Paraná do Castanho 

during the lowering-water were moving in the direction of 

Table 2 General linear model results: F statistic and P values for 

response variable ‘macrophyte proportion in the home ranges’ for full 

and reduced models 

Explanatory variables A/B N_locs ID 

Variable alone 38.48 a 

0.51 d 

0.73 d 

A/B with each – 31.20 b 

67.50 b 

A/B with both – 121.36 c 

a Po0.001. 

b P=0.001. 

c P=0.002. 

d P not significant. 

ID, individual identification. 

Figure 4 Proportion reduction in flooded area (from high- to lowwater) 

was much greater for ranges in várzea lakes (^) than for those 

in River Japurá or Ria Amanã (’). ID, individual identification. 

252 

Table 3 General linear model results: F statistic and P values of the A/ 

B variable ‘proportion reduction in flooded area’ for the full and 

reduced models 

Explanatory variables A/B N_locs ID 

Variable alone 227.37 a 

0.93 c 

0.40 c 

A/B with each – 238.94 a 

165.14 a 

A/B with both – 138.70 b 

a Po0.001. 

b P=0.001. 

c P not significant. 

ID, individual identification. 

Ria Amana˜, and all those captured and/or tracked during 

low-water were within Ria Amana˜ (n=9). This suggests 

that manatees aggregate in Ria Amana˜ during low-water. 

Discussion 

Várzea species are adapted to the seasonality of the environment 

(Junk et al., 1989). In the RDSM region, river dolphins 

Inia geoffrensis spend the high-water in várzea lakes and in 

flooded forest, but during low-water, they are in the main 

channels of Rivers Solimo˜es and Japur a ´ (Martin & da Silva, 

2004). Male Amazonian manatees also lived in várzea lakes 

during high-water, but in the low-water migrated to Ria 

Amana˜. 

The várzea lakes used during high-water offered forage in 

greater abundance [Results (1) and (2); Fig. 3, Table 2] and 

diversity (Junk et al., 1989; Arraut, 2008; Guterres & 

Marmontel, 2008), and less water current than rivers and 

paran as ´ (channels that connect rivers). When the water level 

dropped and the flooded area significantly contracted, 

restricting their home ranges [Result (3), Fig. 4, Table 3], 

male manatees migrated to Ria Amana˜ where they spent the 

low-water season. There, apart from more space, they 

encounter reduced risk from predators like: caimans Melanosuchus 

niger and Caiman crocodilus (Nunes Pereira, 1947), 

jaguars Panthera onca (Bertram & Bertram, 1973) and 

humans Homo sapiens sapiens (Domning, 1982a; Marmontel, 

2008). During the low-water period, caimans aggregate 

in whichever water bodies remain in the várzea (E. M. 

Arraut & M. Marmontel, pers. obs.), jaguars frequent the 

water margins (Ramalho, 2006) and humans come to gather 

the fish that aggregate there. Conversely, local hunters assert 

that the manatees in Ria Amana˜ are more difficult to kill 

(Calvimontes, 2009). 

Further information from interviews with local hunters 

indicates that female manatees have seasonal movement 

patterns similar to those of males. Sixty-four manatees were 

killed in Lake Castanho, Ria Amana˜ and the migration 

route between them during 2002–2004 (Calvimontes, 2009). 

These manatees were killed in Lake Castanho only between 

the rising- and the mid-lowering-water seasons and in Ria 

Amana˜, only between the lowering- and the beginning of the 

rising-water seasons. Of the 35 that had their sex determined, 

there were 13 males and 22 females. All four 

manatees killed in upper-Amanã at the beginning of the 



rising-water were females, including two that were calves 

(Calvimontes, 2009). From estimated birth dates of 24 

neonate Amazonian manatees, Best (1982) suggested that 

calves are normally born during the period of rising-water. 

As gestation is 12–14 months (Rosas, 1994), mating is 

expected to occur during low-water or the start of risingwater. 

Therefore, Ria Amana˜ may be both a mating and 

calving ground for Amazonian manatees. 

Do manatees that live in the várzeas of other 

white-water rivers move similarly as those in 

the mid-Solimões region? 

In the Amazon, immense white-water rivers such as the 

Solimo˜es, Amazonas, Puru´s and Madeira form várzeas and 

have rias annexed to their várzeas. They are also typified by 

flood pulses, and seasonal macrophytes (Junk & Furch, 

1993) (Fig. 5). The habitats available to manatees in these 

other regions of the Amazon, thus, seem similar to that 

which we have described in our study region. 

Evidence for the occurrence of manatees in these areas 

Acuna ˜ (1641), who reported them as abundant enough to be 

easily seen throughout the Rivers Solimo˜es and Amazonas, 

and Domning (1982a), who analysed the records of manatees 

hunted (legally at the time) that were documented in 

Manaus between 1785 and 1983. Based on such information, 

as well as on how the large-scale movements of 

manatees in our study region coincide closely with the flood 

pulse, we conjecture that the habitats that can sustain the 

largest populations of T. inunguis during the high-water are 

the várzeas of large white-water rivers. 

On the other hand, during low-water, when most of the 

várzea dries out, rias remain the main places where aquatic 

space (Hess et al., 2003) with minimal current can be found. 

We thus conjecture that rias are the main low-water refuges 

of manatees that live in the floodplains of these major whitewater 

rivers; these floodplains comprise the great majority 

of the manatees’ known geographical range. 

Evolutionary ecology of the Amazonian 

manatees’ migration 

Seasonal migrations have been well documented in other 

aquatic mammals, and the ecological processes that drive 

River Japurá 

Ria Tefé 

Ria Amanã 

River Solimões 

River Negro 

River Amazonas 

migration often seem to be related to habitat variability. The 

Florida manatee Trichechus manatus latirostris (Deutsch 

et al., 2003) and the dugong Dugong dugon (Sheppard et al., 

2006) migrate to warmer waters in autumn, and back to 

their summer areas in spring. In these two species, the 

evolution of migration can be explained as a means of 

optimizing forage when it is available and avoiding harsh 

environmental conditions during the rest of the year. We 

have demonstrated comparable seasonal movements for 

Amazonian manatees, although in their case the ‘seasons’ 

are determined by variation in water level and the limiting 

factors are space and predation. 

Trichechus inunguis is thought to be the most derived 

species of manatee, having evolved from ancestral trichechids 

that colonized the Western Amazon in the Pliocene 

(2–6 million years ago) (Domning, 1982b). Geological evidence 

suggests that the várzea of River Solimo˜es achieved its 

present form in the Holocene (o10 000 years), and that 

terraces on its sides were formed a bit earlier, in the last 

47 300 years (Rossetti, Toledo & G oes, ´ 2005). Because rias 

are formed by the excavation of such terraces by ancient 

rivers, they must be younger than the terraces. Thus, the use 

of Ria Amana˜ as a breeding and calving ground, and 

migration to it, must be a relatively recent phenomenon in 

the species’ evolutionary history and, if our conjecture is 

correct, this also applies to the use of other rias. The 

geological history of the Western Amazon thus indicates 

that Amazonian manatees have changed their spatial behaviour 

in response to changes in the habitat that occurred 

within the last few tens of thousands of years. 

The fact that manatees living from the mouth of the River 

Amazon and those occurring throughout Amazonia to the 

west are part of a single panmictic population (Cantanhede 

et al., 2005) indicates that any differences in the movements 

of individuals in these widely separated areas are probably a 

result of behavioural plasticity in response to local habitat 

conditions. This raises the question: what are the movement 

patterns of the manatees living near the mouth of River 

Amazon (Domning, 1981), where water level varies daily 

(ANA, 2009) because of the Atlantic tides and where there 

are no rias? How do these differences in the spatial–temporal 

dynamics of their habitats affect manatee reproductive 

ecology? For example, if manatees find forage and living 

space in the same area throughout the year, we would not 

River Tapajós 

N 

1320 km 


Figure 5 Rias (shown by arrows), which are 

numerous and of various sizes, occur throughout 

the margins of Rivers Solimões and Amazonas 

and are conjectured to be the Amazonian 

manatee’s main low-water refuges. Study-region 

limits indicated by dashed-line polygon. 

Landsat-TM mosaic of the central Amazon 

várzea. Source: Shimabukuro, Novo & Mertes 

(2002). 



expect them to migrate. Answers to these questions await 

further research. 

Conservation implications 

Migrating Amazonian manatees pass through narrow channels 

where hunters can wait within harpoon range. Because 

human settlements are numerous and widespread (Fig. 1), 

and local inhabitants relish manatee meat, and are aware of 

the timing of their migration, manatees have to pass through 

perilous bottlenecks to arrive at the relative safety of Ria 

Amana˜. Then, in the beginning of the rising-water, water 

levels rise sufficiently to flood the few beaches where macrophytes 

have been growing close to the mouth of Ria Amana˜. 

The manatees aggregate at these beaches, hungry after 

several months of fasting and again become vulnerable to 

hunters. Hence, the migration to, and prolonged occupation 

of, Ria Amana˜ present clear risks to contemporary manatees. 

Nevertheless, the fact that manatees migrate to Ria 

Amana˜, and that, as argued above, this migratory behaviour 

is probably not genetically determined, suggests that staying 

in várzea lakes during the low-water has been (at least until 

recently) even more perilous. The lowering- and low-water 

seasons are, thus, periods when Amazonian manatees living 

in the mid-Solimo˜es region have to choose between the 

lesser of two evils. 

Any climate changes that lead to more intense droughts, 

and thus to a reduction in the aquatic space during the lowwater 

period, would increase the exposure of Amazonian 

manatees to hunters. A connection between climate change 

and an increase in the frequency of droughts in the Amazon 

is predicted under all scenarios of all 23 IPCC climatic 

models (Malhi et al., 2008), and relationships between 

large-scale climatic phenomena, such as the El Nino ˜ Southern 

Oscillation and the Tropical North Atlantic Ocean 

Temperatures, and the levels of major Amazonian rivers, 

were determined by Richey, Nobre & Deser (1989), Schongart 

& Junk (2007) and Marengo et al. (2008a,b). A situation 

that might become more frequent is exemplified by the 

drought of 2005, estimated to be the most intense in the last 

40 years, when the Amazon River and its major tributaries 

were left with only a fraction of their normal volume 

(Marengo et al., 2008a,b). During this drought, enormous 

quantities of fish died, clogging rivers and poisoning the 

water, and people living in small communities had to walk 

several kilometres to find water and food (Giles, 2006). 

Amazonian manatees also suffered. Local people informed 

us of the killings of at least five manatees in Ria Tefe´, and 

colleagues working in River Puru´s informed us of at least 12 

that were killed in Ria Jari (B. Marioni, E. V. Mullen & F. 

Rossoni, pers. comm.). 

In order to protect the manatees better now, and to 

safeguard them in the face of climate change, it is important 

to research their status in other regions, and to complement 

such research with education. Our experience indicates that to 

be effective, any conservation programme needs to learn from, 

educate and bring benefits to local populations, because local 

people are necessary actors in conserving the manatees and 

254 

their environment. Our conjecture that rias are the manatee’s 

main low-water refuge can serve as a starting point in the 

search for manatees in other regions of the Amazon. 

Acknowledgements 

We are grateful to the Coordenação de Aperfeiçoamento de 

Pessoal de Nível Superior (CAPES) for funding Arraut’s 

PhD stipend and expenses, to the Rede de Modelagem 

Ambiental da Amazoˆnia (GEOMA) Network and to the 

Graduate program in Remote Sensing at INPE (Brazil). We 

are thankful to Antonio Pinto de Oliveira for his help during 

fieldwork, and to all the local hunters and trainees who 

helped with data collection. We thank Dr Paul Johnson for 

his suggestions during data analyses, and Drs Marion 

Valeix, Jorgelina Marino, Thomas Merckx, Laura Fasola 

and Ruth Kanski for fruitful comments on an earlier draft. 

We also thank Dr Dilce Rossetti, Dr Thiago Silva and two 

anonymous referees for their suggestions. 

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The Journal of Experimental Biology 212, 2349-2355 

Published by The Company of Biologists 2009 

doi:10.1242/jeb.027565 

Carbon and nitrogen stable isotope turnover rates and diet–tissue discrimination in 

Florida manatees (Trichechus manatus latirostris) 

Christy D. Alves-Stanley1 and Graham A. J. Worthy1,2, * 

1Physiological Ecology and Bioenergetics Lab, Department of Biology, University of Central Florida, 4000 Central Florida Boulevard, 

Orlando, FL 32816, USA and 2Hubbs-SeaWorld Research Institute, 6295 Sea Harbor Drive, Orlando, FL 32821, USA 

INTRODUCTION 

The isotopic composition of consumer tissues reflects that of local 

food webs and can be used to predict diet composition, the trophic 

level at which the consumer is feeding, and even habitat use and 

migratory patterns (e.g. Deniro and Epstein, 1978; Deniro and 

Epstein, 1981; Fry, 1981; Peterson and Fry, 1987) (reviewed by 

Hobson, 1999). Two stable isotope ratios commonly analyzed in 

feeding ecology studies are those of carbon ( 13 C/ 12 C) and nitrogen 

( 15 N/ 14 N). Carbon isotope ratios indicate the likely source of 

primary production and have been used to differentiate between C3 

and C4 plants, terrestrial and marine ecosystems, deep forest and 

open habitat consumers, and benthic and pelagic aquatic systems 

(e.g. Cloern et al., 2002; Cerling et al., 2004; Hall-Aspland et al., 

2005). Nitrogen isotope ratios exhibit a predictable, step-wise 

enrichment between trophic levels and also have been shown to 

differ between terrestrial and marine ecosystems (e.g. Hobson and 

Welch, 1992). 

Stable isotope analysis is especially advantageous when 

investigating the feeding ecology and habitat use of marine mammals 

where it is often impossible to directly observe feeding or migratory 

behavior. Tissue samples, such as skin or blubber, may be analyzed 

for stable isotope ratios without sacrificing the animal and this 

approach has been successfully applied to a variety of marine 

mammal species including mysticetes (e.g. Lee et al., 2005), 

odontocetes (e.g. Walker et al., 1999), pinnipeds (e.g. Hobson and 

Welch, 1992; Kurle and Worthy, 2002; Newsome et al., 2006), 

sirenians (e.g. Ames et al., 1996; MacFadden et al., 2004; Yamamuro 

et al., 2004; Reich and Worthy, 2006), sea otters (Clementz and 

Koch, 2001) and polar bears (e.g. Ramsay and Hobson, 1991). 

In order to accurately interpret isotopic results, it is imperative 

to determine both isotopic discrimination (the difference in isotopic 

*Author for correspondence (e-mail: gworthy@mail.ucf.edu) 

Accepted 3 May 2009 

SUMMARY 

The Florida manatee (Trichechus manatus latirostris) is a herbivorous marine mammal that occupies freshwater, estuarine and 

marine habitats. Despite being considered endangered, relatively little is known about its feeding ecology. The present study 

expands on previous work on manatee feeding ecology by providing critical baseline parameters for accurate isotopic data 

interpretation. Stable carbon and nitrogen isotope ratios were examined over a period of more than 1 year in the epidermis of 

rescued Florida manatees that were transitioning from a diet of aquatic forage to terrestrial forage (lettuce). The mean half-life for 

13 C turnover was 53 and 59 days for skin from manatees rescued from coastal and riverine regions, respectively. The mean halflife 

for 15 N turnover was 27 and 58 days, respectively. Because of these slow turnover rates, carbon and nitrogen stable isotope 

analysis in manatee epidermis is useful in summarizing average dietary intake over a long period of time rather than assessing 

recent diet. In addition to turnover rate, a diet–tissue discrimination value of 2.8‰ for 13 C was calculated for long-term captive 

manatees on a lettuce diet. Determining both turnover rate and diet–tissue discrimination is essential in order to accurately 

interpret stable isotope data. 

Key words: turnover, stable isotope, Florida manatee, diet–tissue discrimination, 13 C, 15 N, Trichechus manatus, feeding ecology. 

THE JOURNAL OF EXPERIMENTAL BIOLOGY 

2349 

ratios between consumer tissue and diet) and turnover rate (the time 

it takes for the isotope to be assimilated into the consumer’s tissue) 

of the sampled tissue. Diet–tissue discrimination may be difficult 

to determine for animals feeding on multiple, isotopically distinct 

prey items for which the proportions contributing to the diet are 

unknown. However, controlled captive studies on a variety of taxa 

have allowed for more precise measurements (e.g. Roth and Hobson, 

2000; Cherel et al., 2005; Logan et al., 2006; Seminoff et al., 2006). 

In addition to diet–tissue discrimination, turnover rates in tissues 

must be determined in order to assess whether the isotope signature 

of the tissue represents the most recent diet or the long-term diet. 

An effective method to determine turnover rate is to experimentally 

switch an animal from one known diet to another isotopically distinct 

diet. Turnover rates of stable isotopes have been calculated using 

this method for mammals (e.g. Tieszen et al., 1983), birds (e.g. 

Hobson and Clark, 1992a), fish (e.g. Bosley et al., 2002) and 

invertebrates (e.g. Olive et al., 2003). These studies have shown 

that tissues with higher metabolic activity (e.g. blood, liver) have 

faster turnover rates than less active tissue (e.g. bone). 

The endangered Florida manatee (Trichechus manatus latirostris 

L.) is known to feed on a variety of aquatic plants in fresh, estuarine 

and marine habitats (e.g. Campbell and Irvine, 1977; Hartman, 1979; 

Best, 1981), each of which has a distinct isotopic signature (e.g. 

Fry and Sherr, 1984; Reich and Worthy, 2006) (C.D.A.-S. and 

G.A.J.W., in preparation). Little is known about fine-scale manatee 

feeding ecology and habitat use because manatees often occupy 

shallow, turbid water. In addition, manatee population counts and 

trends remain unclear (Lefebvre et al., 1995; US Fish and Wildlife 

Service, 2001). Consequently, it has become increasingly important 

to understand manatee feeding ecology and its relation to habitat 

use in order to improve conservation efforts.

2350 

C. D. Alves-Stanley and G. A. J. Worthy 

The present study used skin samples from Florida manatees 

transitioning between two isotopically distinct diets (aquatic to 

terrestrial) to determine turnover rates and diet–tissue discrimination 

in epidermis tissue. Manatees were part of the rehabilitation program 

at SeaWorld of Florida, and were in need of captive care for reasons 

including physical trauma, nutritional stress and/or cold stress. The 

overall objectives of the present study were to determine 13 C and 

15 N turnover rates in epidermis tissue and to calculate diet–tissue 

discrimination values for carbon and nitrogen stable isotopes in 

manatee skin. 


Sample collection 

Manatees held long-term at SeaWorld of Florida (Orlando, FL, USA) 

were fed a diet consisting primarily of romaine lettuce (>90% by 

mass) with minimal amounts of other terrestrial vegetation (176 Subadult–adult 512 

Charlotte F 1136 330 Adult >365 

Primo F 494 277 Adult >365 

Rita F >900 >275 Adult >365 

Sarah F 1136 325 Adult >365 

Stubby F 823 252* Subadult–adult >365 

SWF Tm 0110 F 367 255 Subadult 1231 

SWF Tm 0302 F Unknown >176 Subadult–adult 512 

SWF Tm 0338 F Unknown >176 Subadult–adult 429 

*Missing large portion of paddle. 


at various time intervals as they transitioned from wild forage to a 

captive diet. Carbon and nitrogen stable isotope turnover rates in skin 

were calculated for manatees rescued from two habitats in Florida: 

‘coastal’ (Naples on the Gulf coast and Cape Canaveral on the central 

east coast) and ‘riverine’ or fresh water (St Johns River near 

Jacksonville; Fig.1). The terms ‘coastal’ and ‘riverine’ represent rescue 

locations only, and are not intended to describe overall habitat use. 

Biopsies of epidermal tissue were collected from the trailing edge 

of the paddle using either a scalpel or ronguers (samples were 

approximately 10mm5mm, full depth of the paddle). Partially 

sloughed epidermis was collected directly off individual manatees 

(approximately 2cm2cm) if biopsies were not available. Body mass 

and sex were determined, and length measurements taken, where body 

length was measured as the straight distance from snout to paddle 

(O’Shea et al., 1985). Manatees were categorized into three age classes 

based on body length measurements (adults >275cm, subadults/late 

juveniles 176–275cm, and calves

Fig. 1. Rescue locations of manatees in Florida. 

time (days) since diet switch. Turnover rate was expressed in terms 

of half-life, the time it takes for the isotopic composition of the 

tissue to reach a midpoint between the initial and final values: 

X = (ln0.5) / c , (3) 

In order to better fit turnover data to the exponential model, an 

‘anchor point’ based on the mean stable isotope ratio 

(δ 13 C=–24.4±0.6‰, δ 15 N=2.7±0.5‰, means ± s.e.) of skin samples 

from nine long-term captive manatees at SeaWorld Of Florida was 

set at 600 days. These animals had been fed a diet of mainly lettuce 

for multiple years. The position of the anchor point at 600 days was 

chosen for several reasons: it was beyond the maximum sampling 

time for all rescued manatees (no manatee was sampled later than 

418 days), plots generally reached an asymptote at or before this 

point, and positions greater than 600 days did not alter results. 

Goodness of fit was first expressed by calculating the coefficient 

of determination (R 2 ) using the anchor point as part of the data set. 

To further illustrate fit, data for skin from each rescued manatee 

were paired with each individual data point contributing to the mean 

anchor point and minimum and maximum R 2 values were computed. 

All statistical analyses were judged to be significant at P

2352 


δ 13 C (‰) 

δ 15 N (‰) 











11 

10 

9 

8 

7 

6 

5 

4 

3 

2 

0 100 200 300 400 500 600 

1 

0 100 200 300 400 500 600 

manatees were also fitted to the exponential decay model (Fig.2). 

Carbon turnover half-lives in the skin of riverine manatees ranged 

from 39 to 72 days with a mean of 59±18 days; however, a halflife 

was not calculated for manatee 0341 because the equation 

showed little to no change in signature over time (Fig.2; Table4). 

Skin samples from these riverine manatees were also enriched 

in 15 N relative to that of captive manatees (mean enrichment= 

6.3±1.6‰) and nitrogen half-lives ranged from 21 to 115 days with 

a mean of 58±42 days (Fig.2; Table4). These turnover times were 

not significantly different from carbon half-lives (paired t-test, 

t=0.13, d.f.=2, P=0.91). MANOVA results indicated there were no 

significant differences in stable carbon or nitrogen isotope half-lives 

between manatees rescued from riverine vs coastal regions (F-test: 

F2,4=0.58, P=0.60). 

DISCUSSION 

Carbon enrichment values calculated in the present study 

(2.8±0.9‰) were similar to values previously reported. Ames and 

colleagues (Ames et al., 1996) found sloughed skin from captive 

manatees to be enriched in 13 C by an average of 4.1‰ compared 

with lettuce. Reich and Worthy (Reich and Worthy, 2006) assumed 

a carbon enrichment value of 3.0‰ in manatee skin when applying 

an isotope mixing model (Phillips and Gregg, 2001) to diet 

interpretation of free-ranging manatees. The only other known study 

on diet–tissue discrimination in any mammalian skin is that of 

Hobson and colleagues (Hobson et al., 1996) in which seal skin 

was found to be enriched in 13 C relative to diet by 2.8‰. In the 

present study, nitrogen enrichment could not be determined because 

Coastal manatees Riverine manatees 

Animal ID Half-life 



0301 63 days –12 

0334 72 days 

0318 60 days 

0322 45 days 


0340 39 days 

0341 N/A 

0431 42 days –16 

0501 67 days 


0301 36 days 

0318 33 days 

0322 14 days 

0431 23 days 







11 

10 

9 

8 

7 

6 

5 

4 

3 

2 

1 

0 100 200 300 400 500 600 

Days since diet change 

0 100 200 300 400 500 600 


0334 115 days 

0340 34 days 

0341 62 days 

0501 21 days 

Fig. 2. 13 C and 15 N turnover in epidermis from manatees rescued near Naples and Cape Canaveral (coastal manatees) and from the St Johns River (riverine 

manatees) in Florida. Mean (±95% CI) stable isotope ratios for skin from long-term captive manatees () were used as ‘anchor points’ set at 600 days to 

better fit the models. To illustrate diet–tissue discrimination, mean (±95% CI) stable isotope ratios for the main diet items fed in captivity (romaine lettuce and 

spinach) are indicated by a horizontal solid black line and horizontal dashed lines. 


of the high degree of variability of nitrogen signatures in the lettuce 

diet. Typically, diet–tissue discrimination values for nitrogen are in 

the range 2–5‰ (Peterson and Fry, 1987; Kelly, 2000). 

Manatees rescued from coastal regions were ideal subjects for 

carbon isotope turnover calculations because carbon signatures in 

their skin differed dramatically from those of captive manatees. 

Interpreting δ 13 C values in the skin of riverine manatees was 

problematic because of variability in values at the time of rescue 

and the similarity of δ 13 C values between the skin of rescued 

manatees and that of long-term captive manatees. The half-lives in 

skin from riverine manatees were not significantly different from 

those of skin from coastal manatees; however, the carbon turnover 

data for manatees rescued from riverine regions did not fit the 

exponential decay models as closely as those for coastal manatees. 

The carbon half-life calculated for manatee epidermis was very 

slow compared with previous turnover studies on other species. 

Stable isotope turnover rates can differ based on the particular 

isotope, tissue and/or taxon analyzed, diet, physiological state, 

feeding rate and/or growth rate of the animal (e.g. Fry and Arnold, 

1982; Bosley et al., 2002; Hobson and Bairlein, 2003; Olive et al., 

2003). Additionally, some studies removed lipids from samples 

while others did not. Therefore, direct comparisons between studies 

are difficult. Dalerum and Angerbjorn (Dalerum and Angerbjorn, 

2005) cautioned that comparisons of turnover rates should be made 

between the same tissues to avoid these complications. Additionally, 

turnover rates in tissues should be compared between animals of 

similar body size as metabolic rates have an effect on isotope 

turnover (Sponheimer et al., 2006).

The present study is the first to calculate stable isotope turnover 

rates in the skin of any marine mammal species. Isotope turnover 

rates that have been reported for large terrestrial mammals including 

bears (Hilderbrand et al., 1996), alpacas (Sponheimer et al., 2006), 

and domestic cattle and horses (Schwertl et al., 2003; Ayliffe et al., 

2004) were determined using blood, muscle and liver, and hair, 

respectively. As no appropriate comparison between turnover rates 

in the skin of large mammals was possible, the results from this 

study will be cautiously compared with others. Previous studies on 

stable isotope ratios in hair were omitted from this comparison as 

hair is a metabolically inert tissue in which the isotopic composition 

represents the period of growth. 

The only reported carbon half-lives in animal tissue that are 

greater than those of manatee epidermis are those of alpaca muscle 

[179 days (Sponheimer et al., 2006)], bat wing membrane and whole 

blood [102–134 days (Voigt et al., 2003)], and quail bone collagen 

[173 days (Hobson and Clark, 1992a)]. In the alpaca study, muscle 

tissues were not lipid extracted so direct comparisons may be 

problematic. Voigt and colleagues (Voigt et al., 2003) suggested 

the slow turnover rate in bat wing membrane was largely due to the 

tissue being composed primarily of collagen and elastin, which are 

known to have slow turnover rates in bone. Additionally, Voigt and 

colleagues (Voigt et al., 2003) attributed the slow turnover rate in 

bat blood to their long-lived erythrocytes. Finally, the long half-life 

in quail bone aligns with collagen being a less metabolically active 

tissue. Epidermal tissue is composed of keratin in the epithelial 

lamina and collagen and elastin in the basal lamina. Manatee 

epidermis has been described as thick and possesses the 

characteristic of hyperkeratosis (Sokolov, 1982; Graham et al., 

2003). It is possible that a slow replacement of keratin in manatee 

Manatee stable isotope turnover 

Table 4. Exponential decay equations and half-lives representing stable isotope turnover in epidermis sampled from rehabilitated Florida 

manatees 

R 2 range 

Animal Half-life δ13C at 

Carbon turnover ID Equation R2 (days) day 0 (‰) Min. Max. 

Coastal manatees 0301 y=–24.4+14.2e –0.01094x 1.00 63 –10.2 1.00 1.00 

0318 y=–24.8+15.1e –0.01158x 0.97 60 –9.7 0.96 0.97 



Mean 53 –10.7 

Riverine manatees 0334 y=–24.6+8.2e –0.00963x 0.95 72 –16.4 0.90 0.96 

0340 y=–24.7+0.9e –0.01787x 0.36 39 –23.8 0.05 0.51 

0341 y=–23.8+1.9e –20920x 0.50 n.d. –21.9 0.43 0.51 


Mean 59 –20.1 

R 2 range 

Animal Half-life δ15N at 

Nitrogen turnover ID Equation R2 (days) day 0 (‰) Min. Max. 

Coastal manatees 0301 y=2.3+3.4e –0.01918x 0.96 36 5.7 0.83 1.00 

0318 y=2.4+2.4e –0.02125x 0.57 33 4.8 0.46 0.62 



Mean 27 5.9 

Riverine manatees 0334 y=2.6+4.9e –0.00601x 1.00 115 7.5 0.98 1.00 




n.d., not determined (see text). 

Mean 58 9.1 


2353 

epidermis and the presence of collagen and elastin in the basal lamina 

also contributed to the slow isotope turnover rate in the skin. 

Another potentially significant factor impacting on turnover rate 

is the manatees’ overall slow metabolism. Metabolic rates in adult 

Florida manatees have been shown to be lower than those predicted 

based on body size [15–40% of predicted values (Irvine, 1983; 

Worthy et al., 2000)]. It is also possible that food passage time 

impacts on turnover rate [as discussed by Post (Post, 2002)]. 

Manatees use hindgut fermentation and have a passage rate through 

the digestive tract of 146–147h (Lomolino and Ewel, 1984; Larkin 

et al., 2007). This rate is consistent with that of the dugong, another 

sirenian [145–166h (Lanyon and Marsh, 1995)], but much slower 

than those of other large hindgut fermenters such as elephants 

[21–46h (Rees, 1982)], horses [26–27h (Rosenfeld et al., 2006)] 

and rhinoceros [61h (Clauss et al., 2005)]. Manatees sampled in 

the present study were rescued for reasons including cold stress, 

entanglement and watercraft injuries. Because of their physical 

condition, their intake rates may have been slower than those of 

manatees not in need of rehabilitation. 

The gruel mixture fed to the manatees for the first few weeks of 

rehabilitation was enriched in 13 C compared with lettuce and 

spinach. It is presumed that the initial supplementation of the diet 

with gruel would have had minimal to no impact on the carbon 

turnover rate as turnover was already very slow. There were no 

significant differences in δ 13 C values between biopsy and sloughed 

skin samples, so the differing sample types had no effect on carbon 

turnover rate. Carbon isotope ratios of manatee fecal material did 

not differ from those of the main diet items, so even if manatees 

were engaging in coprophagy it would not have had any effect on 

carbon turnover rate in the skin. This result is another indication

2354 


that stable isotope analysis of fecal material has great potential in 

assessing short-term, recent dietary choices. 

Phillips and Koch (Phillips and Koch, 2002) suggested 

incorporating carbon and nitrogen concentration analysis to aid in 

stable isotope dietary reconstruction, especially when there are great 

differences in C and N concentration between diet items. We were 

unable to include a concentration analysis in this study; however, 

it may be a useful addition to future analyses. 

Coastal manatees were poor subjects for nitrogen turnover 

calculations because of the high variability in their initial δ 15 N values 

at the time of rescue, the similarity of δ 15 N values between the skin 

of rescued animals and that of captive animals, and the high 

variability in δ 15 N values of captive diet items. Consequently, 

calculated nitrogen half-lives were inconsistent. Riverine manatees 

were better subjects because there was a greater difference in 

nitrogen signatures of skin between rescued and long-term captive 

animals. Even then, nitrogen half-lives for skin from riverine 

manatees were still variable, most likely because of the variability 

in nitrogen signatures of romaine lettuce and spinach fed in captivity. 

The lettuce and spinach in the captive manatee diet often originated 

from different agricultural producers and it is possible that different 

fertilization techniques were used resulting in high variability in 

δ 15 N values (see Georgi et al., 2005). 

There are very few studies on nitrogen turnover in other species. 

Nitrogen half-lives in mammalian tissues have been calculated for 

blood plasma and cells in black bears [3 and 22 days, respectively 

(Hilderbrand et al., 1996)] and avian whole blood [10.0–14.4 days 

(Bearhop et al., 2002; Hobson and Bairlein, 2003; Ogden et al., 

2004)] and plasma [0.5–1.7 days (Pearson et al., 2003)]. Nitrogen 

turnover in manatee skin was relatively slow compared with the 

results of these studies, most likely owing to the low metabolic rate 

of manatees, epidermal tissue composition and/or food passage rate 

as previously discussed in terms of carbon turnover. 

There was no compounding effect of the gruel supplement on 

nitrogen turnover rate as the signature of the gruel was not 

significantly different from that of romaine lettuce and spinach. 

Likewise, coprophagy would have had no effect on nitrogen 

turnover rate in manatee skin as the δ 15 N values of manatee fecal 

material did not differ from those of the main diet items. However, 

sloughed skin samples were significantly enriched in 15 N compared 

with biopsy samples. Though δ 15 N values were adjusted to account 

for this enrichment, variability in nitrogen turnover rates and lack 

of fit indicate that sample type may have contributed to the difficulty 

in calculating more precise half-lives. At the present time, it is 

unclear why sloughed samples differed in δ 15 N values, but not δ 13 C 

values, from biopsy samples. It is possible that materials were 

redistributed within the skin while sloughing, and sloughed samples 

also contained less epidermal depth than biopsies. Both of these 

factors could have contributed to differing δ 15 N values between 

sample types. 

Cerling and colleagues (Cerling et al., 2007) and Ayliffe and 

colleagues (Ayliffe et al., 2004) have suggested that some stable 

isotope turnover data may be better fitted to a multiple-pool model 

than to the traditional single-pool, exponential decay model used 

in the present study. Proper application requires knowledge of each 

pool in vivo (Sponheimer et al., 2006), which at this time is unknown 

for manatees. Consequently, we did not incorporate a multiple-pool 

analysis. Single-pool analyses are still useful for intraspecific and 

interspecific comparisons of stable isotope turnover (Sponheimer 

et al., 2006). 

When proportions of food sources contributing to a mixed diet 

are unknown, mixing models are often used to aid in estimating these 


proportions (e.g. Phillips and Gregg, 2001; Newsome et al., 2004; 

Reich and Worthy, 2006). If a change in diet occurs, the resulting 

signature may not be representative of the current diet but, in fact, 

may be some intermediate value between two distinct diets. While 

this possibility is true for all stable isotope analyses, the impact is 

minimized in tissues with high turnover rates because the time frame 

is short. Free-ranging manatees are known to switch diet sources 

(Best, 1981; Lefebvre et al., 2000), and the very slow turnover rates 

for carbon and nitrogen stable isotopes in epidermis tissue mean that 

unless the manatee has been feeding on the same diet for an extended 

period of time, the skin signature will always be in some transitional 

state. Slow turnover rates in manatee skin especially complicate 

estimation of the proportions of freshwater, estuarine and marine 

sources in the diet because δ 13 C values for estuarine vegetation are 

intermediate between those of freshwater vegetation and seagrasses 

(Reich and Worthy, 2006) (C.D.A.-S. and G.A.J.W., in preparation). 

The incorporation of nitrogen stable isotope analysis can aid in further 

separation of these three diet sources as nitrogen signatures for 

freshwater and estuarine vegetation differ from those of seagrasses 

(C.D.A.-S. and G.A.J.W., in preparation). 

Computing a precise diet–tissue discrimination value is essential 

when interpreting isotopic results. Discrimination values for carbon 

have previously been calculated for manatee skin on a captive diet 

(Ames et al., 1996) and discrimination values for carbon and nitrogen 

have been estimated in the skin of free-ranging manatees on 

possible diets of freshwater, estuarine and/or marine vegetation 

(Reich and Worthy, 2006). It is unknown whether diet–tissue 

discrimination in manatee skin differs between diet types as has 

been shown in other studies (e.g. Hobson and Clark, 1992b). The 

results of the present study are the most extensive thus far. 

Carbon and nitrogen stable isotope analysis of manatee epidermal 

tissue is difficult, if not impossible, to use when assessing shortterm 

or recent changes in diet and habitat use because of slow 

turnover rates. This technique would potentially have more direct 

application in summarizing average dietary intake over longer 

periods of time. In order to accurately interpret isotopic analyses, 

determining diet–tissue discrimination factors and turnover rates in 

the tissue is essential. The difficulty with most studies is that isotope 

discrimination and turnover are best calculated under controlled 

situations in captivity. Mixing model results for tissues with slow 

turnover rates should be interpreted with caution, especially in 

species that may be switching between diets in which an intermediate 

isotope ratio may be mistakenly described as indicating a single 

diet source instead of a mixture of sources. 

We thank R. Bonde, M. Ross and B. Chittick for assistance with manatee skin 

sample collections and we are grateful for funding from the University of Central 

Florida (UCF) Department of Biology and Graduate Studies to C.D.A.-S. and a 

Provosts Research Enhancement Award to G.A.J.W. Manatee research was 

carried out under UCF-Institutional Animal Care and Use Committee protocol 02- 

09W and US Fish and Wildlife Service (USFWS) permit number MA056326 

issued to G.A.J.W. and USFWS permit number MA791721 issued to R. Bonde. 

Plant samples were collected under Florida Department of Environmental 

Protection plant collection permit number 1753 issued to G.A.J.W. We thank J. 

Roth and J. Weishampel for assistance with editing and J. Fauth for assistance 

with statistical analyses. Additional thanks to T. Maddox, R. Harris, R. Runnels, T. 

Doyle, K. Fuhr, J. Greenawalt, L. Hoopes, A. Stephens, M. DiPiazza, N. Browning 

and J. Stanley for field and lab assistance. 

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historic bottlenose dolphin populations reflected through stable isotopes. Mar. 

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Japan. Mammal Study 29, 179-183.

Trend Detection in a Boat-based Method for Monitoring Sirenians: Antillean Manatee 

Case Study 

Katherine S. LaCommare a* , Solange Brault a , Caryn Self-Sullivan b , Ellen M. Hines c 

a University of Massachusetts, Boston 100 Morrissey Blvd. Boston, MA 02125 

katie.lacommare@umb.edu, solange.brault@umb.edu 

b Sirenian International, Inc., 200 Stonewall Dr. Fredericksburg, VA 22401 caryns@sirenian.org 

c Department of Geography and Human Environmental Studies, San Francisco State University, 

1600 Holloway Ave. San Francisco, CA 94132 ehines@sfsu.edu 

Abstract. Accurate monitoring is a critical step in evaluating the conservation and management 

needs of endangered species. We evaluated a low cost, effective survey method for monitoring 

West Indian manatees (Trichechus manatus manatus) in Belize, Central America. The 

objectives for this paper are (1) to evaluate a count-based population index derived from a boatbased 

survey method, (2) to examine trends in manatee abundance in the Drowned Cayes area, 

(3) to conduct a power analysis to explore our ability to detect a trend and the ramifications of 

survey structure on trend detection. We used a generalized linear model to evaluate the impact 

of environmental conditions on sighting probability and to determine whether the number of 

manatees observed per 20-minute scan changed from 2001 - 2007. We used simulations to 

determine statistical power - the ability to detect potential declines of 10%, 25% or 50% over 15 

years and for various sampling regimes. The number of manatees sighted per scan was not 

affected by sighting conditions. There was no change in the mean number of manatees sighted 

per scan from 2001 to the 2007. Our ability to detect a trend ranged from 9% to 100% 

depending on the level of decline, scan duration, number of points surveyed and number of 

surveys. This survey protocol is a practical and repeatable way to examine population trends of 

sirenians in similar habitats around the world. 

Keywords: Monitoring, trend detection, power analysis, West Indian manatees, Trichechus sp., 

sirenians, boat surveys. 

*Corresponding author: Tel. (248) 756-3985. E-mail addresses: kslacommare@gmail.com. 

Abbreviations: IUCN- International Union for the Conservation of Nature; SPAW- Specially Protected 

Areas and Wildlife; CITES- Convention on International Trade of Endangered Species, MMPA – Marine 

Mammal Protection Act 

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1 Introduction 

All four extant species in the order Sirenia are vulnerable to extinction due to small 

population sizes, population declines, fragmentation and continued exploitation (Deutsch et 

al. 2010; Lefebvre et al. 2001; Marsh and Lefebvre 1994). They are listed as vulnerable on 

the IUCN Red List (Deutsch et al. 2010), protected by CITES (CITES 2010), the SPAW 

protocol (CEP 2010), the Memorandum of Understanding on the Conservation and 

Management of Dugongs (CMS 2010), the US Endangered Species Act (USFWS 2001), 

and other national and international wildlife protection laws (see Quintana-Rizzo and 

Reynolds 2008). For many sirenian populations, little information exists on their status 

(e.g. Hines et al. 2005; Lefebvre et al. 2001; Marsh and Lefebvre 1994; Quintana-Rizzo and 

Reynolds 2008). Monitoring – a preliminary step in determining conservation status, 

effects of exploitation and improving management decisions (Gibbs 2000; Gibbs et al. 

1998; Marsh and Trenham 2008; Martin et al. 2006) – is the process of gathering data to 

draw inferences about population abundance changes over time (Yoccoz et al. 2001). 

Monitoring is listed as a key objective in most manatee (Trichechus spp) and dugong 

(Dugong dugon) conservation and management plans (eg. Auil 1998; CEP 1995; USFWS 

2001). 

As others have pointed out, “the need for high quality data is clear, the means for 

getting it is not (Dawson et al. 2008, p. 20; USFWS 2001),” especially for small 

populations of marine mammals that live in complex coastal and riverine habitats – 

conditions that constrain survey designs (see Dawson et al. 2004; Dawson et al. 2008; Dick 

and Hines 2011; Hines et al. 2005; Williams and Thomas 2009). A well designed 

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monitoring program requires two key components: a reliable population index and 

powerful statistical analysis. Indices are a proxy for population abundance (Caughley 

1977; Gibbs 2000; Kindberga et al. 2009) and are based on the premise that systematic 

surveys will detect the same proportion of the population over time. Thus, changes in the 

number of animals detected reflect changes in population size (Gibbs 2000). To be a good 

surrogate to population size, an index must have a positive, linear relationship with actual 

abundance (Gibbs 2000; Gibbs et al. 1998; Williams and Thomas 2009), and a constant 

detection probability over habitat, sighting conditions and time (Anderson 2001; Gibbs 

2000; Gibbs et al. 1998; Thompson 2004; Williams and Thomas 2009). 

Detecting trends in abundance depends on statistical power (Gerrodette 1987; Gibbs 

2000; Gibbs et al. 1998; Taylor and Gerrodette 1993) and an effective monitoring program 

must generate data that can be statistically analyzed to detect trends (Gibbs 2000; Gibbs et 

al. 1998). Both the accuracy of the population index and sampling structure – number of 

plots, survey frequency, scan duration, number of years – will affect the ability to detect 

changes in population abundance. Power analysis, through simulation, is the process used 

to determine the statistical power of an index and sampling regime (Gerrodette 1987; Gibbs 

2000; Gibbs et al. 1998; Taylor and Gerrodette 1993). 

Most sirenian populations are found in developing nations where monitoring funds 

are scarce. To be valuable, monitoring methods must be sound, repeatable and inexpensive 

(Aragones et al. in press; Aragones et al. 1997; Dick and Hines 2011; Hines et al. 2005; 

Williams and Thomas 2009). This paper evaluates a low cost and repeatable boat-based 

method for monitoring sirenians. We used this method on West Indian manatees 

(Trichechus manatus manatus) in the Drowned Cayes area of Belize, Central America and 

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examined trends in manatee abundance from 2001-2007. Through simulations, we 

conducted a power analysis to determine trend detection ability and the ramifications of 

sampling structure on trend detection. 

2. Materials and Methods 

2.1 Study area 

The Drowned Cayes, including Swallow Caye, are a string of mangrove islands -14 km 

long by 4 km wide - along the central coast of Belize, 10-15 km east of Belize City and 3-5 

km west of the Belize Barrier reef (Figure 1). These islands are surrounded by shallow 

seagrass beds. The depth of the study area is less than 1 meter in some places and is never 

greater than 6 meters. The study area also encompasses two points along the Belize Barrier 

Reef. Prior to this study, aerial and boat surveys and DNA analyses documented that this 

area has an important population of manatees (Auil 2004; Bengston and Magor 1979; 

Hunter et al. 2010; LaCommare et al. 2008, Morales-Vela et al. 2000; O'Shea and Salisbury 

1991, Self-Sullivan 2008). 

This study area is typical of manatee coastal habitat making it appropriate for 

testing our survey protocol. It comprises: shallow water (1-3m deep), proximity to deeper 

channels (3-6 m) for escape from danger (boats), freshwater sources, aquatic vegetation 

(mostly submerged), warm water (17°C minimum temperature), shelter from storms, 

waves, strong winds and currents; and travel corridors between habitat areas (Moraes- 

Arraut et al. in press). 

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2.2 Survey design 

We devised a point-based survey design to monitor manatee occurrence by counting the 

number of manatees sighted during a 20-minute period at designated locations throughout 

the Drowned Cayes area (Figure 1). We marked 54 permanent points throughout the study 

area with a global positioning system (GPS) and used a small (8m) fiberglass boat to survey 

the points on a regular basis. To minimize boat and engine-noise disturbance to the 

manatees, we maneuvered the boat with a 8-meter pole when we were within 100 meters of 

the exact point location. During this time, 3 - 13 observers started scanning for manatees. 

At least three experienced observers were on the boat at all times. Experienced observers 

included one of the two of the authors (KSL and CSS), a field assistant that worked with 

the authors for the entire study and student interns that spent 3 – 6 months at the field site. 

Student interns were trained to spot manatees – nose, tail, back - and signs of manatees - 

shadows under the water, tail pressure wave, disturbed silt, floating grass -by the authors 

and field assistant. The number of inexperienced, but trained observers (volunteers), 

ranged from 0 to 10. Inexperienced observers were trained to spot manatees and manatee 

signs by the authors, field assistants and interns at the beginning of each two-week session. 

Volunteers were introduced to manatee viewing first via a PowerPoint lecture and then 

asked to practice spotting and viewing live manatees by visiting Swallow Caye Wildlife 

Sanctuary – a local manatee sanctuary and viewing area. Once anchored in position with 

the pole, observers searched for manatees in a 360 o circle around the boat. Having at least 

three experienced manatee spotters on the boat at all times ensured that experienced 

observers could cover the entire 360 degree circle and not rely on volunteers to detect 

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manatees. A manatee was counted if a tail, back, nose or entire manatee was spotted. If a 

manatee was spotted by an inexperienced observer, it was only counted if it was confirmed 

by an experienced observer. From 2001-2007, we conducted these point scans 4 - 8 times 

per year during two-week survey sessions and sampled the points without replacement for 

the two-week period. Since not all points could be surveyed in one day, we divided the 

study area into 8 zones with 4 – 6 points each. Each day, we randomly chose the survey 

zone and starting point and then surveyed 4 – 5 points. 

2.3 Index and detection probability 

Our population index was the number of manatees sighted per 20-minutes per point. A 

valid population index must have a constant, linear relationship with manatee abundance. 

Two conditions can violate this assumption. When using call indices (indices that rely on 

animal calls such as frog calls or bird songs) or presence/absence data (Gibbs 2000; Gibbs 

et al. 1998), high population densities have an asymptotic relationship between the index 

and abundance. Alternatively, low population densities can have a threshold below which 

animals will not be detected (Gibbs 2000; Gibbs et al. 1998). 

We were not using presence/absence data or call indices, and since we were 

evaluating population declines rather than population increases, we were more concerned 

with the problem of a bottom threshold than population saturation. This point-based 

method has been successfully used to locate and count small and sparse populations of 

manatees in: Lake Volta, Ghana; Estero Hondo, Dominican Republic; and Lake Ossa, 

Cameroon (Self-Sullivan, personal communication; Dominquez, personal communication). 

This method can detect manatees at low population densities. To further evaluate this 

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assumption, we divided our locations into high-sighting probability sites (>30% probability 

of sighting a manatee per scan) and low-sighting probability sites (< 30% probability of 

sighting a manatee per scan) (LaCommare et al. 2008). We then examined cumulative 

histograms of time to first sighting for both categories. We expected that each histogram 

would have a similar asymptotic curve indicating that our ability to detect manatees was 

similar for high versus low-sighting probability locations. 

The relationship of the index to the actual number of animals counted is also a 

function of detection probability (Anderson 2001; Gibbs 2000; Gibbs et al. 1998; 

Thompson 2004; Williams and Thomas 2009) – the ability to detect an animal when it is 

present (MacKenzie and Royle 2005). Three classes of variables affect this: observers, 

environment and species behavior. For each point scan, we counted the number of 

manatees and recorded variables that might influence detection probabilities. We used a 

generalized linear model (GLM) with a negative binomial distribution and a log-link 

function to determine whether the number of manatees sighted was influenced by sighting 

conditions. This distribution was the most appropriate for our over-dispersed (variance 

greater than the mean) Poisson-distributed response variable, number of manatees (Agresti 

1996; Quinn and Keough 2002). Our predictor variables were: environmental conditions 

(sun glare - yes/no, precipitation -dry/light rain, cloud cover -clear/scattered clouds/partly 

cloudy/overcast, Beaufort sea state -0/1/2/3, swell height -in 0.15m increments; water 

clarity and time of day), and manatee behavior (disturbed/feeding/resting/social/travel/ 

undetermined - Table 1). Water clarity was a measure of the horizontal distance between 

an underwater observer and Secchi disk held 0.5 meters under the water. Water clarity was 

measured in this fashion because the vertical Secchi depth was usually greater than or equal 

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to the depth. We did not take seasonality into account because previous analyses indicated 

that there is no difference in seasonal sighting probability within the Cayes (LaCommare et 

al. 2005; Self-Sullivan 2008). 

To test whether detection probability was influenced by number and experience of 

volunteers we used a generalized linear model (GLM) with a negative binomial distribution 

and a log-link function to determine whether the number of manatees sighted was 

influenced by number of volunteers and year (Table 2). 

2.4 Trends of manatee counts in the Drowned Cayes 

Forty-two survey periods were conducted over 79 months from 2001-2007. We used a 

GLM with negative binomial distribution and a log-link function to determine whether 

there was a change in the number of manatees per 20-minute scan from the first survey 

period in 2001 to the last survey period in 2007. 

2.5 Power analysis of trend data 

We used simulations, following Taylor and Gerrodette (1993) and Gibbs (1998, 2000), to 

determine the statistical power of our ability to detect a trend. We fit a negative binomial 

distribution to our manatee count data from our 20-minute scans for the whole 2001 - 2007 

period. Using the parameters from this distribution, we generated a random array of the 

number of manatees for 28 points for each of 6 survey periods per year. The potential 

number of manatees sighted was truncated at 5 since we only had 1 sighting with more than 

5 manatees in 7 years. We chose this sampling regime because this most closely matched 

our annual survey structure from 2001 – 2007. We repeated this process for 15 “years”. 

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Then we examined whether we could detect a decline in the number of manatees over that 

15 year period. We generated our random array, added a linear trend, and ran our GLM 

1000 times to determine our ability to detect each of three declines in the number of 

manatees at the end of these 15 years: slight (10%), moderate (25%) and precipitous (50%). 

These declines are equivalent to a 0.7%, 1.7% and 3.6% annual decrease in the number of 

manatees sighted per 20-minute scan. We considered that a negative trend was detected if 

the slope of the model in each simulation run was negative and significantly different from 

zero. Following Taylor et al. (2007), we chose a 15 year period for our power analysis. 

2.6 Power analysis of sampling design 

Survey structure affects variability in detection probability and therefore statistical power 

(Gibbs 1998, 2000). Number of plots, sampling frequency, sampling interval and scan 

duration interact to influence statistical power and need to be considered when designing a 

monitoring protocol. These factors also influence the cost and time of monitoring. 

Therefore, determining the most efficient experimental design can be critical to carrying 

out an effective monitoring program. In the field, we sampled approximately 28 of our 54 

points during two-week survey periods, 4-8 times per year. Each point was scanned for a 

minimum of 20 minutes. A fraction of the point scans lasted 30 minutes, but this decreased 

the number of points that could be sampled in any one day and during a two-week survey 

period. How does a 30-minute scan duration with fewer samples impact our ability to 

detect a trend? Using data that we collected from our 30-minute scans, we generated new 

negative binomial distribution parameters and a new random array of the number of 

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manatees for 21 sampling points per two-week survey period for 6 survey periods per year 

and repeated our power analysis as described above. 

In the Drowned Cayes, 28 out of 54 point scan locations have a greater than 30% 

probability of sighting a manatee (LaCommare et. al, 2008). Would restricting our survey 

protocol to locations with a higher sighting probability yield a greater ability to detect a 

trend? We generated new negative binomial distribution parameters using our manatee 

count data from 2001 - 2007 from locations with a greater than 30% probability of sighting 

a manatee (LaCommare et. al 2008). Using these parameters, we generated a new random 

array of the number of manatees for 28 sampling points for 6 two-week survey periods. 

We repeated our power analysis as described above. From that distribution, we also created 

an array of the number of manatees for 8 two-week survey periods with both 28 and 21 

points and for 8 two-week survey periods, 28 points with just a 20-minute scan duration. 

3. Results 

3.1 Index and encounter probability 

Histograms of time-to-first sighting indicate that for locations that had a greater than 30% 

probability of sighting a manatee, 90% of all manatees are sighted within the first 20 

minutes of a 30-minute scan (Figure 2). For locations that had a less than 30% probability 

of sighting a manatee, it took slightly longer to spot the first manatee and 90% of all 

manatees were sighted within 24 rather than 20 minutes (Figure 2). 

The number of manatees sighted per scan was not affected by sighting conditions 

(overall Likelihood Ratio Chi-Square = 12.578, df = 18, p = 0.816, n= 131, Table 1). None 

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of the individual factors or covariates had a significant influence on the number of 

manatees sighted per scan (Table 1). 

There was a negative effect between number of volunteers and number of manatees 

spotted (Wald Chi-Square = 7.343 df =1, p < 0.007, Table 2). The greater number of 

volunteers present on the boat, the fewer number of manatees spotted. 

3.2 Trends of manatee counts in the Drowned Cayes 

We conducted 960 20-minute scans during 42 survey periods from 2001 - 2007. The 

number of manatees sighted per scan ranged from 0 to 6. Overall mean number of 

manatees sighted per scan was 0.54 (0.89 SD) (Figure 3). Mean number of manatees per 

survey period ranged from 0.21 to 1.08 manatees per scan. Yearly means per scans ranged 

from 0.33 manatees in 2002 to 0.71 manatees in 2001 (Figure 4). There was no detectable 

change in the mean number of manatees sighted per scan from the first survey period in 

2001 to the last survey period in 2007 (Likelihood Ratio Chi-Square = 1.56, df = 1, p = 

0.212, B = -0.003, Figure 4). 

3.3 Power Analysis 

Using a 20-minute scan duration, 28 points per survey period, and 6 periods, we had 4% 

power to detect a 10% decline in number of manatees over 15 years within 7 years – our 

study duration, 9% power to detect a 25% decline and 22% power to detect a 50% decline. 

Extending this study duration to 15 years would give us a 11% power to detect a 10% 

decline, 51% power to detect a 25% decline and 100% power to detect a 50% decline 

(Table 3; Figure 5a, b, c). 

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3.4 Power Analysis of sampling design 

The highest power, i.e. 16%, 71% and 100% after 15 years, is achieved for all three decline 

rates when 28 points with a high (>30%) probability of sighting a manatee are surveyed 8 

times per year (Table 3). This survey design has a 90% power to detect a 50% decline by 

the 11 th year (Figure 5c). The design with the least power, i.e. 8%, 34% and 99% after 15 

years, surveys just 21 points, regardless of the probability of sighting a manatee, 6 times a 

year (Table 3). Overall, survey protocol changes had little impact on our ability to detect 

slight declines over 15 years, but did impact our ability to detect moderate and precipitous 

declines (Figure 5a, b, c) over that time horizon. Increasing the number of scan points from 

21 to 28 had about the same effect as increasing the scan duration from 20 to 30 minutes 

(about a 10% increase in power to detect moderate declines). Increasing the number of 

survey periods from 6 to 8 resulted in an increase in power from 57% to 71% in the 

moderate decline scenario (Table 3). Differences in power across designs are not observed 

before 10 years of survey in the case of slight declines, 8 years for moderate declines, and 6 

years for precipitous declines (Figure 5a, b, c). All designs show the same basic result: 

only precipitous declines can be detected with a 100% certainty on a 15 year time horizon 

(Figure 5a, b, c). 

4. Discussion 

Using 30-minute point scans from a small boat platform is an effective and repeatable 

method for monitoring manatees in typical manatee habitats around the world. Several 

authors debate the validity of population indices in comparison to population estimates - the 

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former characterized as estimating relative abundance, the latter absolute abundance (see 

Thompson 2004; Williams and Thomas 2009). These authors caution against the use of 

indices in favor of more robust estimating procedures such as distance sampling or mark- 

recapture procedures (e.g. Anderson 2001; Williams and Thomas 2009). Yet, as long as the 

population index is linearly related to actual abundance – that is it doesn’t have an 

asymptote or bottom threshold, and detection probabilities are constant over space and 

time, count-based indices are valid (Skalski et al. 1983; Thompson 2004; Williams and 

Thomas 2009). 

Species behavior – long dive times, short surfacing bouts - and severely limited 

resources hamper the ability to conduct robust monitoring procedures on Antillean 

manatees and other sirenians in developing nations (Aragones et al. in press; Aragones et 

al. 1997; Dawson et al. 2008; Dick and Hines 2011). Distance sampling requires the ability 

to consistently measure the distance from the observer to the animal using a range finder, 

reticulated binoculars or spotting scope (Buckland et al. 2001). Sirenians often surface 

very briefly and only expose their nose to the surface when breathing. In our study, even 

the best trained observers captured distances via range finder only 10% of the time 

(LaCommare and Self-Sullivan, personal observation). Mark-recapture methods are 

equally challenging. It is estimated that 50% of manatees in the study area are scarred by 

boats (Self-Sullivan 2008). Although possible (Self-Sullivan 2008; Auil and Powell, 

personal communication), above-water photo identification methods are difficult because 

manatees in Belize and other tropical habitats do not seasonally aggregate at warm water 

sites, nor do they tend to float at the surface, exposing their scarred backs. Therefore, 

photo-identification via underwater video capturing techniques is more appropriate. 

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However, this involves considerable time and effort by the observer and does not always 

yield individual identification due to lack of natural markings and/or poor visibility in many 

habitats (LaCommare and Self-Sullivan, personal observation). Preliminary analysis 

indicates that population abundance estimates via mark-recapture techniques might be 

possible (Self-Sullivan 2008, Auil & Powell, Personal communication). Distance sampling 

and photo-identification requires considerable observer training. Equipment and observer 

training may price monitoring programs out of reach of most wildlife and conservation 

agencies in developing nations (Aragones et al. in press; Aragones et al. 1997). 

Our index does not appear to have a bottom threshold below which manatees are not 

detected, but 30-minutes is a better scan duration than 20-minutes. The histograms of time- 

to-first-sighting indicate that for locations with a greater than 30% probability of sighting a 

manatee, roughly 90% of all manatees are sighted within the first 20 minutes of a 30- 

minute scan. But, for locations with a less than 30% probability of sighting a manatee, it 

takes longer to spot the first manatee and it takes up 24 minutes before 90% of all manatees 

are sighted. 

Based on our analysis of possible influences on detection probability, the 

relationship between our index and population abundance is constant over conditions and 

time because environmental conditions and manatee behavior do not appear to significantly 

influence the number of manatees sighted. This is a surprising result. Visibility bias, bias 

from the result of observers missing animals due to observer inconsistencies and 

environmental conditions, is significant in aerial surveys for manatees (See Packard et al. 

1985 and Wright et al. 2002). Sighting conditions such as water clarity, turbidity, sea state 

and surface glare have all been shown to affect visibility (i.e. Reynolds and Wilcox 1994) 

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in aerial surveys. There are two principal reasons why these factors may not affect 

visibility of manatees from boats. From a boat, observers search for manatees across the 

horizontal plane of the water looking for signs of the manatees’ body (a nose, tail or back) 

breaking through the surface of the water. Water clarity isn’t going to affect this to the 

same extent as aerial surveys in which observers are searching for manatees within the 

water column. In extremely turbid water, like that found in “black water” lake and river 

systems of the Amazon, lower vantage points allow better visibility of an animal breaking 

the surface of the water than do higher vantage points (Aragones et al. in press). Sea state 

may not impact visibility because when surface choppiness is slight – sea state of zero or 

one – any disturbance to the surface of the water is noticeable and therefore manatees will 

be spotted. Because manatees need to rise their nose above the water to breathe, when 

there is a sea state of two or three – choppy conditions – manatees will raise their entire 

head out of the water (Personal observation, KSL and CSS) which facilitates the observer’s 

ability to spot manatees and negates the impact of sea state on visibility. Surveys were not 

conducted in a sea state higher than three. It is not clear why surface glare does not impact 

visibility. There are three possible explanations. Surveys are conducted between 9:30 am 

and 4:30 pm when surface glare, due to a sun low on the horizon, is at a minimum. 

Multiple trained observers searching for manatees may reduce the negative effects of sun 

glare. And, manatees usually surface multiple times during a 30-minute search duration 

which increases the possibility of spotting a manatee even during difficult observation 

conditions. 

The biggest concern with our study was that number of volunteers had a negative 

effect on our ability to spot manatees. The greater the number of volunteers the fewer 

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number of manatees spotted. Volunteers are easily distracted by each other during long 

scan periods and survey days and do not have the same level of focus as trained observers. 

This can easily be minimized in the future by limiting the number of volunteers present 

during surveys. 

We do not know the relationship of our index to actual abundance. It is an index of 

relative abundance that can be used to detect trends. Index validation, by comparing the 

number of manatees counted via boat surveys to the number counted during concurrent, 

localized aerial surveys, could provide an indication of the relationship between boat counts 

and aerial survey counts which could help determine bias and thus the relationship of our 

index to actual abundance. Aerial surveys were conducted along the entire Belizean 

coastline, including the Drowned Cayes, from 1997 – 2002 (Auil, 2004). These surveys 

overlapped with our boat surveys in 2000 - 2002, but were only conducted once during the 

wet and once during the dry season and did not directly correspond to our survey effort and 

unfortunately, are not useful for evaluating bias of our method. It is interesting to note that 

the trends of Auil’s (2004) index of relative abundance from 2000-2002 mirrors our trends 

across those same years. 

There was a very slight negative trend in the data, but this trend was not significant. 

Our analysis indicates that we would have only had a 4%, 9% and 22% power to detect 

slight, moderate or precipitous declines after 7 years – our study duration. Even slight 

negative trends can be important for small populations which can be impacted by stochastic 

events or behavioral biology that can drive small populations to extinction (Meffe and 

Carroll 1997) or prevent these populations from recovering (Meffe and Carroll 1997). The 

Antillean subspecies of the West Indian Manatee is currently listed as endangered on the 

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IUCN Red List because it is a small and declining population without ongoing, effective 

conservation actions (Self Sullivan et al. 2011). These data provide confirmation of the 

appropriateness of the current IUCN status and highlight the need to improve our ability to 

establish the magnitude of decline. 

Extending our study to 15 years considerably improves our ability to detect a 

population trend. Over a study duration of 15 years, we would still have a limited ability to 

detect slight and moderate declines, but our index and protocol can detect precipitous 

declines within the benchmarks established in the Marine Mammal Protection Act, the 

IUCN Red List (Taylor et al 2007) and other publications. Taylor et al. (2007) defined a 

precipitous decline in marine mammal abundance as a 50 percent decline after 15 years 

because a 50% decline over this period would result in a stock being classified as 

“depleted” under the MMPA. Under the IUCN Red List guidelines, a decline of this 

magnitude could result in a status designation anywhere between “vulnerable” to 

“endangered” depending on initial population size, cause, certainty and the reversibility of 

the decline (IUCN 2010). IUCN Red List guidelines establish level of endangerment – 

nearly threatened to critically endangered – based on declines of 10 – 90% over 10 years or 

3 generations (whichever is longer), depending on initial population size, cause, certainty 

and the reversibility of the decline (IUCN 2010). Bart et al. (2004) recommended a 

standard for landbird surveys of an 80% power to detect a 50% decline over 20 years. 

Similarly, Hatch (2003) recommended a standard for counts of colonial seabirds of a 90% 

power to detect a 50% decline over 10 years. Using this sampling regime over a 15 year 

time interval, we would have a power of 11%, 51% and 100% to detect slight, moderate or 

precipitous declines. All of our survey protocols had 100% power to detect 50% declines 

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over 15 years making it a valuable tool for determining population status based on the 

benchmarks discussed above. Taylor et al. (2007) found that most marine mammal 

monitoring programs had a low power (0-50%) to detect precipitous declines in abundance 

within this time frame. 

We can improve the power of our survey protocol by surveying at least 28 points, 8 

times per year, increasing our scan duration to 30-minutes and choosing locations with a 

30% sighting probability. Under this regime, we have 100% power to detect a 50% decline 

over a 15 year period. We have a power of 90% to detect a 50% decline after 10 years – 

exceeding the MMPA benchmark. The power of this sampling regime also meets the 

IUCN guidelines for establishing whether a population should be listed as critically 

endangered, endangered or vulnerable (IUCN, 2010). We would still have a limited ability 

to detect slight (16% power) declines, but a reasonable ability (71% power) to detect 

moderate declines. The IUCN benchmarks for establishing the vulnerability status of small 

populations for whom the causes and reversibility of declines are uncertain range from 10 – 

30 % declines over 3 generations (60 years for manatees, (Deutsch et al. 2008)). 

To ensure the greatest success in a monitoring program, pilot studies are highly 

recommended (Aragones et al. in press; Buckland et al. 2001; Gibbs 2000; Gibbs et al. 

1998; Scheiner and Gurevitch 2001; Thompson 2004). Local knowledge can be utilized in 

pilot studies to locate high use areas in a short period of time – e.g. 1 year (Self-Sullivan 

and LaCommare, personal observation). Including local knowledge in research programs 

also has the effect of improving success in corollary conservation programs - e.g. poaching 

reduction programs (Aragones et al. in press; Kendall 2009). In addition to being a 

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practical and repeatable way to examine population trends, boat surveys can be used to 

assess spatial distribution and habitat use (LaCommare et al. 2008). 

4. Conclusion 

Using a small-boat platform for systematic surveys is a sound and repeatable 

method for monitoring sirenian populations in developing nations where constraints on 

fiscal resources are severe. We recommend pilot studies and using local knowledge to 

locate high use areas and then using a 30-minute scan duration to conduct point scans. Our 

analysis indicates that surveys should be conducted at least 8 times per year and at least 21 

points should be included in the sampling protocol. For our study area, we estimate this 

monitoring protocol would require approximately 37 dedicated days on the water per year 

(4-5 scans per day, 3 days per month) with the only expenses being boat, fuel, and three 

well-trained observers. Alternatively, this protocol would be well suited for the eco- 

tourism industry where well trained local tour guide/researchers could conduct one or two 

scans during each tour, which are randomly distributed among 21 sites with a >30% 

sighting probability. 

Acknowledgements. We thank Earthwatch Institute for substantial financial support and 

Earthwatch Volunteers for logistical support and data collection. We thank Conservation 

Action Fund for financial support that specifically supported capacity building among local 

field assistants and tour guides. We are ever grateful to Mr. Sidney Turton and Spanish 

Bay Resort, who provided logistical and in kind support from 2001-2004, and to Ms. 

Teresa Parkey and The Hugh Parkey Foundation for Marine Awareness and Education, 

who provided logistical and in kind support in 2005 - 2007. Supplemental financial support 

was provided by two individual Earthwatch volunteers (Mr. Greenwalt, amd Mr Burtt), 

Project Aware, Virtual Explorers and the Lerner-Gray Marine Research Fund (AMNH). 

We are grateful to the numerous interns and field assistants who were vital to data 

collection and field logistics. One author (CSS) was also supported by an NSF Graduate 

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Fellowship from 2001-2003. We are especially thankful for the help and guidance of our 

colleague, friend, primary field assistant and source of traditional knowledge, Mr. Gilroy 

Robinson. Finally, we thank two anonymous reviewers whose comments greatly improved 

this paper. 

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Table 1. Results from the GLM relating number of manatees to variables that may influence detection probability (n = 113). 

Dependent variable is number of manatees. Independent variables are number of volunteers, total number of observers, 

precipitation, cloud cover, sea state, swell height and behavior. 

Variables in the Model 

df Significance 

Wald Chisquare 

n = 131 

Precipitation (subcategories: dry/light rain)* 0.426 1 NS 

Cloud cover (subcategories: clear/scattered/partly cloudy/overcast)* 0.267 3 NS 

 

 

 

 

 

Dependent 

variable 

Number of manatees 

 

 


Environment 

variables 

 

 

 

Sea state (subcategories: Beaufort scale – 0/1/2/3)* 0.174 3 NS 

Glare (subcategores: yes/no)* 0.002 1 NS 

Swell Height 0.001 1 NS 

Secchi Distance 0.481 1 NS 

Sighting Time 0.604 1 NS 

Manatee Behavior* 

Behavior (subcategories: disturbed, feed, mill, rest, social, travel, other) 2.916 7 NS 

*No significant subcategories 

 

 

26

Variables in the Model 

df Significance 

Wald Chisquare 

n = 597 

Dependent variable 

Number of manatees 


Number of volunteers 7.343 1 0.007 

Number of volunteers * Year 

2001 1.620 7 NS 

2002 0.013 1 NS 

2003 1.094 1 NS 

2004 0.616 1 NS 

2005 0.243 1 NS 

2006 0.338 1 NS 

2007 * * * 

Table 2. Generalized linear model (GLM) with a negative binomial distribution and a log-link function to determine 

whether the number of manatees sighted was influenced by number of volunteers and year 

 

 

 

 

27

28

Table 3. Simulation results: Percentage of declines detected (in bold italics) for six different sampling regimens and three different 

levels of decline, assuming a perfectly consistent relationship between population index and actual abundance (1000 runs for each 

simulation). Scan duration indicates whether the negative binomial distribution parameters were generated from 20 or 30-minute 

scans. Number of points indicates the number of points used to create the array of manatee sightings for the simulation models 

Parentheses indicates which points were used to generate the negative binomial distribution parameters. > 30% means points with 

greater than 30% sighting probability. Number of two-week survey periods indicates the number of survey periods used in the 

Sampling Regime 

Scan Interval 20-minute scan 30-minute scan 

6 8 6 6 8 8 

21 

(>30 %) 

28 

(>30 %) 

28 

(>30 %) 

21 points 

(all points) 

28 points 

(>30% ) 

28 points 

(all points) 

Num. of two-week survey 

periods 

Num. of points 

(Points used to generate 

negative binomial 

distribution parameters.) 

Results 

10% 11 14 9 12 16 13 

25% 51 65 33 57 71 60 

50% 100 100 99 100 100 100 

simulation. We ran our simulation for three potential declines in the number of manatees after 15 years: 10%, 25% and 50%. 

These declines are equivalent to a 0.7%, 1.7% and 3.6% decrease in the number of manatees sighted per scan per year. 

 

 

 

29

Figure 1. Map of the Drowned Cayes area and scan points 

30

a. 

b. 

c. 

Number of sightings 



100 

80 

60 

40 

20 

70 

60 

50 

40 

30 

20 

10 

0 

25 

20 

15 

10 

5 

0 

0 

1 2 5 8 9 14 17 20 23 26 29 

Figure 3. Histogram of number of manatees counted per 20-minute point scan (mean = 

0.54, SD = 0.891, n = 960) with negative binomial distribution (solid line). 

32

2001 2002 2003 2004 2005 2006 2007 

Figure 4. No significant trend in mean number of manatees sighted per 20-minute scan 

was detected from 2001-2007 in the Drowned Cayes area of Belize (Likelihood Ratio Chi- 

Square = 1.56, df = 1, B = -0.003, p = 0.212 (NS), n = 960). Error bars: +/- 1 SE. Bottom 

axis is number of the survey period. Number of manatees per 20-minute scan was the 

dependent variable. Independent variable was the time over which the forty-two survey 

periods were conducted. 

33

a. 

b. 

c. 

Power 

Power 

Power 

100 

80 

60 

40 

20 

0 

100 

80 

60 

40 

20 

0 

100 

80 

60 

40 

20 

0 

20 min 6 teams 28 pts 





 


2 4 6 8 10 12 14 15 

2 4 6 8 10 12 14 15 

2 4 6 8 10 12 14 15 

Number of years 

34 

> 30 % 

sighting 

probability

Figure 5. Power to detect 10% (a), 25% (b), and 50% (c) declines in the number of 

manatees over 15 years. 

35

2012 COURSE DATES: AUGUST 4 – 17, 2012 - Sirenian International

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