Behaviors of the pelagic red crab Pleuroncodes planipes observed ...

Behaviors of the pelagic red crab Pleuroncodes planipes(Decapoda: Anomura: Galatheidae) observed in captivity.Diane C. Tulipani and Michel A. BoudriasAbstract.—Little is known about the typicalbehaviors of the pelagic red crab Pleuroncodesplanipes (family Galatheidae). The crabs wereobserved in an aquarium to determine the typicalrepertoire of behaviors. An activity budget wasdeveloped to address two important questions: 1)how important are locomotory behaviors amongoverall red crab behavior; and 2) what additionalnon-locomotory behaviors comprise the behavioralrepertoire of red crabs. Locomotory behaviorsexecuted by the crabs were only 15% of the totalobserved behaviors and were divided into active(90.4%) and passive (9.6%), or benthic (41.9%)and water column (58.1%) components. Activelocomotory behaviors included “power swimming,”“hovering,” “walking” and “climbing,”while “sinking slowly” was the only passive behavior.The crabs spent nearly 79% of their timein feeding and grooming their exoskeleton and6.1% interacting with other crabs. The locomotorybehaviors of captive red crabs are correlatedwell with in situ observations where they feed onplanktonic organisms in the surface waters duringearly stages of their life, alternately swimmingto the surface and sinking down in the water.INTRODUCTIONBehavioral studies contribute to understandingthe interrelationship between evolutionarydevelopment and the possible environmentalinfluences on observed behaviors (Warner,1977; Dunham, 1983; Carefoot, 1989). Thetypes of general behaviors common to all animalsencompass locating food and feeding,mating and reproduction, defense, grooming,locomotion, and agonistic behaviors (Dunham,1983). Locomotory behaviors mainly consistof walking, swimming, crawling, and floating;these behaviors are essential for animals to findfood, escape predators, migrate to new locationsor find mates.Locomotory behaviors of crustaceans aretypically responses to environmental cues(Dunham, 1983). Rhythms and orientationcues of long- or short-distanced movementsare based on a variety of conditions. There aredaily short migrations to feeding areas (Boyd,1967; Aurioles-Gamboa & Pérez-Flores, 1997),long distance seasonal migrations for matingand egg-laying (Dunham, 1983; Tankersley etal., 1998), migrations based on circadian andcircatidal rhythms linked to temperature orlight (Jansson & Källander, 1968; Dunham,1983; Wilber & Herrnkind, 1986; Chatterton& Williams, 1994), and inshore and offshoremovements in order to reduce physiologicalstress and mortality (Dunham, 1983; Wilber &Herrnkind, 1986; Jury et al., 1994).Galatheid crabs Pleuroncodes planipes,or pelagic red crabs, make daily migrations tosurface waters to feed on the rich abundanceof plankton found in the upwelling coastalwaters of the Pacific Ocean along the BajaCalifornia peninsula (Longhurst, 1967; Kato,1974; Aurioles-Gamboa & Pérez-Flores, 1997;Robinson & Gómez-Gutiérrez, 1998). Theyare found in great abundance along the westerncoastline of Baja California Sur (Boyd, 1962;Blackburn, 1977; Longhurst, 1967; Aurioles-Gamboa, 1992; Robinson & Gómez-Gutiérrez,1998) where they form large surface swarmsthousands of miles north of their known breedinggrounds (Boyd, 1967; Longhurst, 1969;Kato, 1974; Aurioles-Gamboa et al., 1994).There have been numerous studies that have focusedon the pelagic red crab’s population den-

68 D. C. Tulipani & M. A. Boudriassity (Boyd, 1962; Longhurst, 1967; Aurioles-Gamboa & Pérez-Flores, 1997), its ecologicalrole in the Baja California peninsula coastalwaters and its viability as a productive fishery(Longhurst, 1967; Kato, 1974; Robinson &Gómez-Gutiérrez, 1998).However, little is known about the typicalbehaviors of P. planipes. Kato (1974)briefly described how they swim to the surface,change posture to a parachute-shaped pose,and then feed while slowly sinking. This briefdescription leaves some important questionsunanswered: 1) how important are locomotorybehaviors to overall red crab behavior; and 2)what additional non-locomotory behaviors comprisethe behavioral repertoire of the red crabs?In this study, the red crabs were observed in anaquarium to determine the typical repertoire ofbehaviors and to develop an activity budget forall locomotory and non-locomotory behaviorsas part of an on-going larger study of locomotionin this species (Tulipani, 2005).MATERIALS AND METHODSGeneral procedurePleuroncodes planipes in captivity wereunder frequent, but not continuous, personalobservation each day. Total observation timefrom June 2001 to September 2003 was approximately800 hours. At any given time overthis period, there were a varying number of redcrabs, from a few up to 100, in an aquariumat the University of San Diego. The crabs incaptivity were videotaped and photographed atvarious times during the study period in supportof behavior, kinematic, fluid dynamic, andlocomotory behaviors analyses.Specimen collection and careIn June 2001, the first group of approximately90 P. planipes was collected, using alarge dip net, from the surface waters at themouth of Bahía Magdalena (24º32.89’ N and112º02.63’ W) on the southwestern coast of theBaja California peninsula in Baja CaliforniaSur, Mexico. Fifteen crabs were transportedlive to the University of San Diego via automobile.Another group of approximately 100crabs was collected from various San Diego,California beaches during multiple strandingevents that occurred over the course of nearlythree weeks from the end of April to early May2002.The crabs were kept at the University of SanDiego in a 250-gallon aquarium with a recirculatingfiltration and cooling system under thecycle of light (07:00 to 21:00) and dark (21:00to 07:00) periods. In addition to daytime observations,the crabs were observed with the aidof a flashlight at various times during the darkphotoperiod. The retention area of the aquariumwas approximately 2.5 m (x-axis) long and 66cm wide (y-axis) with the water depth (z-axis)approximately 1 m. The water temperature wasmaintained between 15–18ºC. The crabs werefed squid once a day and supplemented withphytoplankton and pellet food, with all uneatenfood removed after several hours.Activity budgetFor the purpose of developing a “typical “or “average” activity budget for the red crabs incaptivity, undisturbed activities of a total of 30randomly chosen crabs were videotaped for 15minutes per crab, five crabs on each of six differentoccasions on 23 May, and 8, 12, 20, 22,and 25 June 2002. Using a 8 mm video cameramodel RCA Pro842 attached to a tripod, behaviorswere recorded twice during morning hours(8:00 am–10:00 am Pacific Daylight-savingsTime (PDT), on 8 and 25 June 2002), twiceduring afternoon hours (1:30 pm–4:30 pm PDT,on 20 and 22 June 2002), and twice duringevening hours (6:00 pm–8:30 pm PDT, on 23May and 12 June 2002). The tapes were eachviewed twice, once to categorize the behaviorsand secondly to count the number of times eachbehavior occurred.The behaviors were grouped into two broadcategories: locomotory and stationary, andthese were further broken into subcategoriesthat were more descriptive. Locomotory behaviorwas defined as that conducted when a crabmoved from one place to another and included:1) swimming (using tail-flips for propulsion)

Behaviors of Pleuroncodes planipes 69Fig. 1. Illustration of swimming bout by Pleuroncodes planipes: A) launch from bottom, B) tail-flipswimming, C) breach surface of water, D) sink, E) landing on side wall. Illustration by D. Tulipani.(Fig. 1A–C), 2) sinking (Fig. 1D), 3) surfaceswimming pattern (whereby the crab stays nearthe water’s surface to feed) (Fig. 2A), 4) hovering(crab maintains vertical position within thewater column by using several abbreviated tailflips)(Fig. 2B), 5) walking (Fig. 2D), and 6)climbing (Fig. 2C).Stationary behavior defined as the crabstanding relatively still on a surface was dividedinto three subcategories: 1) interactions withanother crab, included a) pushing, b) bumping,c) landing on (Fig. 2F), d) sparring (Fig. 2E),e) tail-flick, and f) antenna flick; 2) “groomingbehavior” was based on which body part wasbeing cleaned and usually entailed the scrubbing,rubbing, or wiping of these various bodyparts with one (or both) of the two modifiedfifth pereopods, wiping an eye with both maxillipeds,or by dragging an antenna between themaxillipeds; 3) “feeding behavior” was basedon the appendage by which food was capturedand transferred to the mouth region. The abovementionedsubcategories 2) and 3) had moredetailed components based only on the greatervariety of modes of collecting food and areas ofgrooming.Each occurrence of behaviors was tallied ona datasheet during the 15-minute observationtime for each crab. The tallies for each behaviorwere totaled and summarized. Terminology and

70 D. C. Tulipani & M. A. BoudriasFig. 2. Illustration of various locomotory and stationary behaviors by Pleuroncodes planipes: A) surfaceswimming pattern, B) hovering, C) climbing, D) walking, E) sparring, F) landing on. Illustration by D.Tulipani.function described by Bauer (1989) were followedfor the fifth pereopods.Analysis of active swimming and passivesinking sequencesOn 13 and 14 September 2001, the swimmingactivity of four crabs in the aquarium wasvideotaped for two hours each day, using bothan RCA Pro842 8mm and a Panasonic VHS-CPalmcorder IQ model PV-IQ405D video cameras,one attached to a tripod and the otherhandheld. Prior to videotaping, a laminatedgrid (2.54 cm x 2.54 cm squares) was attachedto the back of the aquarium to provide a scaleof horizontal and vertical linear distance. Thevideos were then viewed on a Sony DA Pro4-head VCR, Model SLV-373UC, with stopframecapabilities. Individual swimming boutswere identified for each crab and the crab’s vertical,horizontal and diagonal movements wererecorded, with particular note of ‘power swim’segments and passive sinking segments of eachbout. The elapsed duration of each swimmingbout was calculated based on the start and endtimes recorded while reviewing the videotapes.RESULTSGeneral behavioral observationsAll of the captive Pleuroncodes planipesroutinely observed throughout their captivitywere active at all times of the day and night.

Behaviors of Pleuroncodes planipes 71Fig. 3. Activity budget of Pleuroncodes planipes. Percentage of total activities spent on stationary (feeding,grooming, and interactions with other crabs) and locomotory behaviors.Although many of the crabs were capturedswimming in surface waters, all quickly settledto a mostly benthic lifestyle when introduced tothe aquarium. Common behaviors of decapods,such as swimming, climbing, feeding, grooming,molting, and interacting with each other,were noted at all times during both light anddark photoperiods. When food items, like cutsquid, were dropped into the aquarium, activefeeding was observed, sometimes with aggressiveinteractions between crabs over pieces offood. Crabs would catch, hold, and sometimestear pieces of food with their chelipeds whileeating it.Activity budgetAll of the behaviors observed throughoutthe period of captivity were performed by all ofthe red crabs. Based on the videotaped observations,captive red crabs spent 85% of their totalactivities performing stationary behaviors (Fig.3). Of the stationary behaviors, the majorityof their activity was feeding behaviors, whichaccounted for 66.4% of all observed activitieswhere the crabs performed any of the five feeding-relatedactivities. Grooming as a whole was12.5% of the behaviors (Fig. 3). Interactionswith other crab were 6.1% of all behaviors (Fig.3).Locomotory behaviors accounted for 15%of the total crabs’ observed activities (Fig.3) which included walking (35.7%), surfaceswimming (23.5%), power swimming (16.2%),sinking (9.6%), hovering (8.8%) or climbing(6.2%) (Table 1). These six behaviors werefurther categorized as active or passive movement(Table 1), but only sinking (comprising9.6% of locomotory behaviors) was considereda passive locomotory behavior, as a crab didnot actively move any of its appendages whileit sank. Of all locomotory behaviors, 90.4%were active, with the crab using its appendagesto move in the water column or on a surfacewithin the aquarium (Table 1).The locomotory behaviors were furthercategorized into water column or benthic forthe captive crabs (Table 1) which is reflectiveof reported in situ behaviors of red crabs. Watercolumn behaviors (swimming, sinking, surfaceswimming, and hovering) accounted for 58.1%

72 D. C. Tulipani & M. A. BoudriasTable 1. Activity budget of Pleuroncodes planipes.Detail of locomotory behaviors. See text fordefinition of each behavior.Locomotory behaviors (15%)Active PassiveWater Column:Surface Swimming 23.5%Swimming 16.2%Sinking 9.6%Hovering 8.8%Subtotal 48.5% 9.6% 58.1%Benthic:Walking 35.7%Climbing 6.2%Subtotal 41.9% 0.0% 41.9%Total 90.4% 9.6% 100.0%of all locomotory behaviors, while benthicbehaviors (climbing and walking) comprisedthe other 41.9% (Table 1).Therefore, the crabsspent the majority of the locomotory time activelymoving around in the water column.Locomotory behaviorA swimming bout was a finite event thatbegan once a crab launched itself from a surfacein the aquarium and ended when the crablanded on some other surface in the aquarium(Fig. 1). For example, a complete swimmingbout could start with a crab hanging head downfrom one of the side walls of the aquarium, thenlaunching itself away from the wall, performingseveral tail-flips, alternatively sinking andtail-flip swimming, until landing on the bottom.A ‘power swim’ segment was defined as a portionof a swimming bout when a crab rapidlymoved in a curved or straight path using manyconsecutive tail-flips without stopping until itreached the surface of the water, a side wall, orperformed another maneuver (Fig. 1B).Swimming consisted of propulsive tail-flipsexecuted with the abdomen and tail fan whilethe crab adopted a streamlined swimming position,moving around in the water column. Atail-flip consisted of five sequentially occurringmovements that, when combined, generatedthe propulsive force that moved a crab rapidlyin a posterior and dorsal direction (Fig. 4A–D). First, a tail-flip started from the positionwhere the abdomen was contracted and the tailfan was flat against the thoracic plate (Fig. 4A).Second, there was an extension of the abdomenand tail fan posteriorly (Fig. 4B). Third,when the abdomen was at its maximum extension,the tail fan was extended perpendicular tothe abdomen at the fourth abdominal segmentwith a simultaneous abduction of the uropods(Fig. 4C). Fourth, this was followed by a rapidcontraction of the abdomen with the telson anduropods still expanded (Fig. 4D). Fifth, the tailflipended with a contraction of the abdominalmuscle to press the retracted tail fan againstthe thoracic plate of the crab producing a jet ofwater that propelled the crab posteriorly anddorsally. This final position was the same as thefirst and completed the tail-flip propulsion (Fig.4A).During some swimming bouts, crabs couldhover in mid-water by using several tail-flickswhere the abducted tail fan beat against theabdomen without the full abduction-adductioncycle of the uropods (Fig. 2B). In this case,the crab positioned its body with its rostrumpointing to the bottom of the aquarium, thecurved dorsal edge of its abdomen pointingto the water’s surface, and all of thoracic legswere extended away from the body; once inthis posture, it executed numerous tail-flicks.This particular motion did not create a full jetof water like that in tail-flip swimming. Thusthe crab maintained its relative vertical positionin the water column with this sequence ofmovements. While hovering, crabs sometimesdrifted horizontally due to the water flow in theaquarium.Passive sinking segments were identifiedeasily when a crab splayed out all of its legs,extending them so that none were touching, andslowly sank without moving any appendages.The general body shape in the passive sinkingposture was similar to the shape of an openedparachute, and the setae that line the pereopodsand chelipeds passively extended away fromboth the medial and lateral edges of all limbs tobe perpendicular to the limb (Tulipani, 2005).

Behaviors of Pleuroncodes planipes 73Fig. 4. Pleuroncodes planipes in swimming posture, ventral view (left) and left lateral view (right), withabdomen and tail in: A) 1st position of tail-flip, B) 2nd position of tail-flip, C) 3rd position of tail-flip, D) 4thposition of tail-flip. Illustration by V. Ruiz.Passive sinking continued until the crab landedon the bottom or side wall, hovered, or performedanother series of tail-flips to move toanother location in the aquarium.Using pereopod pairs 2, 3, and 4, red crabswalked or climbed in any direction (anteriorly,posteriorly, or laterally), over the rocks andplastic tubing on the bottom of the aquarium,holding their two chelipeds extended anteriorlyand elevated from the bottom’s surface (Fig. 2).The plastic grating lining the side walls enabledthe crabs to climb to the top of the aquarium,stopping just below the water’s surface (Fig. 2).Stationary behaviorsWhen stationary, red crabs stood with theircheliped tips touching the surface they were on.Grooming behaviors appeared to concentrateon setal maintenance whereby a crab kept thesetae on the carapace and pereopods free fromvisible fouling particles. Using the distal end(propodus and dactylus) of one or both chelatefifth pereopods, which are covered with sickleshapedsetae (Fig. 5), crabs wiped, rubbed, orscrubbed their pereopod in the same directionas the orientation of the body setae. Crabsused the cleaner pereopod to clean the entire

74 D. C. Tulipani & M. A. BoudriasFig. 5. Fifth pereopod of Pleuroncodes planipes. 1)Scanning electron micrograph of the distal end ofthe chelate 5th right pereopod. The limbs are usedmainly clean the exoskeleton and setae. Females uselimbs to stir the fertilized eggs after mating. 2) Rightlateral view of posterior body showing 5th pereopodtucked along the side of the carapace (black arrow).Scale: 1 block = 2 mm.body surface as well. A crab would sometimesscrub the tip of the cleaner pereopod againsta groove in its exoskeleton to loosen particlestrapped by the setae. Crabs folded their chelipedsmedially and posteriorly, enabling thecleaner pereopod to reach the entirety of theselimbs. Additionally, crabs used their maxillipedsto wipe the end of the cleaning pereopods,their antennae and their eyes. When groomingstopped, crabs typically folded and partiallytucked the distal ends of the fifth pereopodsunder the lateral posterior edge of the carapace(Fig. 5).Frequently, grooming behavior was immediatelyfollowed by feeding behavior wherePleuroncodes planipes would use their maxillipedsto wipe off the tip of the fifth pereopod,which was immediately followed by the anterior-posteriormovement of the mandibular palps.The movement of the maxillipeds towards themouth region appeared to transfer particles tothe mouth. The mandibular palps would waverapidly towards and away from the mouth tomove the particles into the mouth. In addition,captive red crabs were observed feeding,independent of grooming, while standing onthe bottom of the aquarium or hanging from aside wall. With the rostral spine tilted slightlyupwards, crabs would extend and retract theirmaxillipeds away from and then towards theirmouth region generating water movement(visible as the movement of food particles)towards their mouth while intermittently oscillatingtheir mandibular palps. Occasionally,red crabs quickly scraped the dactyl tip of oneof the pereopods along the bottom, kicking upparticles and moving them towards the maxillipeds,which in turn would capture any particlesthen move them towards the mandibular palpsand mouth. In the aquarium, red crabs quicklysensed any food dropped into the tank, moveddirectly towards it, and collected as much asthey could hold with their chelipeds and/ormouthparts. Some crabs even performed a coupleof tail-flips moving away from other crabspreventing them from potentially stealing thefood.Regarding interactions between individuals,crabs were often observed walking into,bumping, pushing, or landing on other crabsthat were standing on the bottom or hangingfrom a side wall (Fig. 2). When a crab approachedor bumped into another, typical agonisticbehaviors observed were either apparentaggressive behaviors or avoidance behaviors.Both crabs would usually move away whensuch an encounter occurred. Sometimes neithercrab moved to avoid the other despite antennaeflicks or tail fan flexions from the opponent.Sparring occurred when one crab approachedanother head-on without giving way (Fig. 2).The stationary one would open the dactyls onits chelipeds and gesture forward while raisingthe chelipeds up slightly towards the approach-

Behaviors of Pleuroncodes planipes 75ing crab. This type of gesturing usually resultedin the approaching crab changing directions.Sparring between males also occurred whenone male approached a female that was beingguarded by another male either prior to or justafter mating.DISCUSSIONPleuroncodes planipes have been describedas dividing their time between the benthos duringthe day and the epipelagic zone to feed atnight (Boyd, 1962; Blackburn, 1977). However,the crabs were also found in large surfaceswarms during the day (Boyd, 1967; Aurioles-Gamboa, 1992) and are considered the mostabundant nektonic organism off southern BajaCalifornia waters (Blackburn & Thorn, 1974).When the crabs were initially collected forthis study, they were small (standard carapacelength < 32 mm), which corresponded with thepelagic phase of their life cycle (Boyd, 1967);they floated frequently and could not walk wellwhen stranded on the beaches. However, afterbeing introduced into the aquarium with numeroussurfaces to rest on, P. planipes began toexhibit more benthic behaviors. Once in captivity,the red crabs seemed to grow quickly andmany of those collected in April 2002 moltedafter only a month in the aquarium. Over time,they adopted a mainly benthic lifestyle withintermittent periods of swimming, hovering andpassive sinking. This change in the red crabs’behavior from planktonic to mostly benthic wasalso observed of the captive crabs kept in anaquarium by Boyd (1962).Boyd (1967) described red crabs as voraciouseaters, with an omnivorous diet. This hasbeen supported by observations in the watercolumn off southern Baja California where redcrabs feed on phytoplankton and zooplankton(Longhurst, 1967) and even ingest particulateorganic matter when on the ocean bottom(Aurioles-Gamboa & Pérez-Flores, 1997). Redcrabs moved their maxillipeds and then theirmandibular palps every few seconds ingestingfood particles or moving water towardsthe mouth. Similar limb motions have beenobserved in palinurid lobsters, and many othermalacostracan crustaceans, where they flicktheir antennules and mouthpart appendages andcreate convective flows of water that facilitatethe tracking of the chemical signatures of food(Goldman & Patek, 2002).Additional limb motion, possibly related tofeeding behaviors, occurred frequently whenthe red crabs groomed themselves. In contrastto some species of brachyuran spider crabs(Macropodia spp.) that attach pieces of algaeto their carapace or those that have modifiedpereopods to hold sponges to their bodies forcamouflage (Dromidia spp.) (Warner, 1977;Ross, 1983), Pleuroncodes planipes spent timemeticulously cleaning their exoskeleton of particlesthat had adhered to it with their chelatefifth pereopods. Bauer (1989) listed numeroussources of fouling particles, such as sediment,unicellular algae, and parasites that can accumulateon the exoskeleton of aquatic crustaceansand negatively impact normal functionsof sensory, respiratory and locomotory behaviors.Accumulated debris on the exoskeleton ofthe red crab may be akin to fouling organismson the hull of a ship (Bauer, 1989). If the exoskeletonwas not frequently cleaned betweenmolts, the fouling particles would build up,eventually modifying the natural streamliningof the red crab’s carapace, pereopods, abdomenand tail-fan with their associated setae.Maintaining the exoskeleton appeared to be animportant function that may enhance the pelagicred crabs’ swimming efficiency by reducingthe drag along the body (Tulipani, 2005).Furthermore, these accumulated particles werea food source for the red crabs.When red crabs interacted with each otherin the aquarium, they preferred keeping somedistance between each other, a common behavioramong crabs which allows them to avoidone another (Warner, 1977; Salmon & Hyatt,1983). When distance was not maintained, agonisticbehaviors (gesturing with chelipeds withdactyls abducted or fighting) and avoidancebehaviors (brief tail-flips away) were observedof red crabs and have been similarly describedfor other decapod crab species (Pilumnus sp.,

76 D. C. Tulipani & M. A. BoudriasPagurus sp., and Callinectes sapidus) (Warner,1977).Crustaceans move from one location toanother for purposes of feeding, mating, or dispersalof juveniles (Dunham, 1983; Wilber &Herrnkind, 1986; Chatterton & Williams, 1994;Tankersley et al., 1998) with the pelagic red crabbeing no different. For example, in the wild,they migrate to surface waters to feed (Boyd,1967; Longhurst, 1967; Blackburn, 1977).The red crabs’ benthic inshore-offshore movementswere associated with coastal upwellingof cold water and the crab’s reproductive cycle(Aurioles-Gamboa, 1992; Aurioles-Gamboa& Pérez-Flores, 1997). Red crabs occupy boththe water column and the benthos in the wild,and the movements observed in the aquariumclearly fell into two subcategories reflective ofwhere they occurred. Of all locomotory behaviors,those occurring in the water column wereobserved more often than the ones occurring onthe bottom of the aquarium (58.1% vs. 41.9%,respectively) (Table 1). Differences in benthicbehaviors in captivity vs. in situ can probablybe attributed to influences of external environmentaleffects of each habitat (Chatterton &Williams, 1994).Swimming in the water column or at thesurface were the most frequently performed activebehaviors of Pleuroncodes planipes (Table1). Boyd (1962) and Kato (1974) anecdotallydescribed the same intermittent swimming patternas a way for the crabs to maintain their relativeposition in the water column. In the wild,pelagic red crabs feed on plankton in the surfacewaters (Longhurst, 1967; Longhurst et al.,1967), therefore, it would be advantageous tothe red crab to stay within the epipelagic zoneas long as possible where phytoplankton andzooplankton are abundant. Swimming rapidlyupwards, followed by slow sinking, in the captivered crabs mirrors the classic behavior patternsseen in their coastal habitat. This uniquelyefficient swimming ability (Tulipani, 2005) hadnever previously been described for galatheids.The red crab’s ability to quickly transition to itsstreamlined swimming posture from its highdragsinking position is probably an adaptationto life in the water column.Red crabs also swim to escape predation,though not like typical swimming brachyurancrabs. Red crabs are not like Callinectes sapidus(Portunidae), which use modified fifthpereopods as swimming paddles (Warner,1977; Welch et al., 1999), nor are they likeTritodynamia horvathi (Pinnotheridae), whichuses its heavily setose pereopods to swim(Takahashi et al., 1999). In physical appearanceand swimming mode, pelagic red crabs moreclosely resemble lobsters and crayfish, whichlead to their common name of squat lobsters(Newland et al., 1992). Red crabs tuck in alltheir thoracic limbs; adopt a streamline bodyshape and swim backwards using tail-flip escapeswimming (Boyd, 1962; Tulipani, 2005).Spanier et al. (1991) described a similar typeof escape response and a similar shape of thetail-fan for the Mediterranean slipper lobster,Scyllarides latus (Scyllaridae). The marineshrimp Crangon crangon, also completely flexesits abdomen, squeezing the tail-fan againstthe thorax giving the appearance of folding itsbody completely in half (Arnott et al., 1998).The mantis shrimp, Squilla mantis, exhibits amaximal tail-flip response to rostral stimuli bycompletely inverting itself then righting itselfwith a half-roll before swimming away (Heitleret al., 2000). Other crustaceans similarly performtail-flip escapes but with species-specificmaneuvers, such as half-twists, lateral rolls, orinversion of the body, during the execution ofthe escape movement (Newland et al., 1988,1992; Arnott et al., 1998; Heitler et al., 2000).Thus P. planipes swims much more like a lobsteror a shrimp than like a brachyuran crab.Further evidence of unusual swimming behaviorsfor a crab can be seen in the hoveringbehavior which could permit red crabs to easilytransition to either swimming or sinking postures.It may have developed in the aquariumbecause there were solid surfaces against whichthe crabs could “lean” while in the water column.Just as treading water can help conserveenergy, hovering has the potential for energeticsavings for captive red crabs, enabling themto swim to the surface with less effort than

Behaviors of Pleuroncodes planipes 77launching from the bottom of the aquarium.Comparisons of field observations of crustaceanactivity to observations of laboratory activitypatterns have shown that the two are notnecessarily the same, and that many organismsmodify their behavior in captivity (Chatterton& Williams, 1994). This seems to be the casewith this hovering behavior of P. planipes in theaquarium. We have not seen any evidence ofhovering in any in situ observations (Tulipani,2005).Yet Kato (1974) suggested that red crabsmaintain their position in the water column,akin to hovering, by alternating between activelyswimming and slowly sinking. Analysisof in situ video of Pleuroncodes planipes supportsthese conclusions (Tulipani, 2005) wherethey swim rapidly upward with several tail-flipsand then slowly sink with limbs extended. Theslow sinking was the only passive locomotorybehavior since the red crabs did not movetheir pereopods or chelipeds while they sank.Movement of their mouthparts indicated typicalfeeding behavior while sinking, observedby Kato (1974) and seen on in situ videotapes(Tulipani, 2005). The repeated surface swimmingand sinking pattern probably enables thelarge swarm of crabs to feed without expendingmuch energy once they have reached the surface.Other smaller crustaceans, such as copepods(Buskey et al., 1996) and mysids (Buskey,1998), also form large aggregations in surfaceswaters yet are usually continually swimmingto maintain their position and expending muchenergy to do so. Feeding while sinking is probablybeneficial energetically for the red crabsbecause once they reach the surface, they stopswimming and simply float before beginningtheir slow, passive descent. After each sinkingsegment, they only need to swim a short time toreach the surface again. This may be analogousto blue crabs (Callinectes sapidus) using tidalcycles to assist long distance travel, migratingup to 1000m day –1 to reach spawning areas (Full& Weinstein, 1992; Tankersley et al., 1998) apotential energetic benefit. It is particularly evidentin gravid female Callinectes sapidus whoapparently use ebb-tides to travel seaward to releaseembryos and then use flood-tides to returnup-estuary afterwards (Tankersley et al.1998).Thus, it appears that Pleuroncodes planipesutilize their complex suite of locomotory behaviors,especially the unique alternation ofefficient jet-propelled swimming and low costslow sinking patterns, to feed more efficiently.Analysis of their body design and fluid dynamicparameters support the contention thatthey are very well adapted to active swimmingand passive sinking (Tulipani, 2005). Thoughlocomotion accounts for only 15% of their totalrepertoire, pelagic red crabs show a clear synergybetween their functional morphology andtheir behaviors. They may not appear that differentfrom other decapods in their stationarybehaviors but their unique swimming modes setthem apart from other crabs.Acknowledgements.—Special thanks go toLisa M. Baird, Mary Sue Lowery, and Anne A.Sturz for their editorial assistance and criticalreview of this manuscript, as well as to MissVanessa Ruiz for the wonderful illustrationsincluded in this paper as well as my Master’sthesis. We would also like to thank the Schoolfor Field Studies staff in Puerto San Carlos,BCS, Mexico for their logistic support. Fundingfor this research was provided by the MarineScience Dept. at the University of San Diego,the TransBorder Institute at the University ofSan Diego, a Hannon Foundation fellowship(DCT) and the Coca-Cola Foundation.LITERATURE CITEDArnott, S. A., Neil, D. M., & Ansell, A. D., 1998.Tail-flip mechanism and size-dependentkinematics of escape swimming in thebrown shrimp Crangon crangon. Journal ofExperimental Biology, 201:1771–1784.Aurioles-Gamboa, D., 1992. Inshore-offshoremovements of pelagic red crabs Pleuroncodesplanipes (Decapoda, Anomura, Galatheidae) offthe Pacific Coast of Baja California Sur, Mexico.Crustaceana, 62:71–84.Aurioles-Gamboa, D., Castro-González, M. I., &Pérez-Flores, R., 1994. Annual mass strandingsof pelagic red crabs, Pleuroncodes planipes(Crustacea: Anomura: Galatheidae), in BahíaMagdalena, Baja California Sur, Mexico. Fishery

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Behaviors of Pleuroncodes planipes 79Swimming behavior of the pinnotherid crab,Tritodynamia horvathi, observed during thelow temperature season. Journal of the MarineBiological Association of the United Kingdom,79: 375–377.Tankersley, R. A., Wieber, M. G., Sigala, M. A.,& Kachurak, K. A., 1998. Migratory behaviorof ovigerous blue crabs Callinectes sapidus:evidence for selective tidal-stream transport.Biological Bulletin, 195: 168–173.Tulipani, D. C., 2005. Functional morphology andfluid dynamics of swimming in the pelagic redcrab, Pleuroncodes planipes. xv + 295 pp., M.S.thesis, University of San Diego.Warner, G. F., 1977. The Biology of Crabs. 202 pp.,Van Nostrand Reinhold Company. San Francisco,California.Welch, J. M., Forward, R. B., & Howd, R. A., 1999.Behavioral responses of blue crab Callinectessapidus postlarvae to turbulence: implications forselective tidal stream transport. Marine EcologyProgress Series, 179: 135–143.Wilber, D. H., & Herrnkind, W. F., 1986. The fallemigration of stone crabs Menippe mercenaria(Say) from an intertidal oyster habitat andtemperature’s effect on locomotory activity.Journal of Experimental Marine Biology andEcology, 102: 209–221.Addresses: DCT, *MAB, Marine Science &Environmental Studies Department, University ofSan Diego, 5998 Alcala Park, San Diego, CA 92110,U.S.A.; e-mails: (DCT) dctulipani@yahoo.com,(MAB) boum@sandiego.edu*Author for correspondence