Can Squirrel Monkeys and Crab - University of Miami

Can Squirrel Monkeys and Crab-Eating Macaques Learn to Use NovelVisual Cues to Help Them Forage?Elijah BogdanskyBhargavi PochiRondy PowellPatrick EspitiaFelipe DelgadoCatherine MartinezAshley BellingerResearch in EcologyUniversity of Miami

ABSTRACTThe constant changes of natural environments expose many organisms to novelchallenges. Among those challenges are the introduction or disappearance of seasonalfood sources such as fruit and flowers. Primates often use vision as their primary sense tofind food. As a result of these organisms changing environment, natural selection shouldfavor the ability of primates to quickly learn to use novel visual cues to help them forage.Here, we testes whether two species of Monkeys, crab-eating macaques (Macacafasicularis) and squirrel monkeys (Saimiri bolivianesis peruviensis) would learn to usenovel visual cues to help them find food. We tested this hypothesis by setting up feedingstations with a red and green bucket containing food rewards and recording whether themonkeys could learn which colored buckets contained the food with the highest reward.Both species of monkeys quickly learned that the red buckets contained their preferredfood (grapes) and clearly used the red color to find this food reward. However, it seemsthat the monkeys also use other visual and auditory cues to help them make foragingdecisions.

INTRODUCTIONIn nature, environments are constantly changing and as a result, organisms arefrequently confronted with novel challenges (Reed et al. 2006). Organisms that canrespond appropriately to these new stimuli will be better able to survive and reproduce.For example: changing climates and seasons can influence available resources such as theripening of fruit or the abundance of seasonal predators. Animals that can identify andlearn what these characteristics mean would be better at survival than the others thatcannot learn the significance of these characteristics.Foraging, the act of gathering food, is a basic activity that takes up much of ananimal’s time. Many animals can use different stimuli to aid them in foraging, but indynamic environments, organisms are constantly exposed to novel or seasonal foodsources. If an organism could not use new stimuli to aid them in survival, then it wouldhave a major disadvantage. This disadvantage would include lack of nutrients; whichwould lead to the animal becoming sluggish and would eventually result in the greaterproblem of starvation. Organisms with a flexible response to these novel stimuli may alsobe more tolerant to environmental change. Being able to change with your environment isa vital process that can save an animal’s time, energy, and even its life.Many animals use vision as their primary sense to find food (Jacobs 2008).Learning how to predict the costs and benefits associated with different visual cues iscrucial for the survival of many animals. Yet a variety of organisms do not have thecognitive abilities to learn new visual cues and predict what the consequences of thosecues mean.In our study we are researching how animals react to new stimuli in the context offoraging. We are trying to find out if certain types of primates can distinguish betweentwo new stimuli and react appropriately to the stimuli. This is important because in thewild, primates eat certain things that are better for them than others, and we want tounderstand how they know to do this.Here, we investigated whether monkeys can learn to use novel visual cues to findfood. We hypothesized that monkeys would be able learn to associate visual cues withpreferred foods. Given the wide variety of food souces used by monkeys and theirrelatively advanced cognitive abilities, we predicted that the monkeys would be able toassociate visual cues with preferred foods. We tested the hypothesis with two species ofmonkey - one New World monkey, the squirrel monkey (Saimiri bolivianesisperuviensis), and one Old World monkey, the crab-eating Macaque (Macacafasicularus). To test whether these monkeys could use visual cues to find food weattempted to train monkeys to learn that preferred food could be found in buckets of aparticular color (red); attached green or red buckets to trees (for Squirrel monkeys) orfences (for Crab-eating Macaques). The red buckets were baited with grapes; while thegreen were empty.METHODSStudy Location - Monkey JungleMonkey Jungle is a commercial zoological park and research center withprimates, birds and a few reptiles. This park is located in southwest Miami Dade, Florida.From June 24 th to July 18 th , 2011, we visited Monkey Jungle every Monday, Wednesday,and Friday (with the exception of holidays). Within this park, there are two large primary

enclosures; the macaque enclosure and the rainforest enclosure. The macaque enclosureis 2.46 hectares and the rainforest consists of 1.45 hectares (Figure 1). All monkeys inthese two large enclosures are a semi-free range. Both enclosures containsubtropical/tropical vegetation such as palms and shrubs. The rain forest enclosure alsohas fruit trees. Most plants within each enclosure are native to Florida. The perimeter ofthese enclosures are surrounded by a 2 m electric fence.Crab-eating macaqueThe crab-eating macaque (Macaca fascicularis), are native to the islands of Java,and other Indonesian islands. This species generally forages below 20 meters, mostly inthe lower canopy, understory and on the ground. They mostly eat fruit, but they also eatstems, leaves, flowers, seeds, grass, mushrooms, insects, arthropods and bird eggs. Whenthey forage in the mangroves they eat crabs, but have also been seen eating frogs andshrimp. They prefer foraging close to small bodies of water and the amount of time theyspend foraging decreases as they move away from the riverbank (Thierry et al. 2004).Crab-eating Macaques have a trichromatic vision. That is, they have three kindsof opsins in their cones, which let them see short, medium, and long wavelengths(roughly corresponding to blues, greens and reds, respectively). One advantage of beingtrichromatic is that the monkeys who eat fruit can determine when the fruit is ripe(Mancuso et al. 2009). Also it helps the monkeys to pick out a food target in a greenvegetation background. This species has a strict dominance hierarchy in which everyindividual knows its rank (Jacobs 2008). There are three main troops in the largemacaque enclosure (John Kuendig Pers. Comm.). Each group has an alpha male whoprotects and leads his troop. In this dominance hierarchy, higher-ranking monkeys andpregnant females have first access to higher quality/preferred food sources (Jack 2007).Squirrel Monkeys:The squirrel monkey (Saimiri bolivianesis peruviensis) is native in central andsouth America. This monkey consumes a wide variety of food such as fruits, insects andsometimes nectar. The squirrel monkeys spends most of their day traveling and foragingon the trees in large groups. Squirrel monkeys vision is unique in that some individualshave trichromatic vision while other have dichromatic vision. Research suggests that asingle locus on the X chromosome controls the number of opsins. As a result of femaleshaving two X chromosomes, they can either be dichromatic or trichomatic depending onthe alleles at this locus, while all males are dichromatic, a condition that is similar tocolor-blindness in humans (Jacobs 2008).Experimental Protocol:The Crab-eating Macaques and squirrel monkeys were presented with bucketscontaining food. We used 12 buckets that were divided into six stations. Each stationconsisted of one bucket that was covered in red construction paper and one bucket thatwas covered in green construction paper. The construction paper was attached to thebuckets using clear packing tape; this assisted with keeping the buckets water resistantand protected it from the monkeys being able to rip off the paper. The buckets used forcrab-eating macaques measured 156.5 cm deep with a 15.5 cm opening. While thebuckets used for the squirrel monkeys measured 11 cm wide and 11.5com deep.

To test whether monkeys could learn to associate the colors on these buckets withfood sources, we first performed a learning period with open buckets (no tops coveringthe buckets), such that monkeys that approached each bucket could look inside and seewhat food source was in it. This open bucket period lasted three trails – June 24 th ,June27 th and June 29 th , and was meant to teach the monkeys that their preferred food was inthe red and not the green bucket.We filled the red buckets with grapes (20 grapes for macaques and 15 for squirrelmonkeys) and green buckets with monkey biscuits (20 biscuits for macaques and 15 forsquirrel monkeys). We put two small holes in the back wall of each bucket in order toattach zip ties so that we could attach the buckets to the fence of the macaque enclosureor tree branches in the squirrel monkey enclosure. Our trials were conducted at the southperimeter of the property for the crab eating macaques, near the kitchen; these bucketswere attached directly to the inside of the fence. Each station was no less than threemeters apart and the red and green buckets at each station were placed one and halfmeters from one another. In contrast, the squirrel monkey trials were conducted in therainforest canopy area of monkey jungle. Each station was a distinct location on trees noless than three meters apart. The buckets at each station were tied directly to treebranches or trunks. We prevented any monkeys trying to investigate the buckets until allstations were ready to begin.Once all the buckets were in place, the timekeeper announced the time and webegan recording data. We record the order the monkeys approach the buckets at eachstation. This data was recorded for a total of five minutes at 30-second intervals.Recording data this way allowed us to determine not only the total number of monkeysthat visited each bucket, but also the order in which they approached each bucket (iewhich bucket did they approach first?). When the five minutes were complete, wegathered the buckets and counted how many pieces of food were left. We then recordedthe data on to the timekeeper’s master sheet.After the third trial date (June 29 th ) we closed the tops of each bucket so thatmonkeys could no longer see inside. Each top had a small hole, big enough for a monkeyto put its hand into, but covered with a flap of duct tap that prevented the monkeys fromseeing inside. In the green buckets we took out the biscuits so that the monkeys wouldlearn that food could only be found in the red buckets. We continued our trials with bothspecies of monkeys, following the data collection protocols for the open-bucket trails(explained above). The Crab-eating Macaques learned immediately that they had to puttheir hands into the opening of the buckets. The squirrel monkeys, on the other hand, hadtrouble learning that they had to put their hands in the opening. We thus had todemonstrate to the squirrel monkeys that they had to put their hands into the bucket.Eventually all squirrel monkeys learned how to get food out of the covered buckets. Werecorded data with these closed buckets for four more trials for each monkey species.On the last day of the experiment we switched the food, putting the grapes in thegreen buckets, yet having nothing in the red buckets. We used a χ 2 to test whether bucketcolor effectively predicted which bucket at each station was visited first and whichbucket color had more visits during each trial.All statistical procedures were performed in the program JMP 9.0 (SAS).

RESULTS:Crab Eating MacaquesOn the first day of the trials, before theclosed bucket-training period, there was nodifference in the color of the bucket that wasvisited first. On the second trial, more Crab-Eating Macaques visited the red bucket withthe grapes first, yet this difference was notstatistically significant. On the third trial, thered bucket was visited first at all stationssignificantly more than green-buckets. On thefourth trial we began the closed-buckettraining period and with the exception of thefirst closed bucket trial Crab-eating Macaquesfirst visited the red buckets at each stationsignificantly more than the green buckets. Onthe day of the experimental trial, when thegrapes were placed in the green bucket, therewas no significant difference in which wascolored bucket was visited first (Figure 2a, seeTable 1a for trial period and statistics).During the open-bucket trials, the Crab-eating macaques visited the open greenbuckets with the commercial monkey biscuits more frequently than the red buckets withthe grapes for trials 1- 3. However, only trial one showed that the total number ofmonkeys visiting each bucket was greater for green buckets than the red buckets (Figure3b). Once buckets were closed so that the macaques could not see the contents of thebucket and the biscuits were removed from the greenbuckets (trials 4-7), the total number of monkeysvisiting the red buckets was significantly greater thanthe total number of monkeys visiting the greenbuckets. However, on the last day of the experiment,when we switched the grapes from the red bucket tothe green bucket, the total number of monkeysvisiting the green buckets was significantly greaterthan the total number of monkeys visiting the redbuckets (Figure 2b and see Table 2a for trial period,and statistics).Results for the Squirrel MonkeyWith the exception of the first day of theexperiment (Trial 2-7), the squirrel monkeys visitedthe red buckets at each station first significantly morethan the green buckets (Figure 3a, Table 2a).However, when grapes were switched into the greenbuckets, monkeys did not visit red buckets first morethan green buckets (Figure 2a). The total number of monkeys visiting red buckets was

significantly greater for all trails except the last trial, when grapes were switched fromred to green buckets. On this day, squirrel monkeys visited the green bucketssignificantly more than the red buckets (Figure b see Table 2a &b for trial period andstatistics).DISCUSSIONIn dynamic environments, where, for example, food sources change seasonally,natural selection should favor the ability for organisms to learn to use novel cues to helpthem respond appropriately to their changing environment. For many organisms, vision isthe primary sense they use interpret their environment. In this experiment we tested ifcrab eating macaques and squirrel monkeys can learn to use visual cues to help them findfood. We tested this hypothesis by attempting to train monkeys to learn to find food incolored buckets. Our results suggest that both crab-eating macaques can learn to associatevisual cues with preferred food. Here, we will discuss the results of the crab eatingmacaques and squirrel monkeys separately.Macaques quickly learned how to associate visual cues with finding food. Onthe first day of the experimental trial the monkeys showed no difference between the twobuckets. By the third day the monkeys initially visited more red buckets because theylearned that there preferred food was in the red bucket. After that experiment we closedthe buckets and showed again no significant difference. Two and three days later theyonce again learned that their preferred food was again in the red buckets. Previousresearch suggests that Macaques use a handful of cue to help them forage. For example,one study found that Crab-eating Macaques not only used known landmarks to find food,but also search for food where they see other Macaques searching (Menzel et al. 1996).Despite the fact that the Macaques prefer grapes to monkey biscuits, during theopen-bucket trails, the total number of monkeys visiting green buckets with these biscuitswas greater than the total number of monkeys visiting the red buckets with grapes (theirpreferred food). Yet, as soon as the buckets were closed monkeys visited the red bucketsfirst at each station and more monkeys visited the red buckets. We suggest that thisfinding is a result of the strict dominance hierarchy of the crab-eating macaques. We notethat the first individuals to visit buckets were usually higher ranking adult males andpregnant females. These monkeys would often stay near the bucket and feed untilsatiated. As a result, younger, lower ranking monkeys (the majority of the macaques)were excluded from the preferred foods and were forced to visit the green buckets. Whilewe didn’t collect data on which individuals were at each bucket we strongly believe thatthis is the explanation for more monkeys visiting the green buckets during the openbuckettrials. Especially since after the first two trials the buckets that were firstapproached at each station were red significantly more than green.Squirrel MonkeyThe squirrel monkeys appeared to learn where the grapes were even faster than themacaques. After our first day experimenting with squirrel monkeys, the squirrel monkeysbegan to first approach the red buckets, which contained red grapes (figure 2a),significantly more than the green buckets, which contained commercial monkey chow(Figure 2a). Additionally, the total number of squirrel monkeys visiting red buckets wasgreater than visits to the green buckets in every trial except the last trial, when the grapes

were in the green buckets.Squirrel monkeys are known to use a variety of information when makingforaging decisions. Vision and is most likely the most important sensory cue for them tosearch for food. Spatial memory is known to be a major factor influencing foragingdecisions in the Tuft capuchin monkeys, Cebus apella (Pauknre et al. 2009). Whilespatial memory most likely also plays a role in squirrel monkeys, we eliminated thispossibility by switching the locations of the red and green buckets each trial.One factor that may influence foraging behavior of squirrel monkeys in natureand this experiment is the acoustic information in the monkey’s vocalizations. Squirrelmonkeys are known to make a lot of chatter while foraging. It has been hypothesized thatthis monkey chatter may communicate the location of food sources, therefore allowingthe group to forage together more effectively (Boinski, C L Mitchell 1997). During ourexperiment we heard a great deal of monkey chatter and we suggest that this may be amajor factor influencing our result. Of particular interest is the result that when we switchthe food sources the squirrel monkeys did not still visit the red buckets at each stationfirst more than the green buckets. Perhaps, the first monkeys arriving at each stationrecognized there were no grapes in the red buckets and communicated this to other groupmembers acoustically. Unfortunately, we did not collect data on the order in whichmonkeys first visited buckets at each station. We only know which bucket they chosefirst at each station. Another possibility is that the monkeys used olfactory cues to findthe grapes. However, this is unlikely give the fact that on the first day of the experiment,there was no difference between which colored bucket monkeys first visited at eachstation.Given the difference in color vision between the two species we studied, we hadinitially expected squirrel monkeys to be outperformed by the macaques. As mentionedabove, all males and some female squirrel monkeys are dichromatic, making them redgreencolorblind (Jacobs and Neitz 1987); while the macaques are trichromatic (Mancusoet al. 2009). Contrary to this difference, the squirrel monkeys did seem to distinguishbetween he red and green buckets and they appeared to out perform the macaques in theirability to learn to that they could find food in the red bucket.In conclusion, both crab-eating macaques and squirrel monkeys seem to learn touse visual cues to help them make foraging decisions. However, it seems that they mayuse other cues, including intraspecific communication to help them forage. Future workshould focus on how within group communication and learning by example influenceforaging decisions in both of these species.

LITERATURE CITEDBoinski, S., Mitchell, C.L., 1997. Chuck Vocalizations of Wild Female Squirrel Monkeys(Saimiri Sciureus) Contatin Information on Caller Identity and Foraging Activity.International Journal of Primatology. 18 (6): 975-993.Jack. 2007. The Cebines. In Primates in Perspective. Edited by Campbell, CJ; Fuentes A,Mackinnon, KC., Panger, M., and Bearder, S.K. Oxford University Press. New York,New York.Jacobs, G.H. 2008. The distribution and nature of color vision among mammals.Biological Reviews. 68, pp. 413-471.Lucas, P.W., Darvell, B.W., Lee, P.K.D, Yuen, T.D.B., Chong, M.F. 1998. Color cues forleaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestionfor the evolution of trichromatic color vision. Folia Primatol. 69: 139-162.Menzel, C.R. 1996. Spontaneous use of matching visual cues during foraging by longtaliedmacaques (Macaca fasicularis). Journal of Comparative Psychology. 110 (4): 370-376.Reed, T.E., Wanless, S., Harris, M.P., Frederiksen, M., Kruuk, L.E.B., Cunningham,E.J.A. 2006. Responding to environmental change: plastic responses vary little in asynchronous breeder. Proc. Biol. Sci. 273 (1602): 2713-2719.Thierry, B., Singh, M., and Kaumanns, W. eds. 2004. Macaque Societies: A model forthe study of social organization. Cambridge University Press, Cambridge.

Figure 1. Areal View of Monkey Jungle. The red line marks the perimeter of the Crab-eatingMacaque’s enclosure while the yellow line represents the perimeter of the rainforest enclosure,where the squirrel monkeys can be found. The transparent red and yellow ovals show where weconducted the experiments on each of these species.

2a.Figure 2. Solid lines connecting squares and diamonds indicate which color was visited most.Dashed line between third and fourth trial represents when we closed the buckets. The dashedrectangle surrounds the results of the experimental trial when we switch grapes from the red togreen bucket. Stars represent differences that are significant at the alpha=0.05 level. (a) TheNumber of Stations in Which Monkeys Chose to Approach Red or Green buckets first. Greensquares represent the number of stations where monkeys first visited green buckets and reddiamonds represent stations where monkeys first visited red buckets. (b) Total Number ofMonkeys Visiting Red vs Green Buckets per Five Minute Trial. Green triangles and red squaresrepresent the total number of monkeys visiting green and red buckets respectively, throughoutevery five-minute trail.2b.

3a.Figure 3. Solid lines connecting squares and diamonds indicate which color was visited most.Dashed line between third and fourth trial represents when we closed the buckets. The dashedrectangle surrounds the results of the experimental trial when we switch grapes from the red togreen bucket. Stars represent differences that are significant at the alpha=0.05 level. (a) TheNumber of Stations in Which Squirrel Monkeys Chose to Approach Red or Green buckets first.Green squares represent the number of stations where monkeys first visited green buckets and reddiamonds represent stations where monkeys first visited red buckets. (b) Total Number ofSquirrel Monkeys Visiting Red vs Green Buckets per Five Minute Trial. Green triangles and redsquares represent the total number of monkeys visiting green and red buckets respectively,throughout every five-minute trail.3b.