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Koska, Jennifer, E.
Hbitos de forrajeo y el aprendizaje social de los monos cara blanca (Cebus capucinus)
Foraging habits and social learning of white-faced capuchin monkeys (Cebus capucinus)
Foraging for food is an essential aspect to the life of Cebus capucinus. The transmission of this knowledge takes many months of careful observations and trial and error. I studied the foraging habits of C. capucinus in the Cloud Rainforest. It was predicted that there would be a difference between adults and juveniles. My data suggests that there is no difference in the foraging habits between adults and juveniles. These results suggest social learning during the juvenile phase of life impacts the foraging behavior of the C. capucinus.
El forrajeo en busca de alimento es un factor esencial en la vida de Cebus capucinus. La transmisin de este conocimiento toma varios meses de cuidadosa observacin, prueba y error. Estudi los hbitos de forrajeo de C. capucinus en la reserva del bosque nuboso. Predije que habra una diferencia entre los adultos y los juveniles. Mis datos sugieren que no existe diferencia en los hbitos de forrajeo entre los adultos y los juveniles. Estos resultados sugieren un aprendizaje social durante la fase juvenil que impacta el comportamiento de forrajeo de C. capucinus.
Text in English.
Costa Rica--Puntarenas--Monteverde Zone
Alimentos de animales
Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology Spring 2010
Ecologa Tropical Primavera 2010
t Monteverde Institute : Tropical Ecology
Foraging habits and social learning of white faced capuchin monkeys ( Cebus capucinus ). Jennifer E. Koska Department of Environmental Science and Policy, Drake University ABSTRACT Foraging for food is an essential aspect to the life of Cebus capucinus The transmission of this knowledge takes many months of careful observations and trial and error. I studied the foraging habits of C. cap ucinus in the Cloud Rainforest. It was predicted that there would be a difference between adults and juveniles. My data suggests that there is no difference in the foraging habits between adults and juveniles. These results suggest social learning during the juvenile phase of life impacts the foraging behavior of the C. c apucinus RESUMEN El forrajeo en busca de alimento es un factor esencial en la vida de Cebus capucinus La transmisin de este conocimiento toma varios meses de cuidadosa observacin y prueba y error. Estudi los hbitos de forrajeo de C. capucinus en la reserva del bosque nuboso. Predije que habra una diferencia entre los adultos y juveniles. Mis datos sugieren que no existe diferencia en los hbitos de forrajeo entre adultos y juveniles. Estos resultados sugieren un aprendizaje social durante la fase juvenil que impacta el comportamiento de forrajeo de C. capucinus INTRODUCTION Social learning is a major part of the development in every social animal. It is important for learning successful foraging techniques. There are four main categories of social learning, each category requiring more cognitive development to perform. Stimulus enhancement is the primitive most simplistic type of social learning. During this, subject A orients subject B towards the behavior and subject B completes it (Whitman, 2000, and Nobel et al., 2001). The s econd form of social learning is observational conditioning. This is when a behavior is learned from direct observation of another subject (Whitman 2000) For example of the same objec t. The third form of social learning is imitation. Imitation is when B same result (Whiten 2000 and Wohlschlager et al. 2003). The fourth and most cognitively devel oped form of social learning is emulation. During emulation, subject B without copying the same actions as subject A (Whitman, 2000, Rivkin, 2001). Observational learnin g is seen when attempting to learn what foods are not harmful for the individual to consume In baboons t he primate will pick up food and if the taste is not pleasant will dispose of it. This process will continue until they associate a taste with a foo d item ( Jouventin 1976 ) Imitation has been well documented in
Orangutans ( Fox et al. 1999 ) The fruit genus Neesia (Family) has glass like fibers that irritate the skin if touched. The orangutans have learned to use a stick with their mouth to extract the protein rich seeds into their hands ( Fox et al. 1999) Observations show that infants will watch their parents and attempt to imitate the same skill Fox et al 1999) The Orangutan that was observing would then leave the sight and imitate the same st eps with a similar tool to forage in the same matter (Fox et al 1999). New world monkeys are behaviorally diverse but include many species that live in complex group social systems ( Fragaszy and Bard 1996 ). Social groups often pass foraging skill s vertically (mom baby) or horizontally (within a generation must be one or bot h ) through social learning ( Garber and Paciulli 1997 ) Juvenile w hite f aced c apuchin ( Cebus capucinus ) have a prolonged dependency stage of 12 months where they le arn foraging skills as their mother weans them ( Fragaszy and Bard 1996 ) Juvenile C. capuchinus demonstrate social learning in the form of imitation (Ottoni and Mannu 2000). Nut cracking is a skill that includes the use of two stones: one used as a anvi l and the other used as a gavil. The C. capucinus will hammer the nut until the shell breaks and they can consume the nut within (Ottoni and Mannu, 2000). They have also been observed to perform observational conditioning when foraging (Glader 1982). The weaning age coincides with the time the molars erupt and allow the monkey to process hard seeds and nutshells (Fragaszy & Adams Curtis 1997). Because of the natural history of C. c apucinus I believe that Juveniles will have different foraging habits then the adults in the troop. The age that their pr emolars erupt indicate that they might not be able to forage for the same materials (Fragaszy and Adams Curtis, 1997) In addition, dominate males in the troop do not allow the juveniles feed on th e as regularly and consume more on average ( Janson 1985). Their long juvenile stage shows also that social learning takes a while to be established in the Cebus geunus. Since social learning is how foraging methods passed down to offspring, the foraging habits might not be completely taught to the juvenile C. capucinus METHODS Study Subject C. c apucinus are a new world monkey species with a average lifespan of 36 years The young then have a prolonged juvenile stage. The young spend an average of 3% of there life with their mother post weaning (Fragasz y and Bard 1996). Study Site Data was collected from a 2.5 km transect in Monteverde, Puntarenas, Costa Rica at 1400 meters above sea level in the premontane moist life zone (Holdridge 1966 ). The transect bisected the Park Bajo del Tigre and the n bisected the Finca Ecologia. Part of t he forest in Bajo del tigre was in a state of secondary growth recovering from an old guava plantation Halfway down the transect in Bajo del Tigre the forest turned into primary forest It then switched back to a regenerating secondary growth forest when entering the Finca Ecologica Procedure T he transect was walked every other day starting April 5 and continuing through April 26. The total number of encounters w ere r ecorded If a troop was located,
I recor ded individual behavior for two minutes. First, I determined whether the individual was an adult or a juvenile Then, I recorded the frequency of four behaviors related to foraging (Table 1). After two minutes, I would switch to another individuals. Table 1 : Ethogram for foraging behaviors observed during the sampling period for both adults and juveniles. Category Definition Foraging Leaves Tear, eat, and manipulate leaves for the insects residing in or on the leaves or eating the leaves themselves. Forag ing Bark Break branches or bark off the tree to eat the insects residing in or on the bark Foraging Fruit Harvest fruit off the tree to eat it Foraging Insects Pick insects off of a plant in order to eat them RESULTS During nine walks, totaling a dis tance of 22.5 km and 16.43 h of search time, C. capuchinus were encountered three times (overall encounter rates 0.133 monkey troops/km and 0.18 troop encounters/hr) (Table 2) Table 2 Sampling attempts and Cebus c apucinus during transect walking in M onteverde, Costa Rica Site Number of walks Total Distance (km) Total time (h) Number of troop encounters Monkey troops per km Monkey troop encounters per hour Bajo Del Tigre to Ccological Farm 9 22.5 16.43 3 0.133 0.18 J uvenile s did not forage more tha n the adult s in leaves (t stat= 0.159, 69 df, P>0.5 ), in bark (t stat=0.314, 69 df, P>0.5 ), on fruit (t stat=0.892, 69 df, P>0.5 ) or on seeds (t stat=0.196, 69 df, P>0.5 ) (Fig. 1)
Figure 1: mean frequencies of foraging in bark ( 1 SD), for fruit ( 1 SD), in lea ve s ( 1 SD), and for insects ( 1 SD) for juvenile and adult C. c apucinus n= 71 ), DISCUSSION Social learning in Cebus. spp is just recently being fully understood in the primate world. The rate at which social learning in foraging is tr ansferred can be understood by studying the frequencies at which that activity occurs and seeing how it changes as the infant or juvenile advances in age. The frequencies of foraging for all food sources did not differ between adults and juveniles. Cebus spp behavior (Ottoni and Mannu 2000). The extended period of time that the juveniles spend with their mother and original troop is important for vertically transmitting the correct foragin g habits to their offspring. T he speed of horizontal behavioral transmission and the amount of time an infant spends with its mother may help explain the result that there is no difference in the diets of the C. capucinus During the time spent with thei r mother the i nfants and juveniles show a heightened interest in other food choices (Visalberghi and Fragaszy 1994). In addition, they are tolerated when the y take food out of hands of adults in the troop (Mitra et al 1993 Ottoni and Mannu 2000 ). The tolerance helps expedite the process of social learning (Ottoni Mannu 2000). This inspection helps the juvenile monkey learn which foods choices are rewards for the foraging behavior and are deemed acceptable by the adult When a juvenile s ees the reward they are more likely to imitate the behavior to receive the same reward. Infant and adult Cebus spp. are less likely to try new food choices when they are by themselves, instead they will wait to be foraging with another to try a new food source (Visalberghi and Fragaszy 1994). This refusal to try new foods without a partner makes it less likely for one individual to have different foraging habits then the rest of the troop. This supports the findings in my study. The juveniles and adult s forage for the same food
sources. The established foraging habit is a behavior that is passed on through generations (Perry et al. 2003 ). ACKNOWLEDGMENTS I would like to thank Anjali Kumar for her guidance and patience during this project. Thanks to the Finca Ecological and Bajo del Tigre for the use of their facilities. Special thanks to Vin for his path guidance and understanding while finding the transect path. I would especially like to thanks all members of the Spring 2010 CIEE cours e for their encouragement during the semester. LITERATURE CITED Fox, A. F., A. F. Sitompul, C. P. Schaik. 1999. Intelligent tool use in wild Sumatran. The Mentalities of Gorillas and Orangutans: Comparative Perspectives 1: 99 116. Fragaszy, D. M. an d K. Bard. 1996. Comparison of development and life history in Pan and Cebus. International Journal of Primatology 18: 683 701. ----Adams Curtis L. E. 1997. Developmental changes in manipulation in tufted capuchins ( Cebus apella ) from birth through 2 years and their relation to foraging and weaning. Journal of Comparative Psychology 111: 201 211. Garber, P.A. and L.M. Paciulli. 1997. Experimental field study of spatial memory and learning in wild capuchin monkeys ( Cebus Capucinus ). Folia Primato l 68: 236 253. Glander K. E. 1982. The impact of plant secondary compound on primate feeding behavior. American Journal of Physical Anthropology 25: 1 18. Janson, C. 1985. Aggressive behavior and individual food consumption in wild brown capuchin mon keys (Cebus apella). Behavioral Ecology and Sociobiology 18: 125 138. Jouventin, P., G. Pasteur, J. Cambefort. 1976. Observational learning of baboons and avoidance of mimics: exploratory tests. Evolution 31: 214 218. Mitra, D., D. Fragaszy, J. Feue rstein, L. Toll. 1993. Sometimes you feel like a nut: the social context of resource exploitation by juvenile tufted capuchin monkeys (Cebus Apella). American Journal of Primatology 30: 336. Noble, J., P.M. Todd, and T. Elio. 2001. Social learning of food preferences without aversions: an evolutionary model of Norway rats. Biological Sciences 268: 141 149. Ottoni, D. O. and M. Mannu. 2000. Semifree ranging Tufted Capuchin (Cebus apella) spontaneously use tools to crack open nuts. Internationa l Journal of Primatology 22: 347 358. Perry S., M. Baker, L. Fedigan, J. Gos Louis, K. Jack, K. C. MacKinnon, J. H. Manson, M. Panger, K. Pyle, L. Rose. 2003. Social conventions in wild white faced capuchin monkeys: evidence for traditions in the ne otropical primate. Current Anthropology 44: 241 268. Rivkin, J. W. Reproducing knowledge: replication without imitation at moderate complexity. Organization Science 12: 274 293.
Visalberghi E., and D. Fragaszy. The behavior of capuchin monkeys, Ceb us apella, with novel food: the role of social context. Animal Behavior 29: 1089 1095. Whiten, A. 2000. Primate culture and social learning. Cognitive Science 24: 477 508. Wohlschlager A., M. Gattis, and H. Bekkering. 2003. Action generation and a ction perception in imitation an instance of the ideomotor principle. Philosophical Transactions: Biological Sciences 358: 501 515. Vogal, R. E. Rank differences in energy intake in white faced capuchin monkeys (Cebus capucinus). Behavior Ecology and Sociobiology 58: 333 344.