Abstract
We review socially biased learning about food and problem solving in monkeys, relying especially on studies with tufted capuchin monkeys (Cebus apella) and callitrichid monkeys. Capuchin monkeys most effectively learn to solve a new problem when they can act jointly with an experienced partner in a socially tolerant setting and when the problem can be solved by direct action on an object or substrate, but they do not learn by imitation. Capuchin monkeys are motivated to eat foods, whether familiar or novel, when they are with others that are eating, regardless of what the others are eating. Thus, social bias in learning about foods is indirect and mediated by facilitation of feeding. In most respects, social biases in learning are similar in capuchins and callitrichids, except that callitrichids provide more specific behavioral cues to others about the availability and palatability of foods. Callitrichids generally are more tolerant toward group members and coordinate their activity in space and time more closely than capuchins do. These characteristics support stronger social biases in learning in callitrichids than in capuchins in some situations. On the other hand, callitrichids’ more limited range of manipulative behaviors, greater neophobia, and greater sensitivity to the risk of predation restricts what these monkeys learn in comparison with capuchins. We suggest that socially biased learning is always the collective outcome of interacting physical, social, and individual factors, and that differences across populations and species in social bias in learning reflect variations in all these dimensions. Progress in understanding socially biased learning in nonhuman species will be aided by the development of appropriately detailed models of the richly interconnected processes affecting learning.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Addessi, E., &Visalberghi, E. (2001). Social facilitation of eating novel foods in tufted capuchins (Cebus apella): Input provided by group members and responses affected in the observer.Animal Cognition,4, 297–303.
Addessi, E., &Visalberghi, E. (2002).Capuchin monkeys (Cebus apella) do not match the food choice performed by a group member. Unpublished manuscript.
Boinski, S., Treves, A., &Chapman, C. (2000). A critical evaluation of the effects of predators on primates: Effects on group travel. In S. Boinski & P. Garber (Eds.),On the move: How and why animals travel in groups (pp. 43–72). Chicago: University of Chicago Press.
Bray, D. (2003). Molecular networks: The top-down view.Science,301, 1864–1865.
Buchanan-Smith, H., &Hardie, S. (1997). Tamarin mixed-species groups: An evaluation of a combined captive and field approach.Folia Primatologica,68, 272–286.
Caldwell, C., &Whiten, A. (2003). Scrounging facilitates social learning in marmosets,Callithrix jacchus.Journal of Comparative Psychology,65, 1085–1092.
Camazine, S. (2001).Self-organization in biological systems. Princeton: Princeton University Press.
Cambefort, J. P. (1981). A comparative study of culturally transmitted patterns of feeding habits in the chacma baboonPapio ursinus and the vervet monkeyCercopithecus aethiops.Folia Primatologica,36, 243–263.
Coussi-Korbel, S., &Fragaszy, D. M. (1995). On the relation between social dynamics and social learning.Animal Behaviour,50, 1441–1453.
Custance, D. M., Whiten, A., &Bard, K. A. (1995). Can young chimpanzees (Pan troglodytes) imitate arbitrary actions? Hayes and Hayes (1952) revisited.Behaviour,132, 837–859.
Custance, D. [M.], Whiten, A., &Fredman, T. (1999). Social learning of an artificial fruit task in capuchin monkeys (Cebus apella).Journal of Comparative Psychology,113, 13–23.
Day, R., Coe, R., Kendal, J., &Laland, K. (2003). Neophilia, innovation and social learning: A study of intergeneric differences in callitrichid monkeys.Animal Behaviour,65, 559–571.
de Waal, F. (1997). Food transfers through mesh in brown capuchins.Journal of Comparative Psychology,111, 370–378.
de Waal, F., Luttrell, L., &Canfield, M. (1993). Preliminary data on voluntary food-sharing in brown capuchins.American Journal of Primatology,29, 73–78.
Dietz, J., Peres, C., &Pinder, L. (1997). Foraging ecology and use of space in wild golden lion tamarins.American Journal of Primatology,41, 289–305.
Drapier, M., Addessi, E., &Visalberghi, E. (2003). Response ofCebus apella to foods flavored with familiar or novel odor.International Journal of Primatology,24, 295–315.
Elman, J. L., Bates, E. A., Johnson, M. H., Karmiloff-Smith, A., Parisi, D., &Plunkett, K. (1996).Rethinking innateness. Cambridge, MA: MIT Press.
Feistner, A., &McGrew, W. C. (1989). Food sharing in lion tamarins: Tests of three hypotheses.American Journal of Primatology,31, 211–221.
Ferrari, P.F., Gallese, V., Rizzolatti, G., &Fogassi, L. (2003). Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex.European Journal of Neuroscience,17, 1703–1714.
Fewell, J. (2003). Social insect networks.Science,301, 1867–1870.
Fragaszy, D. M., &Adams-Curtis, L. (1990). Challenge in captivity. In H. Box (Ed.),Primate responses to environmental change (pp. 239–264). London: Chapman & Hall.
Fragaszy, D. M.,Deputte, B. L.,Hemery, C., &Johnson, M. H. (1998).Human-reared capuchins match familiar but not novel actions. Unpublished manuscript.
Fragaszy, D.M., Feuerstein, J.M., &Mitra, D. (1997). Transfers of food from adults to infants in tufted capuchins (Cebus apella).Journal of Comparative Psychology,111, 194–200.
Fragaszy, D. M.,Landau, K., &Leighty, K. (2001).Inducing traditions in capuchin monkeys, Part I. Unpublished raw data.
Fragaszy, D. M., Landau, K., &Leighty, K. (2002). Inducing traditions in captive capuchins: Part I. InCaring for primates. Abstracts of the XIX Congress of the International Primatological Society (pp. 317–318). Bei**g: Mammalogical Society of China.
Fragaszy, D. M., &Visalberghi, E. (1989). Social influences on the acquisition and use of tools in tufted capuchin monkeys (Cebus apella).Journal of Comparative Psychology,103, 159–170.
Fragaszy, D. M., &Visalberghi, E. (2001). Recognizing a swan: Socially-biased learning.Psychologia,44, 82–98.
Fragaszy, D. M., Visalberghi, E., &Fedigan, L. M. (2004).The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.
Fragaszy, D. M., Visalberghi, E., &Galloway, A. (1997). Infant tufted capuchin monkeys’ behaviour with novel foods: Opportunism, not selectivity.Animal Behaviour,53, 1337–1343.
Fragaszy, D.M., Vitale, A. F., &Ritchie, B. (1994). Variation among juvenile capuchins in social influences on exploration.American Journal of Primatology,32, 249–260.
Gallese, V., Fadiga, L., Fogassi, L., &Rizzolatti, G. (1996). Action recognition in the premotor cortex.Brain,119, 593–609.
Galloway, A. (1998).Social inducement of feeding and food preferences in pair-housed capuchin monkeys, Cebus apella. Unpublished doctoral dissertation, University of Georgia.
Goodall, J. (1964). Tool using and aimed throwing in a community of chimpanzees.Nature,201, 1264–1266.
Hardie, S., &Buchanan-Smith, H. (2000). Responses of captive single- and mixed-species groups of Saguinus to novel nonthreatening objects.International Journal of Primatology,21, 629–648.
Hayes, K., &Hayes, C. (1952). Imitation in a home-reared chimpanzee.Journal of Comparative & Physiological Psychology,45, 450–459.
Hemelrijk, C. (2002). Understanding social behaviour with the help of complexity science.Ethology,108, 655–671.
Hemery, C., Fragaszy, D. M., &Deputte, B. [L.] (1998). Humansocialized capuchins match objects but not actions.Congress of the International Primatological Society: Abstracts,17, 45.
Herv., N., &Deputte, B. L. (1993). Social influence in manipulations of a capuchin monkey raised in a human environment: A preliminary case study.Primates,34, 227–232.
Hikami, K. (1991). Social transmission of learning in Japanese monkeys (Macaca fuscata). In A. Ehara, T. Kimura, O. Takemaka, & M. Iwamoto (Eds.),Primatology Today (pp. 343–344). Amsterdam: Elsevier.
Hirata, S., Watanabe, K., &Kawai, M. (2001). “Sweet-potato washing” revisited. In T. Matsuzawa (Ed.),Primate origins of human cognition and behavior (pp. 487–509). Tokyo: Springer-Verlag.
Huffman, M. (1996). Acquisition of innovative cultural behaviors in nonhuman primates: A case study of stone handling, a socially transmitted behavior in Japanese macaques. In C. Heyes & B. Galef (Eds.),Animal social learning: The roots of culture (pp. 267–289). New York: Academic Press.
Huffman, M., &Hirata, S. (2003). Biological and ecological foundations of primate behavioral tradition. In D. Fragaszy & S. Perry (Eds.),The biology of traditions: Models and evidence (pp. 267–296). Cambridge: Cambridge University Press.
Itani, J., &Nishimura, A. (1973). The study of infrahuman culture in Japan. In E.W. Menzel, Jr. (Ed.),Symposia of the Fourth International Congress of Primatology: Vol. 1 (pp. 20–26). Basel: Karger.
Jasny, B., &Ray, L. (2003). Life and the art of networks.Science,301, 1863.
Kamil, A. (1998). On the proper definition of cognitive ethology. In R. Balda, I. Pepperberg, & A. Kamil (Eds.),Animal cognition in nature (pp. 1–28). New York: Academic Press.
Kawai, M. (1965). Newly-acquired pre-cultural behavior of a natural troop of Japanese monkeys on Koshima Island.Primates,6, 1–30.
Kawamura, S. (1965). Sub-culture among Japanese macaques. In S. Kawamura & J. Itani (Eds.),Monkeys and apes: Sociological studies (pp. 237–289). Tokyo: Chuokoronsha.
Klopfer, P.H. (1961). Observation learning in birds: The establishment of behavioral modes.Behaviour,17, 71–80.
Kummer, H., &Goodall, J. (1985). Conditions of innovative behaviour in primates.Philosophical Transactions of the Royal Society of London: Series B,308, 203–214.
Laland, K., &Kendal, J. (2003). What the models tell us about social learning. In D. Fragaszy & S. Perry (Eds.),The biology of traditions: Models and evidence (pp. 33–55). Cambridge: Cambridge University Press.
Lefebvre, L. (2000). Feeding innovations and their cultural transmission in bird populations. In C. Heyes & L. Huber (Eds.),The evolution of cognition (pp. 311–328). Cambridge, MA: MIT Press.
Lepoivre, H., &Pallaud, B. (1985). Social facilitation in a troop of guinea baboons (Papio papio) living in an enclosure.Behavioural Processes,11, 405–418.
McGrew, W. C. (1974). Tool use by wild chimpanzees in feeding upon driver ants.Journal of Human Evolution,3, 501–508.
McGrew, W. C., &Tutin, C. (1973). Chimpanzee tool use in dental grooming.Nature,241, 477–478.
Mineka, S., &Cook, M. (1988). Social learning and acquisition of snake fear responses in monkeys. In T. R. Zentall & B. G. Galef (Eds.),Social learning: Psychological and biological perspectives (pp. 51–73). Hillsdale, NJ: Erlbaum.
Myowa-Yamakoshi, M., &Matsuzawa, T. (1999). Factors influencing imitation of manipulatory actions in chimpanzees (Pan troglodytes).Journal of Comparative Psychology,113, 128–136.
Myowa-Yamakoshi, M., &Matsuzawa, T. (2000). Imitation of intentional manipulatory actions in chimpanzees.Journal of Comparative Psychology,114, 381–391.
Prescott, M., &Buchanan-Smith, H. (1999). Intra- and inter-species social learning of a novel food task in two species of tamarins.International Journal of Comparative Psychology,12, 71–92.
Price, E., &Feistner, A. (1993). Food sharing in lion tamarins: Tests of three hypotheses.American Journal of Primatology,31, 211–221.
Queyras, A., Scolavino, M., Puopolo, M., &Vitale, A. (2000). Social influence on induced food preference in common marmosets (Callithrix jacchus).Folia Primatologica,71, 367–374.
Rapaport, L. (1999). Provisioning of young in golden lion tamarins (Callitrichidae,Leontopithecus rosalia): A test of the information hypothesis.Ethology,105, 619–636.
Rapaport, L., &Ruiz-Miranda, C. (2002). Tutoring in wild golden lion tamarins.International Journal of Primatology,23, 1063–1070.
Rizzolatti, G., Fadiga, L., Gallese, V., &Fogassi, L. (1996). Premotor cortex and the recognition of motor actions.Cognitive Brain Research,3, 131–141.
Rylands, A. (1993).Marmosets and tamarins: Systematics, behaviour, and ecology. Oxford: Oxford University Press.
Snowdon, C., &Boe, C. (2003). Social communication about unpalatable foods in tamarins (Saguinus oedipus).Journal of Comparative Psychology,117, 142–148.
Tomasello, M., Kruger, A. C., &Ratner, H. H. (1993). Cultural learning.Behavioral & Brain Sciences,16, 495–552.
Visalberghi, E. (1990). Tool use in capuchin monkeys.Folia Primatologica,54, 146–154.
Visalberghi, E. (1993). Capuchin monkeys: A window into tool use in apes and humans. In K. Gibson & T. Ingold (Eds.),Tools, language, and cognition in human evolution (pp. 138–150). Cambridge: Cambridge University Press.
Visalberghi, E., &Addessi, E. (2000a). Response to changes in food palatability in tufted capuchin monkeys,Cebus apella.Animal Behaviour,59, 231–238.
Visalberghi, E., &Addessi, E. (2000b). Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys.Animal Behaviour,60, 69–76.
Visalberghi, E., &Addessi, E. (2001). Acceptance of novel foods in capuchin monkeys: Do specific social facilitation and visual stimulus enhancement play a role?Animal Behaviour,62, 567–576.
Visalberghi, E., &Fragaszy, D. M. (1990a). Do monkeys ape? In S. T. Parker & K. R. G. Gibson (Eds.),“Language” and intelligence in monkeys and apes (pp. 247–273). Cambridge: Cambridge University Press.
Visalberghi, E., &Fragaszy, D. M. (1990b). Food-washing behaviour in tufted capuchin monkeys (Cebus apella) and crabeating macaques,Macaca fascicularis.Animal Behaviour,40, 829–836.
Visalberghi, E., &Fragaszy, D. [M.] (1995). The behaviour of capuchin monkeys,Cebus apella, with novel food: The role of social context.Animal Behaviour,49, 1089–1095.
Visalberghi, E., &Fragaszy, D. [M.] (2002). Do monkeys ape? Ten years later. In K. Dautenhahn & C. Nehaniv (Eds.),Imitation in animals and artifacts (pp. 471–479). Cambridge, MA: MIT Press.
Visalberghi, E., Janson, C. H., &Agostini, I. (2003). Response toward novel foods and novel objects in wildCebus apella.International Journal of Primatology,24, 653–675.
Visalberghi, E., Valente, M., &Fragaszy, D. [M.] (1998). Social context and consumption of unfamiliar foods by capuchin monkeys (Cebus apella) over repeated encounters.American Journal of Primatology,45, 367–380.
Voelkl, B., &Huber, L. (2000). True imitation in marmosets.Animal Behaviour,60, 195–202.
Warden, C. J., Fjeld, H. A., &Koch, A. M. (1940). Imitative behavior in cebus and rhesus monkeys.Journal of Genetic Psychology,56, 311–322.
Watanabe, K. (1994). Precultural behavior of Japanese macaques: Longitudinal studies of the Koshima troops. In R. A. Gardner, A. B. Chiarelli, B. T. Gardner, & F. X. Plooij (Eds.),The ethnological roots of culture (pp. 81–94). Dordrecht: Kluwer Academic.
West, M., King, A., &White, D. (2003). Discovering culture in birds: The role of learning and development. In F. de Waal & P. Tyack (Eds.),Animal social complexity (pp. 470–492). Cambridge, MA: Harvard University Press.
Westergaard, G. C., &Fragaszy, D. M. (1985). Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella).Zoo Biology,4, 317–327.
Westergaard, G. C., &Fragaszy, D.M. (1987). The manufacture and use of tools by capuchin monkeys (Cebus apella).Journal of Comparative Psychology,101, 159–168.
Zentall, T., &Galef, B. G. (1988).Social learning: Psychological and biological perspectives. Hillsdale, NJ: Erlbaum.
Zuberbühler, K., Gygax, L., Harley, N., &Kummer, H. (1996). Stimulus enhancement and spread of a spontaneous tool use in a colony of long-tailed macaques.Primates,37, 1–12.
Author information
Authors and Affiliations
Corresponding author
Additional information
We acknowledge financial support by a grant from the FIRB/MIUR to E.V., by the Leakey Foundation and the National Science Foundation to D.F., and by NIH Grant HD63016 to Georgia State University. Thanks to Elsa Addessi, Domenico Parisi, Rosaria Conte, Jeff Galef, Celia Heyes, and several anonymous reviewers for commenting on an earlier draft of this manuscript.
Rights and permissions
About this article
Cite this article
Fragaszy, D., Visalberghi, E. Socially biased learning in monkeys. Animal Learning & Behavior 32, 24–35 (2004). https://doi.org/10.3758/BF03196004
Issue Date:
DOI: https://doi.org/10.3758/BF03196004