Social influences on foraging behavior in young nonhuman primates: Learning what, where, and how to eat

Human infants rely on social interactions to acquire food‐related information. 1 , 2 Adults actively teach children about food through culturally diverse feeding practices. Characteristics we share with the other primates, such as complex diets, highly social lives, and extended juvenile periods, suggest that social learning may be important during ontogeny throughout the order. Although all young primates typically pay attention to feeding adults, great apes and callitrichids, in particular, acquire new foraging techniques through abilities unknown in other nonhuman primates; that is, they learn by imitation. However, ape social learning is almost exclusively infant‐initiated, while adult callitrichids actively teach their young. It is unlikely that the same selective forces have acted to favor sophisticated social‐learning mechanisms in both taxa. 3 , 4 Equipped with an ape brain, complex foraging methods, and a cooperative infant‐care system, early hominins were uniquely poised to take social learning about food and foraging techniques to a new level.

[1]  A. Thornton,et al.  Teaching in Wild Meerkats , 2006, Science.

[2]  Dorothy M. Fragaszy,et al.  CHAPTER 4 – Social Learning in Monkeys: Primate “Primacy” Reconsidered , 1996 .

[3]  Tetsuro Matsuzawa,et al.  Primate Origins of Human Cognition and Behavior , 2001, Springer Japan.

[4]  T. Nishida,et al.  Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park, Tanzania , 1996, International Journal of Primatology.

[5]  S. Hrdy 2. Evolutionary context of human development: the cooperative breeding model , 2005 .

[6]  Christian Rutz,et al.  Development of tool use in New Caledonian crows: inherited action patterns and social influences , 2006, Animal Behaviour.

[7]  Jeanne Altmann,et al.  Baboon mothers and infants , 1980 .

[8]  C. Snowdon,et al.  Developmental changes in food transfers in cotton‐top tamarins (Saguinus oedipus) , 2007, American journal of primatology.

[9]  J. Goodall The Chimpanzees of Gombe: Patterns of Behavior , 1986 .

[10]  F. Wiens,et al.  Social Dependence of Infant Slow Lorises to Learn Diet , 2003, International Journal of Primatology.

[11]  Michael Gurven,et al.  How long does it take to become a proficient hunter? Implications for the evolution of extended development and long life span. , 2006, Journal of human evolution.

[12]  C. Heyes,et al.  SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS , 1994, Biological reviews of the Cambridge Philosophical Society.

[13]  A. Fletcher,et al.  Food transfers in immature wild western lowland gorillas (Gorilla gorilla gorilla) , 2006, Primates.

[14]  Craig B. Stanford,et al.  The Hunting Apes: Meat Eating and the Origins of Human Behavior , 1999 .

[15]  B. Voelkl,et al.  Social contact influences the response of infant marmosets towards novel food , 2006, Animal Behaviour.

[16]  C. Heyes,et al.  Social learning in animals : the roots of culture , 1996 .

[17]  L. Tarnaud Ontogeny of Feeding Behavior of Eulemur fulvus in the Dry Forest of Mayotte , 2004, International Journal of Primatology.

[18]  B. Galef,et al.  CHAPTER 3 – Social Enhancement of Food Preferences in Norway Rats: A Brief Review1 , 1996 .

[19]  A. Keuroghlian,et al.  Foraging behavior and microhabitats used by black lion tamarins, Leontopithecus chrysopygus (Mikan) (Primates, Callitrichidae) , 1999 .

[20]  M. Huck,et al.  The many faces of helping: possible costs and benefits of infant carrying and food transfer in wild moustached tamarins (Saguinus mystax) , 2004 .

[21]  Y. V. Bergen,et al.  Begging, stealing, and offering : food transfer in nonhuman primates , 2004 .

[22]  Gillian R. Brown,et al.  Adult–infant food transfer in common marmosets: an experimental study , 2005, American journal of primatology.

[23]  E. Menzel,et al.  Vocalizations and their behavioral contexts in the tamarin Saguinus fuscicollis. , 1976, Folia primatologica; international journal of primatology.

[24]  P. Izar,et al.  Capuchin monkey tool use: Overview and implications , 2008 .

[25]  A. Ueno Development of co-feeding behavior in young wild Japanese macaques (Macaca fuscata) , 2005 .

[26]  S. Kuroda Interaction over Food among Pygmy Chimpanzees , 1984 .

[27]  E. Visalberghi,et al.  Infant tufted capuchin monkeys’ behaviour with novel foods: opportunism, not selectivity , 1997, Animal Behaviour.

[28]  Elisabetta Visalberghi,et al.  Specific social influences on the acceptance of novel foods in 2–5-year-old children , 2005, Appetite.

[29]  L. Rapaport Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young , 2006 .

[30]  J. French,et al.  The reproductive status of nonbreeding group members in captive golden lion tamarin social groups , 1989, American journal of primatology.

[31]  T. Zentall CHAPTER 11 – An Analysis of Imitative Learning in Animals , 1996 .

[32]  R. Byrne,et al.  THE ONTOGENY OF MANUAL SKILL IN WILD CHIMPANZEES: EVIDENCE FROM FEEDING ON THE FRUIT OF SABA FLORIDA , 2002 .

[33]  C. Boesch Teaching among wild chimpanzees , 1991, Animal Behaviour.

[34]  S. Uehara,et al.  Local Differences in plant-feeding Habits of chimpanzees between the Mahale Mountains and Gombe National Park, Tanzania , 1983 .

[35]  B. Voelkl,et al.  True imitation in marmosets , 2000, Animal Behaviour.

[36]  L. R. Moscovice,et al.  The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus , 2006, Animal Behaviour.

[37]  R. Byrne Imitation of novel complex actions: What does the evidence from animals mean? , 2002 .

[38]  E. Starin Food transfer by wild titi monkeys (Callicebus torquatus torquatus). , 1978, Folia primatologica; international journal of primatology.

[39]  C. Ruiz-Miranda,et al.  Ontogeny of provisioning in two populations of wild golden lion tamarins (Leontopithecus rosalia) , 2006, Behavioral Ecology and Sociobiology.

[40]  E. Fernández‐Duque,et al.  Food transfers to young and mates in wild owl monkeys (Aotus azarai) , 2008, American journal of primatology.

[41]  B. Smuts Sex and friendship in baboons , 1987 .

[42]  S. Perry,et al.  Begging and transfer of coati meat by white-faced capuchin monkeys,Cebus capucinus , 1994, Primates.

[43]  J. Pruetz,et al.  Savanna Chimpanzees, Pan troglodytes verus, Hunt with Tools , 2007, Current Biology.

[44]  P. Richerson,et al.  Not by genes alone: How culture transformed human evolution. , 2004 .

[45]  R. Timm,et al.  Predation by squirrel monkeys and double‐toothed kites on tent‐making bats , 1985, American journal of primatology.

[46]  E. Visalberghi,et al.  Social facilitation of eating novel food in tufted capuchin monkeys (Cebus apella): input provided by group members and responses affected in the observer , 2001, Animal Cognition.

[47]  L. Huber,et al.  Social influences on the development of foraging behavior in free‐living common marmosets (Callithrix jacchus) , 2006, American journal of primatology.

[48]  J. Silk Patterns of food sharing among mother and infant chimpanzees at Gombe National Park, Tanzania. , 1978, Folia primatologica; international journal of primatology.

[49]  C. Snowdon,et al.  Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus) , 1984, Animal Behaviour.

[50]  P. Garber,et al.  Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care. , 1997, Folia primatologica; international journal of primatology.

[51]  B. Beck,et al.  Food transfers in wild and reintroduced golden lion tamarins, Leontopithecus rosalia , 1999, American journal of primatology.

[52]  T. Bugnyar,et al.  Push or pull: an experimental study on imitation in marmosets , 1997, Animal Behaviour.

[53]  M. E. Yamamoto,et al.  Effect of Removal from the Family Group on Feeding Behavior by Captive Callithrix jacchus , 2004, International Journal of Primatology.

[54]  A. Stone Foraging Ontogeny is not Linked to Delayed Maturation in Squirrel Monkeys (Saimiri sciureus) , 2006 .

[55]  A. Whiten,et al.  Testing for social learning and imitation in common marmosets, Callithrix jacchus, using an artificial fruit , 2004, Animal Cognition.

[56]  D. Watts Observations on the ontogeny of feeding behavior in mountain gorillas (Gorilla gorilla beringei) , 1985, American journal of primatology.

[57]  E. Lonsdorf What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? , 2005, Animal Cognition.

[58]  D. Fragaszy,et al.  Variation among juvenile capuchins in social influences on exploration , 1994, American journal of primatology.

[59]  S. Zimmerman,et al.  The influence of social-affective context on the formation of children's food preferences. , 1980 .

[60]  Julie Gros-Louis,et al.  The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller , 2004, Animal Behaviour.

[61]  P L Gildenberg Where have we been? Where are we going? , 1997, Stereotactic and functional neurosurgery.

[62]  S. Gursky Allocare in a Nocturnal Primate: Data on the Spectral Tarsier, Tarsius spectrum , 2000, Folia Primatologica.

[63]  L. Rapaport Provisioning of Young in Golden Lion Tamarins (Callitrichidae, Leontopithecus rosalia): A Test of the Information Hypothesis , 1999 .

[64]  H. Kummer,et al.  Cues of ownership in long-tailed macaques, Macaca fascicularis , 1991, Animal Behaviour.

[65]  A. Whiten,et al.  On the Nature and Evolution of Imitation in the Animal Kingdom: Reappraisal of a Century of Research , 1992 .

[66]  Dorothy M. Fragaszy,et al.  On the relation between social dynamics and social learning , 1995, Animal Behaviour.

[67]  D. Fragaszy,et al.  The ontogeny of foraging in squirrel monkeys, Saimiri oerstedi , 1989, Animal Behaviour.

[68]  L. T. Nash,et al.  Introduction: evolution, morphology, and behavior of lorisoid primates , 2007 .

[69]  C. V. van Schaik,et al.  Begging for information: mother–offspring food sharing among wild Bornean orangutans , 2008, American journal of primatology.

[70]  A. Feistner,et al.  Food sharing in lion tamarins: Tests of three hypotheses , 1993, American journal of primatology.

[71]  K. Izawa A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis) , 1978, Primates.

[72]  Kim Hill,et al.  A theory of human life history evolution: Diet, intelligence, and longevity , 2000 .

[73]  J. Terborgh,et al.  On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis) , 2004, Behavioral Ecology and Sociobiology.

[74]  B. King Social information transfer in monkeys, apes, and hominids , 1994 .

[75]  E. Visalberghi,et al.  Social influences on the acquisition of sex‐typical foraging patterns by juveniles in a group of wild tufted capuchin monkeys (Cebus nigritus) , 2005, American journal of primatology.

[76]  P. Garber,et al.  A Preliminary Field Study of the Moustached Tamarin Monkey (Saguinus mystax) in Northeastern Peru: Questions Concerned with the Evolution of a Communal Breeding System , 1984 .

[77]  Yanjie Su,et al.  A preliminary study of food transfer in sichuan snub‐nosed monkeys (Rhinopithecus roxellana) , 2008 .

[78]  A. Feistner,et al.  Food Offering in New World Primates: Two Species Added , 1991 .

[79]  D. Mack,et al.  Food sharing among captive Leontopithecus rosalia. , 1978, Folia primatologica; international journal of primatology.

[80]  T. Matsuzawa,et al.  Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. , 1990, Journal of comparative psychology.

[81]  T. Matsuzawa,et al.  Response to novel food in infant chimpanzees: Do infants refer to mothers before ingesting food on their own? , 2005, Behavioural Processes.

[82]  C. Snowdon,et al.  Social communication about unpalatable foods in tamarins (Saguinus oedipus). , 2003, Journal of comparative psychology.

[83]  N. Caine,et al.  Factors affecting the rates of food calls given by red-bellied tamarins , 1995, Animal Behaviour.

[84]  A. Vitale,et al.  The Response to Novel Foods in Common Marmoset (Callithrix jacchus): The Effects of Different Social Contexts , 2010 .

[85]  A. Whiten,et al.  Social learning by orangutans (Pongo abelii and Pongo pygmaeus) in a simulated food-processing task. , 2003, Journal of comparative psychology.

[86]  L. Fedigan,et al.  Evaluating social influences on food-processing behavior in white-faced capuchins (Cebus capucinus). , 2005, American journal of physical anthropology.

[87]  E. Zimmermann Reproduction, physical growth and behavioral development in slow loris (Nycticebus coucang, Lorisidae) , 1989 .

[88]  Andrew Whiten,et al.  Studies of imitation in chimpanzees and children. , 1996 .

[89]  D. Biro,et al.  Emergence of a culture in wild chimpan-zees: education by master-apprenticeship , 2001 .

[90]  E. Visalberghi,et al.  Socially biased learning in monkeys , 2004, Learning & behavior.

[91]  S. Boinski,et al.  The Biology of Traditions: Do brown capuchins socially learn foraging skills? , 2003 .

[92]  K. MacDonald Cross-cultural Comparison of Learning in Human Hunting , 2007, Human nature.

[93]  Dorothy Fragaszy,et al.  Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools , 2004, American journal of primatology.

[94]  T. Caro,et al.  Is There Teaching in Nonhuman Animals? , 1992, The Quarterly Review of Biology.

[95]  N. Nicolson Infants, mothers, and other females , 1987 .

[96]  C. Ruiz-Miranda,et al.  Tutoring in Wild Golden Lion Tamarins , 2002, International Journal of Primatology.

[97]  R. Hoage Social and physical maturation in captive lion Tamarins, Leontopithecus rosalia rosalia (Primates, Callitrichidae) , 1982 .

[98]  C. Snowdon,et al.  Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins, Saguinus oedipus , 2008, Animal Behaviour.

[99]  A. Whiten,et al.  Cultures in chimpanzees , 1999, Nature.

[100]  L. Giraldeau,et al.  Social influences on foraging in vertebrates: causal mechanisms and adaptive functions , 2001, Animal Behaviour.

[101]  C. Snowdon,et al.  Food Transfer and Development of Feeding Behavior and Food‐Associated Vocalizations in Cotton‐Top Tamarins , 2001 .

[102]  Communication about potentially harmful foods in free-ranging chacma baboons,Papio ursinus , 2006, Primates.

[103]  Bernhard Voelkl,et al.  Imitation as Faithful Copying of a Novel Technique in Marmoset Monkeys , 2007, PloS one.