What Did You Get? What Social Learning, Collaboration, Prosocial Behaviour, and Inequity Aversion Tell Us About Primate Social Cognition

  • Lydia M. HopperEmail author
  • Katherine A. Cronin
Part of the Interdisciplinary Evolution Research book series (IDER)


Consideration of social cognition—how an individual’s decision-making is influenced by her/his social environment—is key to understanding the behaviour of socially living nonhuman primates. In this chapter we discuss primate social cognition by focusing on primates’ behavioural responses to the presence and actions of others, how they adjust their behaviour to maximize their own gains, and possibly also the rewards received by a partner. Individuals can observe and replicate the actions of others, or the outcomes of their actions, to accelerate behavioural acquisition of techniques to obtain rewards (social learning). Beyond passively observing others, primates can also work with group mates to obtain rewards more easily or to get rewards that would otherwise be unattainable by a single individual (collaboration). Although not universally seen among primates, one individual may also help another to acquire resources (prosocial behaviour). Prosocial and collaborative interactions may result in an imbalance of benefits received, and certain primate species respond negatively when receiving less than a social partner (inequity aversion), a response which may protect individuals against cheating. Such behaviours demonstrate how the interplay between an individual’s desires and those of others can modify behavioural outcomes and the importance of considering cognition from a social perspective in order to understand the decision-making of individuals. However, there is variation both within and between species in their sensitivity to the actions of others and their responses to them. Thus, a comparative framework is needed when studying what is meant by ‘primate social cognition’.


Inequity aversion Cooperation Social learning Prosociality Collaboration Fairness 


  1. Amici F, Visalberghi E, Call J (2014) Lack of prosociality in great apes, capuchin monkeys and spider monkeys: convergent evidence from two different food distribution tasks. Proc R Soc B 281(1793). CrossRefPubMedGoogle Scholar
  2. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Tai National Park. Am J Phys Anthropol 78:547–573CrossRefPubMedGoogle Scholar
  3. Bräuer J, Call J, Tomasello M (2009) Are apes inequity averse? New data on the token-exchange paradigm. Am J Primatol 71(2):175–181CrossRefPubMedGoogle Scholar
  4. Brosnan SF (2011) A hypothesis of the co-evolution of cooperation and responses to inequity. Front Neurosci 5.
  5. Brosnan SF (2013) Justice and fairness related behaviors in non-human primates. Proc Natl Acad Sci USA 110:10416–10423CrossRefPubMedGoogle Scholar
  6. Brosnan SF, de Waal FBM (2003) Monkeys reject unequal pay. Nature 425(6955):297–299CrossRefPubMedGoogle Scholar
  7. Brosnan SF, Hopper LM (2014) Psychological limits on animal innovation. Anim Behav 92:325–332CrossRefGoogle Scholar
  8. Brosnan SF, Talbot C, Ahlgren M, Lambeth SP, Schapiro SJ (2010) Mechanisms underlying responses to inequitable outcomes in chimpanzees, Pan troglodytes. Anim Behav 79(6):1229–1237CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brosnan SF, Hopper LM, Richey S, Freeman HD, Talbot CF, Gosling S, Lambeth SP, Schapiro SJ (2015) Personality influences responses to inequity and contrast in chimpanzees. Anim Behav 101:75–87CrossRefPubMedPubMedCentralGoogle Scholar
  10. Burkart JM, Rueth K (2013) Preschool children fail primate prosocial game because of attentional task demands. PLoS One 8(7):e68440CrossRefPubMedPubMedCentralGoogle Scholar
  11. Burkart JM, Hrdy SB, van Schaik CP (2009) Cooperative breeding and human cognitive evolution. Evol Anthropol 18:175–186CrossRefGoogle Scholar
  12. Burkart JM, Allon O, Amici F, Fichtel C, Finkenwirth C, Heschl A, Huber J, Isler K, Kosonen ZK, Martins E, Meulman EJ, Richiger R, Rueth K, Spillmann B, Wiesendanger S, van Schaik CP (2014) The evolutionary origin of human hyper-cooperation. Nat Commun 5:4747CrossRefPubMedGoogle Scholar
  13. Byrne RW, Rapaport LG (2011) What are we learning from teaching? Anim Behav 82(5):1207–1211CrossRefGoogle Scholar
  14. Byrne RW, Whiten A (1988) Machiavellian intelligence. Oxford University Press, OxfordGoogle Scholar
  15. Caldwell CA, Schillinger K, Evans CL, Hopper LM (2012) End state copying by humans (Homo sapiens): implications for a comparative perspective on cumulative culture. J Comp Psychol 126:161–169CrossRefPubMedPubMedCentralGoogle Scholar
  16. Carter AJ, Marhsall HH, Heinsohn R, Cowlishaw G (2014) Personality predicts the propensity for social learning in a wild primate. Peer J 2:e283CrossRefPubMedGoogle Scholar
  17. Castro L, Toro MA (2004) The evolution of culture: from primate social learning to human culture. Proc Natl Acad Sci USA 101(27):10235–10240CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chalmeau R, Visalberghi E, Gallo A (1997) Capuchin monkeys, Cebus apella, fail to understand a cooperative task. Anim Behav 54(5):1215–1225CrossRefPubMedGoogle Scholar
  19. Claidière N, Messer EJE, Hoppitt W, Whiten A (2013) Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr Biol 23:1251–1255CrossRefPubMedGoogle Scholar
  20. Claidière N, Whiten A, Mareno MC, Messer EJE, Brosnan SF, Hopper LM, Lambeth SP, Schapiro SJ, McGuigan N (2015) Selective and contagious prosocial resource donation in capuchin monkeys, chimpanzees and humans. Sci Rep 5:7631CrossRefPubMedPubMedCentralGoogle Scholar
  21. Coussi-Korbel S, Fragaszy DM (1995) On the relation between social dynamics and social learning. Anim Behav 50(6):1441–1453CrossRefGoogle Scholar
  22. Crawford MP (1937) The cooperative solving of problems by young chimpanzees. Comp Psychol Mono 14:1–88Google Scholar
  23. Crockford C, Wittig R, Mundry R, Zuberbuhler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22(2):142–146CrossRefPubMedGoogle Scholar
  24. Cronin KA (2012) Cognitive aspects of prosocial behavior in nonhuman primates. In: Seel NM (ed) Encyclopedia of the sciences of learning, vol 3. Springer, Berlin, pp 581–583Google Scholar
  25. Cronin KA (2016a) Comparative studies of cooperation: collaboration and prosocial behavior in animals. In: Call J, Burghardt GB, Pepperberg I, Snowdon CT, Zental T (eds) APA handbook of comparative psychology. American Psychological Association, Washington, DCGoogle Scholar
  26. Cronin KA (2016b) Unnatural paradigm calls into question whether macaques’ social decisions represent empathy. Proc Natl Acad Sci USA 113(10):E1331CrossRefPubMedGoogle Scholar
  27. Cronin KA, Hopper LM (2017) A Comparative perspective on helping and fairness. In: Sommerville J, Decety J (eds) Social cognition, frontiers in developmental science series. Routledge Taylor and Francis Group, New York, NY, pp 26–45Google Scholar
  28. Cronin KA, Sánchez A (2012) Social dynamics and cooperation: the case of nonhuman primates and its implications for human behavior. Adv Complex Sys 15:1250066CrossRefGoogle Scholar
  29. Cronin KA, Snowdon CT (2008) The effects of unequal reward distributions on cooperative performance by cottontop tamarins, Saguinus oedipus. Anim Behav 75(1):245–257CrossRefPubMedPubMedCentralGoogle Scholar
  30. Cronin KA, Kurian AV, Snowdon CT (2005) Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus). Anim Behav 69(1):133–142CrossRefPubMedPubMedCentralGoogle Scholar
  31. Cronin KA, Pieper BA, van Leeuwen EJC, Mundry R, Haun DBM (2014) Problem solving in the presence of others: how rank and relationship quality impact resource acquisition in chimpanzees (Pan troglodytes). PLoS One 9(4):e93204CrossRefPubMedPubMedCentralGoogle Scholar
  32. Cronin KA, Acheson DJ, Hernandez P, Sanchez A (2015a) Hierarchy is detrimental for human cooperation. Sci Rep 5:18634CrossRefPubMedPubMedCentralGoogle Scholar
  33. Cronin KA, Pieper B, van Leeuwen EJC, Crockford C, Haun DBM (2015b) Cooperating to compete: evaluating behavioral coordination in response to simulated territorial intrusion in chimpanzees (Pan troglodytes). Am J Primatol 77(S1):77Google Scholar
  34. Cronin KA, Jacobson SL, Bonnie KE, Hopper LM (2017) Studying primate cognition in a social setting to improve validity and welfare: a literature review highlighting successful approaches. PeerJ 5:e3649CrossRefPubMedPubMedCentralGoogle Scholar
  35. de Waal FBM (1982) Chimpanzee politics: power and sex among apes. Jonathon Cape, LondonGoogle Scholar
  36. de Waal FBM, Davis JM (2003) Capuchin cognitive ecology: cooperation based on projected returns. Neuropsychol 41(2):221–228CrossRefGoogle Scholar
  37. de Waal FBM, Suchak M (2010) Prosocial primates: selfish and unselfish motivations. Phil Trans R Soc B 365(1553):2711–2722CrossRefPubMedGoogle Scholar
  38. DeCasien AR, Williams SA, Higham JP (2017) Primate brain size is predicted by diet but not sociality. Nat Ecol Evol 1:112CrossRefPubMedGoogle Scholar
  39. Drea CM (2006) Studying primate learning in group contexts: tests of social foraging, response to novelty and cooperative problem solving. Methods 38:162–177CrossRefPubMedGoogle Scholar
  40. Drea CM, Wallen K (1999) Low-status monkeys “play dumb” when learning in mixed social groups. Proc Natl Acad Sci USA 96(22):12965–12960CrossRefPubMedGoogle Scholar
  41. Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190CrossRefGoogle Scholar
  42. Feistner ATC, McGrew WC (1989) Food-sharing in primates: a critical review. In: Seth PK, Seth S (eds) Perspectives in primate biology, vol 3. Today & Tomorrow’s Printers and Publishers, New Delhi, pp 21–36Google Scholar
  43. Freeman HD, Sullivan J, Hopper LM, Talbot CF, Holmes AN, Schultz-Darken N, Williams LE, Brosnan SF (2013) Different responses to reward comparisons by three primate species. PLoS One 8(10):e76297CrossRefPubMedPubMedCentralGoogle Scholar
  44. Gunst N, Leca JB, Vasey PL (2015) Influence of sexual competition and social context on homosexual behavior in adolescent female Japanese macaques. Am J Primatol 77(5):502–515CrossRefPubMedGoogle Scholar
  45. Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623CrossRefPubMedGoogle Scholar
  46. Hecht EE, Gutman DA, Preuss TM, Sanchez MM, Parr LA, Riling JK (2012) Process versus product in social learning: comparative diffusion tensor imaging of neural systems for action execution–observation matching in macaques, chimpanzees, and humans. Cereb Cortex 23(5):1014–1024CrossRefPubMedPubMedCentralGoogle Scholar
  47. Herbinger I, Papworth S, Boesch C, Zuberbühler K (2009) Vocal, gestural and locomotor responses of wild chimpanzees to familiar and unfamiliar intruders: a playback study. Anim Behav 78(6):1389–1396CrossRefGoogle Scholar
  48. Hirata S, Fuwa K (2007) Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task. Primates 48:13–21CrossRefPubMedGoogle Scholar
  49. Hopper LM (2010) ‘Ghost’ experiments and the dissection of social learning in humans and animals. Biol Rev 85:685–701CrossRefPubMedGoogle Scholar
  50. Hopper LM (2017) Social learning and decision making. In: Schapiro SJ (ed) Handbook of primate behavior management. CRC Press, Taylor & Francis Group, Boca Raton, FL, pp 225–242CrossRefGoogle Scholar
  51. Hopper LM, Marshall-Pescini S, Whiten A (2012) Social learning and culture in child and chimpanzee. In: de Waal FBM, Ferrari PF (eds) The primate mind: built to connect with other minds. Harvard University Press, Cambridge, pp 99–118Google Scholar
  52. Hopper LM, Lambeth SP, Schapiro SJ, Brosnan SF (2014) Social comparison mediates chimpanzees’ responses to loss, not frustration. Anim Cogn 17(6):1303–1311CrossRefPubMedPubMedCentralGoogle Scholar
  53. Horner V, Proctor D, Bonnie KE, Whiten A, de Waal FBM (2010) Prestige affects cultural learning in chimpanzees. PLoS One 5(5):e10625CrossRefPubMedPubMedCentralGoogle Scholar
  54. House BR (2013) Ontogenetic and phylogenetic variation in prosocial behavior: differences in prosociality across human development and primate species. Retrieved from
  55. House BR, Silk JB, Lambeth SP, Schapiro SJ (2014) Task design influences prosociality in captive chimpanzees (Pan troglodytes). PLoS One 9(9):e103422CrossRefPubMedPubMedCentralGoogle Scholar
  56. Hrdy SB (2009) Mothers and others. Belknap Press, Cambridge, MAGoogle Scholar
  57. Huguet P, Barbet I, Belletier C, Monteil JM, Fagot J (2014) Cognitive control under social influence in baboons. J Exp Psychol Gen 143(6):2067–2073CrossRefPubMedGoogle Scholar
  58. Humle T, Snowdon CT (2008) Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins, Saguinus oedipus. Anim Behav 75:67–277CrossRefGoogle Scholar
  59. Humphrey NK (1976) The social function of intellect. In: Bateson PPG, Hinde RA (eds) Growing Points in Ethology. Cambridge University Press, Cambridge, pp 303–317Google Scholar
  60. Kendal RL, Hopper LM, Whiten A, Brosnan SF, Lambeth SP, Schapiro SJ, Hoppitt W (2015) Chimpanzees copy dominant and knowledgeable individuals: implications for cultural diversity. Evol Hum Behav 36(1):65–72CrossRefPubMedPubMedCentralGoogle Scholar
  61. Marshall HH, Carter AJ, Ashford A, Rowcliffe JM, Cowlishaw G (2015) Social effects on foraging behavior and success depend on local environmental conditions. Ecol Evol 5(2):475–492CrossRefPubMedPubMedCentralGoogle Scholar
  62. McAuliffe K, Chang LW, Leimgruber KL, Spaulding R, Blake PR, Santos LR (2015) Capuchin monkeys, Cebus apella, show no evidence for inequity aversion in a costly choice task. Anim Behav 103:65–74CrossRefGoogle Scholar
  63. Melis AP, Hare B, Tomasello M (2006) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72(2):275–286CrossRefGoogle Scholar
  64. Mendres KA, de Waal FBM (2000) Capuchins do cooperate: the advantage of an intuitive task. Anim Behav 60(4):523–529CrossRefPubMedGoogle Scholar
  65. Mitani JC (2009) Cooperation and competition in chimpanzees: current understanding and future challenges. Evol Anthropol 18:215–227CrossRefGoogle Scholar
  66. Nishida T, Matsusaka T, McGrew CW (2009) Emergence, propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review. Primates 50(1):23–36CrossRefPubMedPubMedCentralGoogle Scholar
  67. Noe R (2006) Cooperation experiments: coordination through communication versus acting apart together. Anim Behav 71(1):1–18CrossRefGoogle Scholar
  68. Padilla-Walker LM, Carlo G (2014) The study of prosocial behavior: past, present and future. In: Padilla-Walker LM, Carlo G (eds) Prosocial development: a multidimensional approach. Oxford University Press, Oxford, pp 3–16CrossRefGoogle Scholar
  69. Pasquaretta C, Levé M, Claidière N, van de Waal E, Whiten A, Macintosh A, Pelé M, Bergstrom M, Borgeaud C, Brosnan F, Crofoot M, Fedigan L, Fichtel C, Hopper LM, Mareno M, Petit O, Schnoell AV, Polizzi di Sorrentino E, Thierry B, Tiddi B, Sueur C (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600CrossRefPubMedPubMedCentralGoogle Scholar
  70. Petit O, Desportes C, Thierry B (1992) Differential probability of “coproduction” in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90(2):107–120CrossRefGoogle Scholar
  71. Powell LE, Isler K, Barton RA (2017) Re-evaluating the link between brain size and behavioural ecology in primates. Proc R Soc B 284:20171765CrossRefPubMedGoogle Scholar
  72. Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci USA 99(7):4436–4441CrossRefPubMedGoogle Scholar
  73. Salwiczek LH, Prétôt L, Demarta L, Proctor D, Essler J, Pinto AI, Wismer S, Stoinski T, Brosnan SF, Bshary R (2012) Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner-client reef fish cooperation. PLoS One 7(11):e49068CrossRefPubMedPubMedCentralGoogle Scholar
  74. Schmelz M, Call J (2016) The psychology of primate cooperation and competition: a call for realigning research agendas. Phil Trans R Soc B 371(1686):20150067. CrossRefPubMedGoogle Scholar
  75. Silk JB, Brosnan SF, Vonk J, Henrich J, Povinelli DJ, Richardson AS, Lambeth SP, Mascaro J, Schapiro SJ (2005) Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437:1357–1359CrossRefPubMedGoogle Scholar
  76. Snowdon CT, Cronin KA (2009) Comparative cognition and neuroscience. In: Berntson G, Cacioppo J (eds) Handbook of neuroscience for the behavioral sciences. Wiley, Hoboken, NJ, pp 32–55Google Scholar
  77. Sterck EH, Olesen CU, Massen JJ (2015) No costly prosociality among related long-tailed macaques (Macaca fascicularis). J Comp Psychol 129(3):275–282CrossRefPubMedGoogle Scholar
  78. Stevens JR (2010) Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus). Anim Cogn 13:663–670CrossRefPubMedGoogle Scholar
  79. Strandburg-Peshkin A, Farine DR, Couzin ID, Crofoot MC (2015) Shared decision-making drives collective movement in wild baboons. Science 348(6241):1358–1361CrossRefPubMedPubMedCentralGoogle Scholar
  80. Suchak M, Eppley TM, Campbell MW, de Waal FBM (2014) Ape duos and trios: spontaneous cooperation with free partner choice in chimpanzees. PeerJ 2:e417CrossRefPubMedPubMedCentralGoogle Scholar
  81. Thierry B (1985) Patterns of agonistic interactions in three species of macaque (Macaca mulatta, M fascicularis, M tonkeana). Aggress Behav 11:223–233CrossRefGoogle Scholar
  82. Thierry B (2007) Unity in diversity: lessons from macaque societies. Evol Anthropol 16(6):224–238CrossRefGoogle Scholar
  83. Thornton A, McAuliffe K (2015) Cognitive consequences of cooperative breeding? A critical appraisal. J Zool 295(1):12–22CrossRefGoogle Scholar
  84. Tinklepaugh OL (1928) An experimental study of representative factors in monkeys. Comp Psychol 8:197–236CrossRefGoogle Scholar
  85. van Schaik CP (2003) Local traditions in orangutans and chimpanzees: social learning and social tolerance. In: Fragaszy D, Perry SE (eds) The biology of animal traditions. Cambridge University Press, Cambridge, pp 297–328CrossRefGoogle Scholar
  86. Visalberghi E, Pellegrini Quarantotti B, Tranchida F (2000) Solving a cooperation task without taking into account the partner’s behavior: the case of capuchin monkeys (Cebus apella). J Comp Psychol 114(3):297–301CrossRefPubMedGoogle Scholar
  87. Vonk J, Shackelford TK (2012) The Oxford handbook of comparative evolutionary psychology. Oxford University Press, New York, NYGoogle Scholar
  88. Watson CFI, Caldwell CA (2009) Understanding behavioral traditions in primates: are current experimental approaches too focused on food? Int J Primatol 30:143–167CrossRefGoogle Scholar
  89. Wilson ML, Britton NF, Franks NR (2002) Chimpanzees and the mathematics of battle. Proc R Soc Lond B 269(1496):1107–1112CrossRefGoogle Scholar
  90. Wilson ML, Kahlenberg SM, Wells M, Wrangham RW (2011) Ecological and social factors affect the occurrence and outcomes of intergroup encounters in chimpanzees. Anim Behav 83(1):277–291CrossRefGoogle Scholar
  91. Yamamoto S, Humle T, Tanaka M (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc Natl Acad Sci USA 109(9):3588–3592CrossRefPubMedGoogle Scholar
  92. Zentall TR, Wasserman EA (2012) The Oxford handbook of comparative cognition. Oxford University Press, New York, NYGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park ZooChicagoUSA

Personalised recommendations