, Volume 55, Issue 3, pp 447–457 | Cite as

Calculated reciprocity? A comparative test with six primate species

  • Federica AmiciEmail author
  • Filippo Aureli
  • Roger Mundry
  • Alejandro Sánchez Amaro
  • Abraham Mesa Barroso
  • Jessica Ferretti
  • Josep Call
Original Article


Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.


Calculated reciprocity Great apes Capuchin monkeys Spider monkeys Altruism 



This work was conducted while the first author held a Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID number 1138999). We thank Elisabetta Visalberghi, Roberto Pacheco Mendez, Fernando Victoria Arceo, Iber Rodriguez Castillo and all the animal keepers at the different facilities for endless support and cooperation. Thanks to Sebastian Egner for coding data for inter-observer reliability purposes and to Hanna Petschauer for helping wonderfully with organizing data collection. This study complies with the ethical standards as laid down by the Primate Society of Japan and was ethically approved by an internal committee at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany.

Supplementary material

10329_2014_424_MOESM1_ESM.docx (1.7 mb)
Supplementary material (DOCX 1744 kb)


  1. Addessi E, Crescimbene L, Visalberghi E (2008) Food and token quantity discrimination in capuchin monkeys (Cebus apella). Anim Cogn 11:275–282PubMedCrossRefGoogle Scholar
  2. Addessi E, Paglieri F, Focaroli V (2011) The ecological rationality of delay tolerance: insights from capuchin monkeys. Cognition 119:142–147PubMedCrossRefGoogle Scholar
  3. Amici F, Aureli F, Call J (2008) Fission-fusion dynamics, behavioral flexibility and inhibitory control in primates. Curr Biol 18:1415–1419PubMedCrossRefGoogle Scholar
  4. Amici F, Aureli F, Call J (2010) Monkeys and apes: are their cognitive skills really so different? Am J Phys Anthropol 143:188–197PubMedCrossRefGoogle Scholar
  5. Amici F, Call J, Aureli F (2012) Aversion to violation of expectations of food distribution: the role of social tolerance and relative dominance in seven primate species. Behaviour 149:345–368CrossRefGoogle Scholar
  6. Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B (2013) lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2Google Scholar
  8. Beran MJ (2001) Summation and numerousness judgments of sequentially presented sets of items by chimpanzees (Pan troglodytes). J Comp Psychol 115:181–191PubMedCrossRefGoogle Scholar
  9. Brosnan SF, de Waal FBM (2002) A proximate perspective on reciprocal altruism. Hum Nat 13:129–152CrossRefGoogle Scholar
  10. Brosnan SF, Silk JB, Henrich J, Mareno MC, Lambeth SP, Schapiro SJ (2009) Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task. Anim Cogn 12:587–597PubMedCentralPubMedCrossRefGoogle Scholar
  11. Burkart JM, van Schaik CP (2010) Cognitive consequences of cooperative breeding in primates? Anim Cogn 13:1–19PubMedCrossRefGoogle Scholar
  12. Burkart JM, Fehr E, Efferson C, van Schaik CP (2007) Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. Proc Natl Acad Sci USA 104:19762–19766PubMedCentralPubMedCrossRefGoogle Scholar
  13. Burkart JM, Hrdy SB, van Schaik CP (2009) Cooperative breeding and human cognitive evolution. Evol Anthropol 18:175–186CrossRefGoogle Scholar
  14. Call J (2000) Estimating and operating on discrete quantities in orangutans (Pongo pygmaeus). J Comp Psychol 114:136–147PubMedCrossRefGoogle Scholar
  15. Cheney DL, Moscovice LR, Heesen M, Mundry R, Seyfarth RM (2010) Contingent cooperation between wild female baboons. Proc Natl Acad Sci USA 107:9562–9566PubMedCentralPubMedCrossRefGoogle Scholar
  16. Clutton-Brock TH (2009) Cooperation between non-kin in animal societies. Nature 462:51–57PubMedCrossRefGoogle Scholar
  17. de Waal FBM (1997) The chimpanzee’s service economy: food for grooming. Evol Hum Behav 18:375–386CrossRefGoogle Scholar
  18. de Waal FBM, Luttrell LM (1988) Mechanisms of social reciprocity in three primate species: symmetrical relationship characteristics or cognition? Ethol Sociobiol 9:101–118CrossRefGoogle Scholar
  19. Dobson AJ (2002) An introduction to generalized linear models. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  20. Dufour V, Pelé M, Neumann M, Thierry B, Call J (2009) Calculated reciprocity after all: computation behind token transfers in orangutans. Biol Lett 5:172–175PubMedCentralPubMedCrossRefGoogle Scholar
  21. Field A (2005) Discovering statistics using SPSS. Sage Publications, LondonGoogle Scholar
  22. Forstmeier W, Schielzeth H (2011) Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav Ecol Sociobiol 65:47–55PubMedCentralPubMedCrossRefGoogle Scholar
  23. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand OaksGoogle Scholar
  24. Freeman EW, Schulte BA, Brown JL (2010) Using behavioral observations and keeper questionnaires to assess social relationships among captive female African elephants. Zoo Biol 29:140–153PubMedGoogle Scholar
  25. Gomes CM, Mundry R, Boesch C (2009) Long-term reciprocation of grooming in wild West-African chimpanzees. Proc R Soc B 276:699–706PubMedCentralPubMedCrossRefGoogle Scholar
  26. Hattori Y, Kuroshima H, Fujita K (2005) Cooperative problem solving by tufted capuchin monkeys (Cebus apella): spontaneous division of labor, communication and reciprocal altruism. J Comp Psychol 119:335–342PubMedCrossRefGoogle Scholar
  27. Hauser MD, Chen MK, Chen F, Chuang E (2003) Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc R Soc B 270:2363–2370PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hemelrijk CK (1994) Support for being groomed in long-tailed macaques, Macaca fascicularis. Anim Behav 48:479–481CrossRefGoogle Scholar
  29. Herrelko ES, Vick SJ, Buchanan-Smith HM (2012) Cognitive research in zoo-housed chimpanzees: influence of personality and impact on welfare. Am J Primatol 74:828–840PubMedCrossRefGoogle Scholar
  30. Jaeggi AV, Gurven M (2013) Reciprocity explains food sharing in humans and other primates independent of kin selection and tolerated scrounging: a phylogenetic meta-analysis. Proc R Soc B 280:20131615PubMedCrossRefGoogle Scholar
  31. Jensen K, Hare B, Call J, Tomasello M (2006) What’s in it for me? Self-regard precludes altruism and spite in chimpanzees. Proc R Soc B 273:1013–1021PubMedCentralPubMedCrossRefGoogle Scholar
  32. Koyama NF, Caws C, Aureli F (2006) Interchange of grooming and agonistic support in chimpanzees. Int J Primatol 27:1293–1309CrossRefGoogle Scholar
  33. Lakshminarayanan VR, Santos LR (2008) Capuchin monkeys are sensitive to others’ welfare. Curr Biol 18:R999–R1000PubMedCrossRefGoogle Scholar
  34. McCullagh P, Nelder JA (2008) Generalized linear models. Chapman and Hall, LondonGoogle Scholar
  35. Melis AP, Hare B, Tomasello M (2006) Chimpanzees recruit the best collaborators. Science 311:1297–1300PubMedCrossRefGoogle Scholar
  36. Melis AP, Hare B, Tomasello M (2008) Do chimpanzees reciprocate received favours? Anim Behav 76:951–962CrossRefGoogle Scholar
  37. Pelé M, Dufour V, Thierry B, Call J (2009) Token transfers among great apes: species differences, gestural requests and reciprocal exchange. J Comp Psychol 123:375–384PubMedCrossRefGoogle Scholar
  38. Quinn GP, Keough MJ (2002) Experimental designs and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  40. Sabbatini G, de Bortoli Vizioli A, Visalberghi E, Schino G (2012) Food transfers in capuchin monkeys: an experiment on partner choice. Biol Lett 8:757–759PubMedCentralPubMedCrossRefGoogle Scholar
  41. Savage-Rumbaugh ES, Rumbaugh D, Boysen S (1978) Linguistically mediated tool use and exchange by chimpanzees (Pan troglodytes). Behav Brain Sci 4:539–554CrossRefGoogle Scholar
  42. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420PubMedCentralPubMedCrossRefGoogle Scholar
  43. Schino G, Aureli F (2008) Grooming reciprocation among female primates: a meta-analysis. Biol Lett 4:9–11PubMedCentralPubMedCrossRefGoogle Scholar
  44. Schino G, Aureli F (2009) Reciprocal altruism in primates: partner choice, cognition and emotions. Adv Stud Behav 39:45–69CrossRefGoogle Scholar
  45. Schino G, Aureli F (2010a) Primate reciprocity and its cognitive requirements. Evol Anthropol 19:130–135CrossRefGoogle Scholar
  46. Schino G, Aureli F (2010b) The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett 13:45–50PubMedCrossRefGoogle Scholar
  47. Schino G, Pellegrini B (2009) Grooming in mandrills and the time frame of reciprocal partner choice. Am J Primatol 71:884–888PubMedCrossRefGoogle Scholar
  48. Silk JB (2003) Cooperation without counting: the puzzle of friendship. In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. MIT Press, Cambridge, pp 37–54Google Scholar
  49. Silk JB, Brosnan SF, Vonk J, Henrich J, Povinelli DJ, Richardson AS, Lambeth SP, Mascaro J, Shapiro SJ (2005) Chimpanzees are indifferent to the welfare of unrelated group members. Nature 27:1357–1359CrossRefGoogle Scholar
  50. Silk JB, Brosnan SF, Henrich J, Lambeth SP, Shapiro SJ (2013) Chimpanzees share food for many reasons: the role of kinship, reciprocity, social bonds and harassment on food transfers. Anim Behav 85:941–947CrossRefGoogle Scholar
  51. Stevens JR (2010) Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus). Anim Cogn 13:663–670PubMedCrossRefGoogle Scholar
  52. Stevens JR, Hauser MD (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn Sci 8:60–65PubMedCrossRefGoogle Scholar
  53. Tan J, Hare B (2013) Bonobos share with strangers. PLoS ONE 8(1):e51922. doi: 10.1371/journal.pone.0051922 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57CrossRefGoogle Scholar
  55. Vonk J, Brosnan SF, Silk JB, Henrich J, Richardson AS, Lambeth SP, Schapiro SJ, Povinelli DJ (2008) Chimpanzees do not take advantage of very low cost opportunities to deliver food to unrelated group members. Anim Behav 75:1757–1770CrossRefGoogle Scholar
  56. Yamamoto S, Tanaka M (2009) Do chimpanzees (Pan troglodytes) spontaneously take turns in a reciprocal cooperation task? J Comp Psychol 123:242–249PubMedCrossRefGoogle Scholar
  57. Yamamoto S, Tanaka M (2010) The influence of kin relationship and reciprocal context on chimpanzees’ other-regarding preferences. Anim Behav 79:595–602CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2014

Authors and Affiliations

  • Federica Amici
    • 1
    Email author
  • Filippo Aureli
    • 2
    • 3
  • Roger Mundry
    • 1
  • Alejandro Sánchez Amaro
    • 1
  • Abraham Mesa Barroso
    • 4
  • Jessica Ferretti
    • 5
  • Josep Call
    • 1
    • 6
  1. 1.Department of Comparative and Developmental PsychologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.Instituto de NeuroetologiaUniversidad VeracruzanaXalapaMexico
  3. 3.Research Centre in Evolutionary Anthropology and PalaeoecologyLiverpool John Moores UniversityLiverpoolUK
  4. 4.Facultat de PsicologiaUniversitat de BarcelonaBarcelonaSpain
  5. 5.Istituto di Scienze e Tecnologie della Cognizione, CNRRomeItaly
  6. 6.School of Psychology and NeuroscienceUniversity of St AndrewsSt. AndrewsUK

Personalised recommendations