Animal Cognition

, Volume 19, Issue 4, pp 813–818 | Cite as

Evaluation of third-party reciprocity by squirrel monkeys (Saimiri sciureus) and the question of mechanisms

  • James R. Anderson
  • Benoit Bucher
  • Hika Kuroshima
  • Kazuo Fujita
Original Paper


Social evaluation during third-party interactions emerges early in human ontogeny, and it has been shown in adult capuchin monkeys who witness violations of reciprocity in object exchanges: Monkeys were less inclined to accept food from humans who refused to reciprocate with another human. A recent study reporting similar evidence in marmoset monkeys raised the possibility that such evaluations might be based on species’ inherent cooperativeness. We tested a species not renowned for cooperativeness—squirrel monkeys—using the procedure used with marmosets and found a similar result. This finding rules out any crucial role for cooperative tendencies in monkeys’ responses to unfair exchanges. We then tested squirrel monkeys using procedures more similar to those used in the original study with capuchins. Squirrel monkeys again accepted food less frequently from non-reciprocators, but unlike capuchins, they also strongly preferred reciprocators. We conclude that neither squirrel monkeys nor marmoset monkeys engaged in emotional bookkeeping of the type that probably underlies social evaluation in capuchin monkeys; instead, they employed one or more simple behavioral rules. Further comparative studies are required to clarify the mechanisms underlying social evaluation processes across species.


Non-human primates Saimiri sciureus Social exchange Third-party relationships Reciprocity Social evaluation 



This research was supported by JSPS Grant-in-Aid for Research Activity Start-up No. 2688503 to JRA, and by JSPS Grant-in-Aid for Scientific Research (A) No. 25240020 and that for Priority Areas No. 25118002 to KF. Housing and care of the monkeys adhered to Kyoto University Primate Research Institute’s Guide for the Care and Use of Laboratory Primates (2nd ed.). The study was approved by the Animal Experiment Committee of the Graduate School of Letters, Kyoto University.

Supplementary material

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  1. Alexander RD (1987) The biology of moral systems. Aldine de, GruyterGoogle Scholar
  2. Anderson JR, Takimoto A, Kuroshima H, Fujita K (2013a) Capuchin monkeys judge third-party reciprocity. Cognition 127:140–146. doi: 10.1016/j.cognition.2012.12.007 CrossRefPubMedGoogle Scholar
  3. Anderson JR, Kuroshima H, Takimoto A, Fujita K (2013b) Third-party social evaluation of humans by monkeys. Nat Commun 4:1561. doi: 10.1038/ncomms2495 CrossRefPubMedGoogle Scholar
  4. Boinski S, Mitchell CL (1994) Male residence and association patterns in Costa Rican squirrel monkeys (Saimiri oerstedi). Am J Primatol 34:157–169CrossRefGoogle Scholar
  5. Borgeaud C, van de Waal E, Bshary R (2013) Third-party ranks knowledge in wild vervet monkeys (Chlorecebus aethiops pygerythrus). PLoS One 8(3):e58562. doi: 10.1371/journal.pone.0058562 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brosnan SF, de Waal FBM (2014) Evolution of responses to (un)fairness. Science. doi: 10.1126/science.1251776 PubMedPubMedCentralGoogle Scholar
  7. Cheney DL (2011) Extent and limits of cooperation in animals. Proc Natl Acad Sci USA 108(suppl.2):10902–10909. doi: 10.1073/pnas.1100291108 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cheney DL, Seyfarth RM, Silk JB (1995) The responses of female baboons (Papio cynocephalus anubis) to anomalous social interactions: evidence for causal reasoning? J Comp Psychol 109:134–141. doi: 10.1037/0735-7036.109.2.134 CrossRefPubMedGoogle Scholar
  9. Crockford C, Wittig RM, Seyfarth RM, Cheney DL (2007) Baboons eavesdrop to deduce mating opportunities. Anim Behav 73:885–890. doi: 10.1016/j.anbehav.2006.10.016 CrossRefGoogle Scholar
  10. deWaal FBM, Leimgruber K, Greenberg AR (2008) Giving is self-rewarding for monkeys. Proc Nal Acad Sci USA 105:13685–13689. doi: 10.1073/pnas.0807060105 CrossRefGoogle Scholar
  11. Earley RL (2010) Social eavesdropping and the evolution of conditional cooperation and cheating strategies. Phil Trans R Soc Lond B 365:2675–2686. doi: 10.1098/rstb.2010.0147 CrossRefGoogle Scholar
  12. Geraci A, Surian L (2011) The developmental roots of fairness: infants’ reactions to equal and unequal distributions of resources. Dev Sci 14:1012–1020. doi: 10.1111/j.1467-7687.2011.01048.x CrossRefPubMedGoogle Scholar
  13. Hamlin JK, Wynn K, Bloom P (2010) Three-month-olds show a negativity bias in their social evaluations. Dev Sci 13:923–929. doi: 10.1111/j.1467-7687.2010.00951.x CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kawai N, Yasue M, Banno T, Ichinohe N (2014) Marmoset monkeys evaluate third-party reciprocity. Biol Lett 10:20140058. doi: 10.1098/rsbl.2014.0058 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Mendres KA, de Waal FBM (2000) Capuchins do cooperate: the advantage of an intuitive task. Anim Behav 60:523–539CrossRefPubMedGoogle Scholar
  16. Nowak MA, Sigmund K (1998) Evolution of indirect reciprocity by image scoring. Nature 393:573–577. doi: 10.1038/31225 CrossRefPubMedGoogle Scholar
  17. Russell YI, Call J, Dunbar RIM (2008) Image scoring in great apes. Behav Process 78:108–111. doi: 10.1016/j.beproc.2007.10.009 CrossRefGoogle Scholar
  18. Sabbatini G, de Bortoli Vizioli A, Visalberghi E, Schino G (2012) Food transfers in capuchin monkeys: an experiment on partner choice. Biol Lett 8:757–759. doi: 10.1098/rsbl.2012.0534 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Schino G, Aureli F (2009) Reciprocal altruism in primates: partner choice, cognition, and emotions. Adv Stud Behav 39:45–69. doi: 10.1016/S0065-3454(09)39002-6 CrossRefGoogle Scholar
  20. Schmitt MFH, Sommerville JA (2011) Fairness expectations and altruistic sharing in 15-month-old human infants. PLoS One 6(10):e23223. doi: 10.1371/journal.pone.0023223 CrossRefGoogle Scholar
  21. Sloane S, Baillargeon R, Premack D (2012) Do infants have a sense of fairness? Psychol Sci 23:196–204. doi: 10.1177/0956797611422072 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Snowdon CT, Ziegler TE (2007) Growing up cooperatively: family processes and infant development in marmosets and tamarins. J Dev Process 2:40–66Google Scholar
  23. Subiaul F, Vonk J, Okamoto-Barth S, Barth J (2008) Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. Anim Cogn 11:611–623. doi: 10.1007/s10071-008-0151-6 CrossRefPubMedGoogle Scholar
  24. Sun L (2013) The fairness instinct: the Robin Hood mentality and our biological nature. Prometheus Books, New YorkGoogle Scholar
  25. Takimoto A, Kuroshima H, Fujita K (2010) Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food choice for conspecifics. Anim Cogn 13:249–261. doi: 10.1007/s10071-009-0262-8 CrossRefPubMedGoogle Scholar
  26. Talbot CF, Freeman HD, Williams LE, Brosnan SF (2011) Squirrel monkeys’ responses to inequitable outcomes indicates a behavioural convergence within the primates. Biol Lett 7:680–682CrossRefPubMedPubMedCentralGoogle Scholar
  27. Werdenich D, Huber L (2002) Social factors, determine cooperation in marmosets. Anim Behav 64:771–781CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • James R. Anderson
    • 1
  • Benoit Bucher
    • 1
  • Hika Kuroshima
    • 1
  • Kazuo Fujita
    • 1
  1. 1.Department of PsychologyKyoto University Graduate School of LettersKyotoJapan

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