Skip to main content

Delay Maintenance in Tonkean Macaques (Macaca tonkeana) and Brown Capuchin Monkeys (Cebus apella)

Abstract

Animals commonly face choices requiring them to wait and postpone action. The ability to delay gratification is a prerequisite for making future-oriented decisions. We investigated the ability of brown capuchins (Cebus apella) and Tonkean macaques (Macaca tonkeana) to delay benefits in several experiments. In exchange tasks, subjects had to return a piece of cookie after a given time lag to obtain a larger one from an experimenter. Capuchins could wait 10–40 s and macaques 20–80 s depending on subjects and the size of rewards. Both groups were able to anticipate delay durations, but unlike macaques, capuchins discounted all sizes of reward at the same speed, meaning that their delay-maintenance was not affected by the reward size. When the subjects could give the initial piece of cookie back immediately and then wait for the return, performances increased to 10–21 min for capuchins and 21–42 min for macaques, demonstrating the role of consumption inhibition in postponing gratification. In a further task, we presented subjects with an accumulation of food pieces added at short intervals until they seized them. On average, brown capuchins could wait 33–42 s and macaques 38–72 s before seizing the rewards. Our results confirmed that brown capuchins were more impulsive than Tonkean macaques in several tasks. We did not find significant differences between the waiting performances of the Tonkean macaques and those previously reported in long-tailed macaques. The contrasting performances of macaques and capuchins might be related to their different skills in the physical and social domains.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Abeyesinghe, S. M., Nicol, C. J., Hartnell, S. J., & Wathes, C. M. (2005). Can domestic fowl, Gallus gallus domesticus, show self-control? Animal Behaviour, 70, 1–11.

    Article  Google Scholar 

  2. Addessi, E., Crescimbene, L., & Visalberghi, E. (2007). Do capuchin monkeys (Cebus apella) use tokens as symbols? Proceedings of the Royal Society of London B: Biological Series, 274, 2579–2585.

    CAS  Article  Google Scholar 

  3. Addessi, E., Crescimbene, L., & Visalberghi, E. (2008). Food and token quantity discrimination in capuchin monkeys (Cebus apella). Animal Cognition, 11, 275–282.

    Article  PubMed  Google Scholar 

  4. Amici, F., Aureli, F., & Call, J. (2008). Fission-fusion dynamics, behavioral flexibility and inhibitory control in primates. Current Biology, 18, 1415–1419.

    CAS  Article  PubMed  Google Scholar 

  5. Amici, F., Call, J., & Aureli, F. (2009). Variation in withholding of information in three monkey species. Proceedings of the Royal Society of London B: Biological Series, 276, 3311–3318.

    Article  Google Scholar 

  6. Anderson, J. R. (1996). Chimpanzees and capuchin monkeys: comparative cognition. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into thought: The minds of the great apes (pp. 23–56). Cambridge: Cambridge University Press.

    Google Scholar 

  7. Aureli, F., Das, M., & Veenema, H. C. (1997). Differential kinship effect on reconciliation in three species of macaques (Macaca fascicularis, M. fuscata, and M. sylvanus). Journal of Comparative Psychology, 111, 91–99.

    CAS  Article  PubMed  Google Scholar 

  8. Beran, M. J. (2002). Maintenance of self-imposed delay of gratification by four chimpanzees (Pan troglodytes) and an orangutan (Pongo pygmaeus). The Journal of General Psychology, 129, 49–66.

    Article  PubMed  Google Scholar 

  9. Brosnan, S. F., & de Waal, F. B. M. (2004). A concept of value during experimental exchange in brown capuchin monkeys, Cebus apella. Folia Primatologica, 75, 317–330.

    Article  Google Scholar 

  10. Brosnan, S. F., & de Waal, F. B. M. (2005). Responses to a simple barter task in chimpanzees, Pan troglodytes. Primates, 46, 173–182.

    Article  PubMed  Google Scholar 

  11. Brunner, D., & Gibbon, J. (1995). Value of food aggregates: parallel versus serial discounting. Animal Behaviour, 50, 1627–1634.

    Article  Google Scholar 

  12. Chalmeau, R., & Peignot, P. (1998). Exchange of objects between human and captive western lowland gorillas. Primates, 39, 389–398.

    Article  Google Scholar 

  13. Drapier, M., Chauvin, C., Dufour, V., Uhlrich, P., & Thierry, B. (2005). Food-exchange with humans in brown capuchin monkeys. Primates, 46, 241–248.

    Article  PubMed  Google Scholar 

  14. Dufour, V., Pelé, M., Sterck, E. H. M., & Thierry, B. (2007). Chimpanzee (Pan troglodytes) anticipation of food return: coping with waiting time in an exchange task. Journal of Comparative Psychology, 121, 145–155.

    CAS  Article  PubMed  Google Scholar 

  15. Evans, T. A., & Beran, M. J. (2007a). Delay of gratification and delay maintenance by rhesus macaques (Macaca mulatta). The Journal of General Psychology, 134, 199–216.

    Article  PubMed  Google Scholar 

  16. Evans, T. A., & Beran, M. J. (2007b). Chimpanzees use self-distraction to cope with impulsivity. Biology Letters, 3, 599–602.

    Article  PubMed  Google Scholar 

  17. Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: the biology of the genus Cebus. Cambridge: Cambridge University Press.

    Google Scholar 

  18. Green, L., & Myerson, J. (1996). Exponential versus hyperbolic discounting of delayed outcomes: Risk and waiting time. American Zoologist, 36, 496–505.

    Google Scholar 

  19. Green, L., Myerson, J., Holt, D. D., Slevin, J. R., & Estle, S. J. (2004). Discounting of delayed food rewards in pigeons and rats: is there a magnitude effect? Journal of the Experimental Analysis of Behavior, 81, 39–50.

    Article  PubMed  Google Scholar 

  20. Grosch, J., & Neuringer, A. (1981). Self-control in pigeons under the Mischel paradigm. Journal of the Experimental Analysis of Behavior, 35, 3–21.

    CAS  Article  PubMed  Google Scholar 

  21. Haccou, P., & Meelis, E. (1992). Statistical analysis of behavioural data. Oxford: Oxford University Press.

    Google Scholar 

  22. Hyatt, C. W., & Hopkins, W. D. (1998). Interspecies object exchange: bartering in apes? Behavioural Processes, 42, 177–187.

    Article  Google Scholar 

  23. Kacelnik, A. (2003). The evolution of patience. In G. Loewenstein, D. Read, & R. Baumeister (Eds.), Time and decision: Economic and psychological perspectives on intertemporal choice (pp. 115–138). New York: Russell Sage Foundation.

    Google Scholar 

  24. Kagel, J. H., Green, L., & Caraco, T. (1986). When foragers discount the future: constraint or adaptation? Animal Behaviour, 34, 271–283.

    Article  Google Scholar 

  25. Killeen, P. R., Smith, J. P., & Hanson, S. J. (1981). Central place foraging in Rattus norvegicus. Animal Behaviour, 29, 64–70.

    Article  Google Scholar 

  26. Lefebvre, L. (1982). Food exchange strategies in an infant chimpanzee. Journal of Human Evolution, 11, 195–204.

    Article  Google Scholar 

  27. Mazur, J. E. (1987). An adjusting procedure for studying delayed reinforcement: The effects of delay and intervening events on reinforcement value. In M. L. Commons, J. E. Mazur, J. A. Nevin, & H. Rachlin (Eds.), Quantitative analyses of behavior (Vol. 5, pp. 55–73). Hillsdale, NJ: Lawrence Erlbaum.

    Google Scholar 

  28. Mischel, W. (1974). Processes in delay of gratification. In L. Berkowitz (Ed.), Advances in experimental social psychology (pp. 249–292). New York: Academic Press.

    Google Scholar 

  29. Pelé, M., Dufour, V., Micheletta, J., & Thierry, B. (2010). Long-tailed macaques display unexpected waiting abilities in exchange tasks. Animal Cognition, 13, 263–271.

    Article  PubMed  Google Scholar 

  30. Ramseyer, A., Pelé, M., Dufour, V., Chauvin, C., & Thierry, B. (2006). Accepting loss: the temporal limits of reciprocity in brown capuchin monkeys. Proceedings of the Royal Society of London B: Biological Series, 273, 179–184.

    CAS  Article  Google Scholar 

  31. Richards, J. B., Mitchell, S. H., de Wit, H., & Seiden, L. S. (1997). Determination of discount functions in rats with an adjusting-amount procedure. Journal of the Experimental Analysis of Behavior, 67, 353–366.

    CAS  Article  PubMed  Google Scholar 

  32. Rosati, A. G., Stevens, J. R., Hare, B., & Hauser, M. D. (2007). The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults. Current Biology, 17, 1663–1668.

    CAS  Article  PubMed  Google Scholar 

  33. Schino, G., di Giuseppe, F., & Visalberghi, E. (2009). Grooming, rank, and agonistic support in tufted capuchin monkeys. American Journal of Primatology, 71, 101–105.

    Article  PubMed  Google Scholar 

  34. Siegel, S., & Castellan, N. J. (1988). Nonparametric statistics for the behavioral sciences. Singapore: McGraw-Hill.

    Google Scholar 

  35. Stevens, J. R., Hallinan, E. V., & Hauser, M. D. (2005). The ecology and evolution of patience in two New World monkeys. Biology Letters, 1, 223–226.

    Article  PubMed  Google Scholar 

  36. Stevens, J. R., Cushman, F. A., & Hauser, M. D. (2005). Evolving the psychological mechanisms for cooperation. Annual Review of Ecology and Systematics, 36, 499–518.

    Article  Google Scholar 

  37. Thierry, B. (1986). A comparative study of aggression and response to aggression in three species of macaque. In J. G. Else & P. C. Lee (Eds.), Primate ontogeny, cognition, and social behaviour (pp. 307–313). Cambridge: Cambridge University Press.

    Google Scholar 

  38. Thierry, B. (2007). Unity in diversity: lessons from macaque societies. Evolutionary Anthropology, 16, 224–238.

    Article  Google Scholar 

  39. Thierry, B., Aureli, F., Nunn, C., Petit, O., Abegg, C., & de Waal, F. B. M. (2008). A comparative study of conflict resolution in macaques: insights into the nature of trait covariation. Animal Behaviour, 75, 847–860.

    Article  Google Scholar 

  40. Toner, I. J., & Smith, R. A. (1977). Age and overt verbalization in delay-maintenance behavior in children. Journal of Experimental Child Psychology, 24, 123–128.

    Article  Google Scholar 

  41. Toner, I. J., Lewis, B. C., & Gribble, C. M. (1979). Evaluative verbalization and delay maintenance behavior in children. Journal of Experimental Child Psychology, 28, 205–210.

    Article  Google Scholar 

  42. 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.

    Article  Google Scholar 

  43. Westergaard, G. C., Liv, C., Rocca, A. M., Cleveland, A., & Suomi, S. J. (2004). Tufted capuchins (Cebus apella) attribute value to foods and tools during voluntary exchanges with humans. Animal Cognition, 7, 19–24.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank N. Poulin and C. Sueur for statistical advice; A. Delabouglise, C. Dilger, P. Gayet, A. Jacquemin, C. Morin, A. Navarre, F. Vogelweith, M. Plasse, C. Pichon, F.Colas, C.Rosière, and F. Wehrle for their valuable assistance in experiments, and 2 anonymous reviewers whose thoughtful comments greatly improved a previous version of the manuscript. The research was supported by a grant from the Agence Nationale de la Recherche (ANR-08-BLAN-0042-01).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marie Pelé.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 715 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pelé, M., Micheletta, J., Uhlrich, P. et al. Delay Maintenance in Tonkean Macaques (Macaca tonkeana) and Brown Capuchin Monkeys (Cebus apella). Int J Primatol 32, 149–166 (2011). https://doi.org/10.1007/s10764-010-9446-y

Download citation

Keywords

  • Decision-making
  • Delay of gratification
  • Economics
  • Exchange
  • Primates