Animal Cognition

, Volume 18, Issue 5, pp 1019–1029 | Cite as

When is it worth waiting for? Food quantity, but not food quality, affects delay tolerance in tufted capuchin monkeys

  • Francesca De Petrillo
  • Emanuele Gori
  • Antonia Micucci
  • Giorgia Ponsi
  • Fabio Paglieri
  • Elsa AddessiEmail author
Original Paper


When faced with choices between smaller sooner options and larger later options (i.e. intertemporal choices), both humans and non-human animals discount future rewards. Apparently, only humans consistently show the magnitude effect, according to which larger options are discounted over time at a lower rate than smaller options. Most of the studies carried out in non-human animals led instead to negative results. Here, we tested ten tufted capuchin monkeys (Sapajus spp.) in a delay choice task to evaluate whether they show a magnitude effect when choosing between different quantities of the same food or when the options are represented by high- and low-preferred foods in different conditions. Whereas food quality did not play a role, we provided the first evidence of an effect of the reward amount on temporal preferences in a non-human primate species, a result with potential implications for the validity of comparative studies on the evolution of delay tolerance. In contrast with human results, but as shown in other animal species, capuchins’ choice of the larger later option decreased as the amount of the smaller sooner option increased. Capuchins based their temporal preferences on the quantity of the smaller sooner option, rather than on that of the larger later option, probably because in the wild they virtually never have to choose between the above two options at the same time, but they more often encounter them consecutively. Thus, paying attention to the sooner option and deciding on the basis of its features may be an adaptive strategy rather than an irrational response.


Delay choice task Magnitude effect Food quantity Food quality Non-human primates 



We especially thank Dan Ariely for his fundamental support, Gabriele Schino for statistical advice and Elisabetta Visalberghi for valuable comments on a previous version of the manuscript. We also thank Roma Capitale-Museo Civico di Zoologia and the Fondazione Bioparco for hosting the ISTC-CNR Unit of Cognitive Primatology and Primate Centre, and Arianna Manciocco, Massimiliano Bianchi and Simone Catarinacci for assistance with capuchins. This study was funded by an ISTC-CNR intramural grant to Elsa Addessi and Fabio Paglieri and by the PNR-CNR Aging Program 2012–2014.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Addessi E, Mancini A, Crescimbene L, Padoa-Schioppa L, Visalberghi E (2008) Preference transitivity and symbolic representation in capuchin monkeys (Cebus apella). PLoS One 3(6):e2414. doi: 10.1371/journal.pone.0002414 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Addessi E, Mancini A, Crescimbene L, Ariely D, Visalberghi E (2010) How to spend a token? Trade-offs between food variety and food preference in tufted capuchin monkeys (Cebus apella). Behav Process 83:267–275CrossRefGoogle Scholar
  3. Addessi E, Paglieri F, Focaroli V (2011) The ecological rationality of delay tolerance: insights from capuchin monkeys. Cognition 119:142–147CrossRefPubMedGoogle Scholar
  4. Addessi E, Paglieri F, Beran MJ, Evans TA, Macchitella L, De Petrillo F, Focaroli V (2013) Delay choice vs. delay maintenance: different measures of delayed gratification in capuchin monkeys (Cebus apella). J Comp Psychol 27:392–398CrossRefGoogle Scholar
  5. Addessi E, Bellagamba F, Delfino A, De Petrillo F, Focaroli V, Macchitella L, Maggiorelli V, Pace B, Pecora G, Rossi S, Sbaffi A, Tasselli MI, Paglieri F (2014) Waiting by mistake: symbolic representation of rewards modulates intertemporal choice in capuchin monkeys (Cebus apella), preschool children and adult humans. Cognition 130:428–441CrossRefPubMedGoogle Scholar
  6. Ainslie GW (1974) Impulse control in pigeons. J Exp Anal Behav 21:485–489PubMedCentralCrossRefPubMedGoogle Scholar
  7. Ainslie GW (2001) Breakdown of will. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  8. Amici F, Aureli F, Call J (2008) Fission–fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol 18:1–5CrossRefGoogle Scholar
  9. Anderson JR, Kuroshima H, Fujita K (2010) Delay of gratification in capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus). J Comp Psychol 124:205–210CrossRefPubMedGoogle Scholar
  10. Animal Behavior Society (2012) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 83:301–309CrossRefGoogle Scholar
  11. Auersperg AMI, Laumer IB, Bugnyar T (2013) Goffin cockatoos wait for qualitative and quantitative gains but prefer ‘better’ to ‘more’. Biol Lett 9:1–4CrossRefGoogle Scholar
  12. Baker F, Johnson MW, Bickel WK (2003) Delay discounting in current and never-before cigarette smokers: similarities and differences across commodity, sign, and magnitude. J Abnorm Psychol 112:382–392CrossRefPubMedGoogle Scholar
  13. Beran M (2015) The Comparative Science of “Self-Control”: What Are We Talking About? Front Psychol 6:51PubMedCentralCrossRefPubMedGoogle Scholar
  14. Bramlett JL, Perdue BM, Evans TA, Beran MJ (2012) Capuchin monkeys (Cebus apella) let lesser rewards pass them by to get better rewards. Anim Cogn 15:963–969PubMedCentralCrossRefPubMedGoogle Scholar
  15. Calvert AL, Green L, Myerson J (2010) Delay discounting of qualitatively different reinforcers in rats. J Exp Anal Behav 93:171–184PubMedCentralCrossRefPubMedGoogle Scholar
  16. Chapman GB (1996) Temporal discounting and utility for health and money. J Exp Psychol Learn Mem Cogn 22:771–791CrossRefPubMedGoogle Scholar
  17. Drapier M, Chauvin C, Dufour V, Uhlrich P, Thierry B (2005) Food-exchange with humans in brown capuchin monkeys. Primates 46:241–248CrossRefPubMedGoogle Scholar
  18. Du W, Green L, Myerson J (2002) Cross-cultural comparisons of discounting delayed and probabilistic rewards. Psychol Rec 52:479–492Google Scholar
  19. Estle SJ, Green L, Myerson J, Holt DD (2007) Discounting of monetary and directly consumable rewards. Psychol Sci 18:58–63CrossRefPubMedGoogle Scholar
  20. Evans T, Beran M, Paglieri F, Addessi E (2012) Delaying gratification for food and tokens in capuchin monkeys (Cebus apella) and chimpanzees (Pan troglodytes): when quantity is salient, symbolic stimuli do not improve performance. Anim Cogn 15:539–548CrossRefPubMedGoogle Scholar
  21. Fawcett TW, McNamara JM, Houston AI (2012) When is it adaptive to be patient? A general framework for evaluating delayed rewards. Behav Process 89:128–136CrossRefGoogle Scholar
  22. Ferree M (1973) What is food quality? J Food Distrib Res 4:34–36Google Scholar
  23. Frederick S, Loewenstein G, O’Donoghue T (2002) Time discounting and time preference: a critical review. J Econ Lit 40:350–401CrossRefGoogle Scholar
  24. Freeman KB, Green L, Myerson J, Woolverton WL (2009) Delay discounting of saccharin in rhesus monkeys. Behav Process 82:214–218CrossRefGoogle Scholar
  25. Freeman KB, Nonnemacher JE, Green L, Myerson J, Woolverton WL (2012) Delay discounting in rhesus monkeys: equivalent discounting of more and less preferred sucrose concentrations. Learn Behav 40:54–60CrossRefPubMedGoogle Scholar
  26. Genty E, Karpel H, Silberberg A (2012) Time preferences in long-tailed macaques (Macaca fascicularis) and humans (Homo sapiens). Anim Cogn 15:1161–1172CrossRefPubMedGoogle Scholar
  27. Giordano LA, Bickel WK, Loewenstein G, Jacobs EA, Marsch L, Badger GJ (2002) Mild opioid deprivation increases the degree that opioid-dependent outpatients discount delayed heroin and money. Psychopharmacology 163:174–182CrossRefPubMedGoogle Scholar
  28. Grace RC (1999) The matching law and amount-dependent exponential discounting as accounts of self-control choice. J Exp Anal Behav 71:27–44PubMedCentralCrossRefPubMedGoogle Scholar
  29. Grace RC, Sargisson RJ, White KG (2012) Evidence for a magnitude effect in temporal discounting with pigeons. J Exp Psychol Anim B 38:102–108CrossRefGoogle Scholar
  30. Green L, Myerson J (2004) A discounting framework for choice with delayed and probabilistic rewards. Psychol Bull 130:769–792PubMedCentralCrossRefPubMedGoogle Scholar
  31. Green L, Myerson J (2010) Experimental and correlational analyses of delay and probability discounting. In: Madden GJ, Bickel WK (eds) Impulsivity: the behavioral and neurological science of discounting. American Psychological Association, Washington, pp 67–92CrossRefGoogle Scholar
  32. Green L, Myerson J, McFadden E (1997) Rate of temporal discounting decreases with amount of reward. Mem Cogn 25:717–723CrossRefGoogle Scholar
  33. Green L, Myerson J, Holt DD, Slevin JR, Estle SJ (2004) Discounting of delayed food rewards in pigeons and rats: is there a magnitude effect? J Exp Anal Behav 81:39–50PubMedCentralCrossRefPubMedGoogle Scholar
  34. Hillemann F, Bugnyar T, Kotrschal K, Wascher CAF (2014) Waiting for better, not for more: corvids respond to quality in two delay maintenance tasks. Anim Behav 90:1–10PubMedCentralCrossRefPubMedGoogle Scholar
  35. Kirby KN, Marakovic NN (1996) Delay-discounting probabilistic rewards: rates decrease as amounts increase. Psychon Bull Rev 3:100–104CrossRefPubMedGoogle Scholar
  36. Leonardi RJ, Vick SJ, Dufour V (2012) Waiting for more: the performance of domestic dogs (Canis familiaris) on exchange tasks. Anim Cogn 15:107–120CrossRefPubMedGoogle Scholar
  37. Lynch Alfaro JW, Silva JD Jr, Rylands AB (2012) How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. Am J Primatol 74:273–286CrossRefGoogle Scholar
  38. Oliveira L, Green L, Myerson J (2014) Pigeons’ delay discounting functions established using a concurrent-chains procedure. J Exp Anal Behav 102:151–161CrossRefPubMedGoogle Scholar
  39. Ong EL, White KG (2004) Amount-dependent temporal discounting? Behav Process 66:201–212CrossRefGoogle Scholar
  40. Orduña V, Valencia-Torres L, Cruz G, Bouzas A (2013) Sensitivity to delay is affected by magnitude of reinforcement in rats. Behav Process 98:18–24CrossRefGoogle Scholar
  41. Paglieri F (2013) The costs of delay. Waiting vs. postponing in intertemporal choice. J Exp Anal Behav 99:362–377CrossRefPubMedGoogle Scholar
  42. Paglieri F, Borghi A, Colzato L, Hommel B, Scorolli C (2013a) Heaven can wait. How religion modulates temporal discounting. Psychol Res 77:738–747CrossRefPubMedGoogle Scholar
  43. Paglieri F, Focaroli V, Bramlett J, Tierno V, McIntyre J, Addessi E, Evans T, Beran M (2013b) The hybrid delay task: can capuchin monkeys (Cebus apella) sustain a delay after an initial choice to do so? Behav Process 94:45–54CrossRefGoogle Scholar
  44. Pelé M, Micheletta J, Uhlrich P, Thierry B, Dufour V (2011) Delay maintenance in tonkean macaques (Macaca tonkeana) and brown capuchin monkeys (Cebus apella). Int J Primatol 32:149–166CrossRefGoogle Scholar
  45. Rabe-Hesketh S, Skrondal A (2008) Multilevel and longitudinal modelling using Stata, 2nd edn. Stata Press, Lakeway Drive College Station, pp 229–275Google Scholar
  46. Rachlin H (1971) On the tautology of the matching law. J Exp Anal Behav 15:249–251PubMedCentralCrossRefPubMedGoogle Scholar
  47. Ramseyer A, Pelé M, Dufour V, Chauvin C, Thierry B (2006) Accepting loss: the temporal limits of reciprocity in brown capuchin monkeys. Proc R Soc B 273:179–184PubMedCentralCrossRefPubMedGoogle Scholar
  48. Richards JB, Mitchell SH, de Wit H, Seiden LS (1997) Determination of discount functions in rats with an adjusting-amount procedure. J Exp Anal Behav 67:353–366PubMedCentralCrossRefPubMedGoogle Scholar
  49. Snijders TAB, Bosker RJ (1999) Multilevel analysis: an introduction to basic and advanced multilevel modeling. Sage, LondonGoogle Scholar
  50. Stephens DW (2002) Discrimination, discounting and impulsivity: a role for informational constraint. Philos Trans R Soc Lond B 357:1527–1537CrossRefGoogle Scholar
  51. Stevens JR (2010) Rational decision making in primates: the bounded and the ecological. In: Platt ML, Ghazanfar AA (eds) Primate neuroethology. Oxford University Press, Oxford, pp 98–116CrossRefGoogle Scholar
  52. Stevens JR (2014) Evolutionary pressures on primate intertemporal choice. Proc R Soc B 281:20140499PubMedCentralCrossRefPubMedGoogle Scholar
  53. Stevens JR, Mühlhoff N (2012) Intertemporal choice in lemurs. Behav Process 89:121–127CrossRefGoogle Scholar
  54. Stevens JR, Stephens DW (2009) The adaptive nature of impulsivity. In: Madden GJ, Bickel WK (eds) Impulsivity: the behavioral and neurological science of discounting. American Psychological Association, Washington, pp 361–387Google Scholar
  55. Stevens JR, Rosati AG, Ross KR, Hauser MD (2005) Will travel for food: spatial discounting in two new world monkeys. Curr Biol 15:1855–1860CrossRefPubMedGoogle Scholar
  56. Tan C, Johnson R (1996) To wait or not to wait: The influence of culture on discounting behavior. In: Loke W (ed) Perspectives on judgment and decision making. Scarecrow Press, Maryland, pp 297–305Google Scholar
  57. Van De Pol M, Wright J (2009) A simple method for distinguishing within-versus between-subject effects using mixed models. Anim Behav 77:753–758CrossRefGoogle Scholar
  58. Ventricelli M, Focaroli V, De Petrillo F, Macchitella L, Paglieri F, Addessi E (2013) How capuchin monkeys (Cebus apella) behaviourally cope with increasing delay in a self-control task. Behav Process 100:146–152CrossRefGoogle Scholar
  59. Wascher CAF, Dufour V, Bugnyar T (2012) Carrion crows cannot overcome impulsive choice in a quantitative exchange task. Front Psychol 3:118. doi: 10.3389/fpsyg.2012.00118 PubMedCentralCrossRefPubMedGoogle Scholar
  60. Wogar MA, Bradshaw CM, Szabadi E (1992) Choice between delayed reinforcements in an adjusting-delay schedule: the effects of absolute reinforcement size and deprivation level. Q J Exp Psychol 45B:1–13Google Scholar
  61. Woolverton WL, Myerson J, Green L (2007) Delay discounting of cocaine by rhesus monkeys. Exp Clin Psychopharmacol 15:238–244PubMedCentralCrossRefPubMedGoogle Scholar
  62. Yuki S, Okanoya K (2014) Relatively high motivation for context-evoked reward produces the magnitude effect in rats. Behav Proc 107:22–28CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Francesca De Petrillo
    • 1
    • 2
  • Emanuele Gori
    • 1
    • 3
  • Antonia Micucci
    • 1
    • 4
  • Giorgia Ponsi
    • 1
    • 5
  • Fabio Paglieri
    • 6
  • Elsa Addessi
    • 1
    Email author
  1. 1.Unit of Cognitive Primatology and Primate Center, Istituto di Scienze e Tecnologie della CognizioneCNRRomeItaly
  2. 2.Dipartimento di Biologia AmbientaleSapienza Università di RomaRomeItaly
  3. 3.Dipartimento di Scienze della TerraSapienza Università di RomaRomeItaly
  4. 4.Dipartimento di BiologiaUniversità degli Studi di FirenzeSesto FiorentinoItaly
  5. 5.Dipartimento di PsicologiaSapienza Università di RomaRomeItaly
  6. 6.Goal-Oriented Agents Lab, Istituto di Scienze e Tecnologie della CognizioneCNRRomeItaly

Personalised recommendations