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Do tufted capuchin monkeys play the odds? Flexible risk preferences in Sapajus spp.

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Abstract

As humans, several non-human animal species avoid risk, defined as “variability in rate of gain”. However, non-human primate studies revealed a more complicated picture, with different species ranging from risk aversion to risk proneness. Within an ecological rationality framework, a species’ feeding ecology should influence its risk preferences, as it has been shown in bonobos and chimpanzees. Although the feeding ecology hypothesis is promising, it has not been yet verified in species other than apes. Here, we aimed to assess whether this hypothesis holds true in tufted capuchin monkeys (Sapajus spp.). Ten capuchins were presented with choices between a “safe” option and a “risky” option in three conditions differing for the probability of receiving the larger reward when selecting the risky option. Similarly to chimpanzees, capuchins were risk prone. However, capuchins’ behaviour was not the result of a bias towards the choice of the risky option, since—when facing options with different probabilities of obtaining the larger outcome—they were able to flexibly modify their preferences. Capuchins’ decision-making under risk mirrors their risk-prone behaviour in the wild, where they often rely on unpredictable and/or hazardous food sources, thus satisfying the feeding ecology hypothesis.

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Notes

  1. Recent molecular analysis has revealed that capuchin monkeys, formerly identified as the single genus Cebus, are two genera, with the robust forms now recognized as the genus Sapajus and the gracile forms retained as the genus Cebus (Lynch Alfaro et al. 2012). The nomenclature for Sapajus is registered with ZooBank (urn:lsid:zoobank.org:act:3AAFD645-6B09-4C88-B243-652316B55918). Animals identified as Cebus apella in laboratory colonies outside of South America may be any combination of the several species recognized as separate species from 2001 (Fragaszy et al. 2004), but previously considered C. apella.

References

  • Addessi E (2008) Food variety-seeking in capuchin monkeys. Physiol Behav 93:304–309

    Article  CAS  PubMed  Google Scholar 

  • Addessi E, Rossi S (2011) Tokens improve capuchin performance in the reverse–reward contingency task. Proc R Soc B 278:849–854

    Article  PubMed Central  PubMed  Google Scholar 

  • Addessi E, Crescimbene L, Visalberghi E (2007) Do capuchin monkeys (Cebus apella) use tokens as symbols? Proc R Soc B 247:2579–2585

    Article  Google Scholar 

  • Addessi E, Crescimbene L, Visalberghi E (2008) Food and token quantity discrimination in capuchin monkeys (Cebus apella). Anim Cogn 11:275–282

    Article  PubMed  Google Scholar 

  • 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 83:267–275

    Article  Google Scholar 

  • Addessi E, Paglieri F, Focaroli V (2011) The ecological rationality of delay tolerance: insights from capuchin monkeys. Cognition 119:142–147

    Article  PubMed  Google Scholar 

  • 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 modulate intertemporal choice in capuchin monkeys (Cebus apella), preschool children and adult humans. Cognition 130:428–441

    Article  PubMed  Google Scholar 

  • ASAB/ABS (2014) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 87:I–IX

    Google Scholar 

  • Barraclough DJ, Conroy ML, Lee D (2004) Prefrontal cortex and decision making in a mixed-strategy game. Nat Neurosci 7:404–410

    Article  CAS  PubMed  Google Scholar 

  • Bastiani L, Gori M, Colasante E, Siciliano V, Capitanucci D, Jarre P, Molinaro S (2013) Complex factors and behaviors in the gambling population of Italy. J Gambl Stud 29:1–13

    Article  PubMed  Google Scholar 

  • Caraco T (1981) Energy budgets, risk and foraging preferences in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 8:213–217

    Article  Google Scholar 

  • Chen MK, Lakshminaryanan V, Santos LR (2006) The evolution of our preferences: evidence from capuchin monkey trading behavior. J Polit Econ 114:517–537

    Article  Google Scholar 

  • Estle SJ, Green L, Myerson J, Holt DD (2007) Discounting of monetary and directly consumable rewards. Psychol Sci 18:58–63

    Article  PubMed  Google Scholar 

  • Evans TA, Beran MJ, Harris EH, Rice DF (2009) Quantity judgments of sequentially presented food items by capuchin monkeys (Cebus apella). Anim Cogn 12:97–105

    Article  PubMed  Google Scholar 

  • Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of genus Cebus. Cambridge University Press, Cambridge

    Google Scholar 

  • Gigerenzer G, Todd PM (1999) Simple heuristics that make us smart. Oxford University Press, Oxford

    Google Scholar 

  • Gilby IC, Wrangham RW (2007) Risk-prone hunting by chimpanzees (Pan troglodytes schweinfurthii) increases during periods of high diet quality. Behav Ecol Sociobiol 61:1771–1779

    Article  Google Scholar 

  • Goldstein SJ, Richard AF (1989) Ecology of rhesus macaques (Macaca mulatta) in Northwest Pakistan. Int J Primatol 10:531–567

    Article  Google Scholar 

  • Green L, Myerson J (2009) Experimental and correlational analyses of delay and probability discounting. In: Madden GJ, Bickel WK (eds) Impulsivity: the behavioral and neurological science of discounting. APA Press, Washington, pp 67–92

    Google Scholar 

  • Haun DBM, Nawroth C, Call J (2011) Great apes’ risk taking strategies in a decision making task. PLoS One 6:e2880. doi:10.1371/journal.pone.0028801

    Article  Google Scholar 

  • Hayden BY, Platt ML (2007) Temporal discounting predicts risk sensitivity in rhesus macaques. Curr Biol 17:49–53

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayden BY, Heilbronner SR, Nair AC, Platt ML (2008) Cognitive influences on the risk-seeking by rhesus macaques. Judgm Decis Mak 3:389–395

    PubMed Central  PubMed  Google Scholar 

  • Hayden BY, Heilbronner SR, Platt ML (2010) Ambiguity aversion in rhesus macaques. Front Neurosci 4:166. doi:10.3389/fnins.2010.00166

    Article  PubMed Central  PubMed  Google Scholar 

  • Heilbronner SR, Hayden BY (2013) Contextual factors explain risk-seeking preferences in rhesus monkeys. Front Neurosci 7:7. doi:10.3389/fnins.2013.00007

    Article  PubMed Central  PubMed  Google Scholar 

  • Heilbronner SR, Rosati AG, Stevens JR, Hare B, Hauser MD (2008) A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biol Lett 4:246–249

    Article  PubMed Central  PubMed  Google Scholar 

  • Heilbronner SR, Hayden BY, Platt ML (2011) Decision salience signals in posterior cingulate cortex. Front Neurosci 5:55. doi:10.3389/fnins.2011.00055

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes RN (1997) Intrinsic exploration in animals: motives and measurement. Behav Process 41:213–226

    Article  CAS  Google Scholar 

  • Kacelnik A, Bateson M (1996) Risky theories: the effects of variance on foraging decisions. Am Zool 36:402–434

    Google Scholar 

  • Kacelnik A, El Mouden C (2013) Triumphs and trials of the risk paradigm. Anim Behav 86:1117–1129

    Article  Google Scholar 

  • Kahneman D, Tversky A (1979) Prospect theory: an analysis of decision under risk. Econometrica 47:263–292

    Article  Google Scholar 

  • Lakshminarayanan VR, Chen MK, Santos LR (2011) The evolution of decision-making under risk: framing effects in monkey risk preferences. J Exp Soc Psychol 47:689–693

    Article  Google Scholar 

  • Long AB, Kuhn CM, Platt ML (2009) Serotonin shapes risky decision making in monkeys. Soc Cogn Affect Neurosci 4:346–356

    Article  PubMed Central  PubMed  Google Scholar 

  • Lynch Alfaro JW, Silva JD Jr, Ryland AB (2012) How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. Am J Primatol 74:273–286

    Article  Google Scholar 

  • MacLean EL, Mandalaywala TM, Brannon EM (2012) Variance-sensitive choice in lemurs: constancy trumps quantity. Anim Cogn 15:15–25

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM, Boogert NJ, Brannon EM, Bray EE, Bray J, Brent LJN, Burkart JM, Call J, Cantlon JF, Cheke LG, Clayton NS, Delgado MM, DiVincenti LJ, Fujita K, Herrmann E, Hiramatsu C, Jacobs LF, Jordan KE, Laude JR, Leimgruber KL, Messer EJE, Moura ACA, Ostojić L, Picard A, Platt ML, Plotnik JM, Range F, Reader SM, Reddy RB, Sandel AA, Santos LR, Schumann K, Seed AM, Sewall KB, Shaw RC, Slocombe KE, Su Y, Takimoto A, Tan J, Tao R, van Schaik CP, Virányi Z, Visalberghi E, Wade JC, Watanabe A, Widness J, Young J, Zentall TR, Zhao Y (2014) The evolution of self-control. Proc Natl Acad Sci USA 111:E2140–E2148

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McAlister L, Pessemier EA (1982) Variety seeking behavior: an interdisciplinary review. J Consum Res 9:311–322

    Article  Google Scholar 

  • McCoy AN, Platt ML (2005) Risk-sensitive neurons in macaque posterior cingulate cortex. Nat Neurosci 8:1220–1227

    Article  CAS  PubMed  Google Scholar 

  • Myerson J, Green L, Hanson JS, Holt DD, Estle SJ (2003) Discounting delayed and probabilistic rewards: processes and traits. J Econ Psychol 24:619–635

    Article  Google Scholar 

  • O’Neill M, Schultz W (2010) Coding of reward risk by orbitofrontal neurons is mostly distinct from coding of reward value. Neuron 68:789–800

    Article  PubMed  Google Scholar 

  • Ostaszewski P, Green L, Myerson J (1998) Effect of inflation on the subjective value of delayed and probabilistic rewards. Psychon Bull Rev 5:324–333

    Article  Google Scholar 

  • Perry S, Rose L (1994) Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates 35:409–415

    Article  Google Scholar 

  • Piaget J, Inhelder B (1974) The child’s construction of quantities: conservation and atomism. Basic Books, New York

    Google Scholar 

  • Proctor D, Williamson RA, Latzman RD, de Waal FBM, Brosnan SF (2014) Gambling primates: reactions to a modified Iowa Gambling Task in humans, chimpanzees and capuchin monkeys. Anim Cogn 17:983–995

  • Richard AF, Goldstein SJ, Dewar RE (1989) Weed macaques: the evolutionary implications of macaque feeding ecology. Int J Primatol 10:569–594

    Article  Google Scholar 

  • Rosati AG, Hare B (2012) Decision making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879

    Article  Google Scholar 

  • Rosati AG, Hare B (2013) Chimpanzees and bonobos exhibit emotional responses to decision outcomes. PLoS One 8:e63058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sirianni G, Visalberghi E (2013) Wild bearded capuchins process cashew nuts without contacting caustic compounds. Am J Primatol 75:387–393

    Article  PubMed  Google Scholar 

  • So NY, Stuphorn V (2010) Supplementary eye field encodes option and action value for saccades with variable reward. J Neurophysiol 104:2634–2653

    Article  PubMed Central  PubMed  Google Scholar 

  • Spagnoletti N, Visalberghi E, Verderane MP, Ottoni E, Izar P, Fragaszy D (2012) Stone tool use in wild bearded capuchin monkeys (Cebus libidinosus). Is it a strategy to overcome food scarcity? Anim Behav 83:1285–1294

    Article  Google Scholar 

  • Stephens DW (1981) The logic of risk-sensitive foraging preferences. Anim Behav 29:628–629

    Article  Google Scholar 

  • 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 98–116

    Chapter  Google Scholar 

  • Strait CE, Hayden BY (2013) Preference patterns for skewed gambles in rhesus monkeys. Biol Lett 9:20130902

    Article  PubMed Central  PubMed  Google Scholar 

  • vanMarle K, Aw J, McCrink K, Santos LR (2006) How capuchin monkeys (Cebus apella) quantify objects and substances. J Comp Psychol 20:416–426

    Article  Google Scholar 

  • Visalberghi E, Fragaszy D (2013) The EthoCebus Project. Stone tool use by wild capuchin monkeys. In: Sanz C, Call J, Boesch C (eds) Multidisciplinary perspectives on the cognition and ecology of tool using behaviors. Cambridge University Press, Cambridge, pp 203–222

    Chapter  Google Scholar 

  • von Neumann J, Morgenstern O (1947) Theory of games and economic behaviour. Princeton University Press, Princeton

    Google Scholar 

  • Watson KK, Ghodasra JH, Platt ML (2009) Serotonin transporter genotype modulates social reward and punishment in rhesus macaques. PLoS One 4:e4156

    Article  PubMed Central  PubMed  Google Scholar 

  • Wrangham RW, Peterson D (1996) Demonic males: apes and the origins of human violence. Harvard University Press, Cambridge

    Google Scholar 

  • Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Am J Phys Anthropol Suppl 29:31–72

    Article  Google Scholar 

  • Xu ER, Kralik JD (2014) Risky business: rhesus monkeys exhibit persistent preferences for risky options. Front Psychol 5:258

    PubMed Central  PubMed  Google Scholar 

  • Yamada H, Tymula A, Louie K, Glimcher PW (2013) Thirst-dependent risk preferences in monkeys identify a primitive form of wealth. Proc Natl Acad Sci USA 110:15788–15793

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Maria Bobbio and Luca Marino for help with data collection. We especially thank Fabio Paglieri, Gabriele Schino, and Elisabetta Visalberghi for constructive discussions and valuable comments and Dan Ariely for his fundamental support. 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 Massimiliano Bianchi and Simone Catarinacci for assistance with capuchins. This study was funded by the PNR-CNR Aging Program 2012–2014.

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Authors and Affiliations

  1. Unità di Primatologia Cognitiva e Centro Primati, Istituto di Scienze e Tecnologie della Cognizione, CNR, Rome, Italy

    Francesca De Petrillo, Marialba Ventricelli, Giorgia Ponsi & Elsa Addessi

  2. Dipartimento di Biologia Ambientale, “Sapienza” Università di Roma, Rome, Italy

    Francesca De Petrillo

  3. Dipartimento di Biologia e Biotecnologie “Charles Darwin”, “Sapienza” Università di Roma, Rome, Italy

    Marialba Ventricelli

  4. Dipartimento di Psicologia, “Sapienza” Università di Roma, Rome, Italy

    Giorgia Ponsi

  5. Fondazione Santa Lucia IRCCS, Rome, Italy

    Giorgia Ponsi

Authors
  1. Francesca De Petrillo
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  2. Marialba Ventricelli
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  3. Giorgia Ponsi
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  4. Elsa Addessi
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Correspondence to Elsa Addessi.

Additional information

Francesca De Petrillo and Marialba Ventricelli have contributed equally to this study.

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Supplementary material Movie 1. Experiment 1, Neutral condition. Robin hood, a male capuchin, is presented with the choice between a “safe” option (four food items covered by the white bowl, on the experimenter’s left) and a “risky” option (in this case, one food item covered by the red bowl, on the experimenter’s right). He chooses the “safe” option by inserting his finger in the hole of the corresponding transparent box and the experimenter provides him with the food. (MPG 56796 kb)

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De Petrillo, F., Ventricelli, M., Ponsi, G. et al. Do tufted capuchin monkeys play the odds? Flexible risk preferences in Sapajus spp.. Anim Cogn 18, 119–130 (2015). https://doi.org/10.1007/s10071-014-0783-7

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