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Animal Cognition

, Volume 19, Issue 4, pp 819–834 | Cite as

Comparing species decisions in a dichotomous choice task: adjusting task parameters improves performance in monkeys

  • Laurent PrétôtEmail author
  • Redouan Bshary
  • Sarah F. Brosnan
Original Paper

Abstract

In comparative psychology, both similarities and differences among species are studied to better understand the evolution of their behavior. To do so, we first test species in tasks using similar procedures, but if differences are found, it is important to determine their underlying cause(s) (e.g., are they due to ecology, cognitive ability, an artifact of the study, and/or some other factor?). In our previous work, primates performed unexpectedly poorly on an apparently simple two-choice discrimination task based on the natural behavior of cleaner fish, while the fish did quite well. In this task, if the subjects first chose one of the options (ephemeral) they received both food items, but if they chose the other (permanent) option first, the ephemeral option disappeared. Here, we test several proposed explanations for primates’ relatively poorer performance. In Study 1, we used a computerized paradigm that differed from the previous test by removing interaction with human experimenters, which may be distracting, and providing a more standardized testing environment. In Study 2, we adapted the computerized paradigm from Study 1 to be more relevant to primate ecology. Monkeys’ overall performance in these adapted tasks matched the performance of the fish in the original study, showing that with the appropriate modifications they can solve the task. We discuss these results in light of comparative research, which requires balancing procedural similarity with considerations of how the details of the task or the context may influence how different species perceive and solve tasks differently.

Keywords

Decision-making Cues Ecological relevance Labroides dimidiatus Cebus apella Macaca mulatta 

Notes

Acknowledgments

We thank Michael J. Beran for helping with computer programming.

Funding

L.P. was funded by the Swiss Science Foundation (Doc.Mobility) and the Second Century Initiative in Primate Social Cognition, Evolution & Behavior (2CI-PSCEB) at Georgia State University. R.B. was funded by the Swiss Science Foundation. S.F.B. was funded by National Science Foundation Grants SES 1123897 and SES 1425216.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals in this study were followed. All procedures performed in this study were in accordance with the Georgia State University Institutional and Animal Care and Use Committee (capuchins: A13022, rhesus: A13021) and met the standards of the USA.

References

  1. Anderson JR, Degiorgio C, Lamarque C, Fagot J (1996) A multi-task assessment of hand lateralization in capuchin monkeys (Cebus apella). Primates 37:97–103CrossRefGoogle Scholar
  2. Barros RDS, Galvão ODF, Mcilvane WJ (2002) Generalized identity matching-to-sample in Cebus apella. Psychol Rec 52:441–460Google Scholar
  3. Beran MJ (2007) Rhesus monkeys (Macaca mulatta) enumerate sequentially presented sets of items using analog numerical representations. J Exp Psychol Anim B 33:42–54CrossRefGoogle Scholar
  4. Beran MJ (2008) Monkeys (Macaca mulatta and Cebus apella) track, enumerate, and compare multiple sets of moving items. J Exp Psychol Anim B 34:63–74CrossRefGoogle Scholar
  5. Beran MJ, Parrish AE (2012) Sequential responding and planning in capuchin monkeys (Cebus apella). Anim Cogn 15:1085–1094CrossRefPubMedPubMedCentralGoogle Scholar
  6. Beran MJ, Smith JD (2011) Information seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella). Cognition 120:90–105CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beran MJ, Harris EH, Evans TA, Klein ED, Chan B, Flemming TM, Washburn DA (2008a) Ordinal judgments of symbolic stimuli by capuchin monkeys (Cebus apella) and rhesus monkeys (Macaca mulatta): the effects of differential and nondifferential reward. J Comp Psychol 122:52–61CrossRefPubMedGoogle Scholar
  8. Beran MJ, Klein ED, Evans TA, Chan B, Flemming TM, Harris EH, Washburn DA, Rumbaugh DM (2008b) Discrimination reversal learning in capuchin monkeys (Cebus apella). Psychol Rec 58:3–14Google Scholar
  9. Beran MJ, Smith JD, Coutinho MVC, Couchman JJ, Boomer J (2009) The psychological organization of “uncertainty” responses and “middle” responses: a dissociation in capuchin monkeys (Cebus apella). J Exp Psychol Anim B 35:371–381CrossRefGoogle Scholar
  10. Beran MJ, Evans TA, Klein ED, Einstein GO (2012) Rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella) remember future responses in a computerized task. J Exp Psychol Anim B 38:233–243CrossRefGoogle Scholar
  11. Beran MJ, Perdue BM, Smith JD (2014) What are my chances? Closing the gap in uncertainty monitoring between rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella). J Exp Psychol Anim Learn Cogn 40:303–316CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bitterman ME (1960) Toward a comparative psychology of learning. Am Psychol 15:704–712CrossRefGoogle Scholar
  13. Bitterman ME (1965) Phyletic differences in learning. Am Psychol 20:396–410CrossRefPubMedGoogle Scholar
  14. Blanchard TC, Wilke A, Hayden BY (2014) Hot-hand bias in rhesus monkeys. J Exp Psychol Anim Learn Cogn 40:280–286CrossRefPubMedGoogle Scholar
  15. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Taï National Park. Am J Phys Anthropol 78:547–573CrossRefPubMedGoogle Scholar
  16. Boysen ST, Berntson GG (1995) Responses to quantity: perceptual versus cognitive mechanisms in chimpanzees (Pan troglodytes). J Exp Psychol Anim B 21:82–86CrossRefGoogle Scholar
  17. Boysen ST, Berntson GG, Hannan MB, Cacioppa JT (1996) Quantity-based interference and symbolic representations in chimpanzees (Pan troglodytes). J Exp Psychol Anim B 22:76–86CrossRefGoogle Scholar
  18. Boysen ST, Mukobi KL, Berntson GG (1999) Overcoming response bias using symbolic representations of number by chimpanzees (Pan troglodytes). Anim Learn Behav 27:229–235CrossRefGoogle Scholar
  19. Boysen ST, Berntson GG, Mukobi KL (2001) Size matters: impact of size and quantity on array choice by chimpanzees (Pan troglodytes). J Comp Psychol 115:106–110CrossRefPubMedGoogle Scholar
  20. Brosnan SF (2010) What do capuchin monkeys tell us about cooperation? In: Forsyt DR, Hoyt CL (eds) For the greater good of all: perspectives on individualism, society, and leadership. Palgrave Macmillan, Basingstoke, pp 11–28Google Scholar
  21. Brosnan SF, de Waal FBM (2004) Socially learned preferences for differentially rewarded tokens in the brown capuchin monkey (Cebus apella). J Comp Psychol 118:133–139CrossRefPubMedGoogle Scholar
  22. Brosnan SF, Wilson B, Beran MJ (2012) Old World monkeys are more similar to humans than New World monkeys when playing a coordination game. Proc R Soc Lond B Biol Sci 279:1522–1530CrossRefGoogle Scholar
  23. Bshary R (2001) The cleaner fish market. In: Noë R, van Hooff JARAM, Hammerstein P (eds) Economics in nature. Cambridge University Press, Cambridge, pp 146–172CrossRefGoogle Scholar
  24. Bshary R, Grutter AS (2002) Asymmetric cheating opportunities and partner control in the cleaner fish mutualism. Anim Behav 63:547–555CrossRefGoogle Scholar
  25. Bshary R, Schäffer D (2002) Choosy reef fish select cleaner fish that provide high-quality service. Anim Behav 63:557–564CrossRefGoogle Scholar
  26. Chalmeau R, Lardeux K, Brandibas P, Gallo A (1997) Cooperative problem solving by orangutans (Pongo pygmaeus). Int J Primatol 18:23–32CrossRefGoogle Scholar
  27. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Erlbaum, HillsdaleGoogle Scholar
  28. Davison M, Baum WM (2000) Choice in a variable environment: every reinforce counts. J Exper Anal Behav 74:1–24CrossRefGoogle Scholar
  29. de Waal FBM, Leimgruber K, Greenberg AR (2008) Giving is self-rewarding for monkeys. Proc Natl Acad Sci USA 105:13685–13689CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dufour V, Pelé M, Neumann M, Thierry B, Call J (2009) Calculated reciprocity after all: computation behind token transfers in orangutans. Biol Lett 5:172–175CrossRefPubMedPubMedCentralGoogle Scholar
  31. Evans TA, Beran MJ (2012) Monkeys exhibit prospective memory in a computerized task. Cognition 125:131–140CrossRefPubMedPubMedCentralGoogle Scholar
  32. Evans TA, Beran MJ, Chan B, Klein ED, Menzel CR (2008) An efficient computerized testing method for the capuchin monkey (Cebus apella): adaptation of the LRC-CTS to a socially housed nonhuman primate species. Behav Res Methods 40:590–596CrossRefPubMedGoogle Scholar
  33. Fragaszy DM, Visalberghi E, Fedigan LM (2004) The complete capuchin: the biology of the Genus Cebus. Cambridge University Press, CambridgeGoogle Scholar
  34. Galdikas BMF (1988) Orang-utan diet, range, and activity at Tanjung Puting, Central Borneo. Int J Primatol 9:1–35CrossRefGoogle Scholar
  35. Girndt A, Meier T, Call J (2008) Task constraints mask great apes’ ability to solve the trap table task. J Exp Psychol Anim B 34:54–62CrossRefGoogle Scholar
  36. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, CambridgeGoogle Scholar
  37. Gossette RL, Inman N (1966) Comparison of spatial successive discrimination reversal performances of two groups of New World monkeys. Percept Motor Skill 23:169–170CrossRefGoogle Scholar
  38. Grant DA (1946) New statistical criteria for learning and problem solution in experiments involving repeated trials. Psychol Bull 43:272–282CrossRefPubMedGoogle Scholar
  39. Harlow HF (1949) The formation of learning sets. Psychol Rev 56:51–65CrossRefPubMedGoogle Scholar
  40. Harlow HF, Warren JM (1952) Formation and transfer of discrimination learning sets. J Comp Physiol Psychol 45:482–489CrossRefPubMedGoogle Scholar
  41. Kamil AC (1988) Synthetic approach to the study of animal intelligence. In: Leger DW (ed) Comparative perspectives in modern psychology: Nebraska symposium on motivation. University of Nebraska Press, Lincoln, pp 230–257Google Scholar
  42. Kamil AC (1998) On the proper definition of cognitive ethology. In: Balda RP, Bednekoff PA, Kamil AC (eds) Animal cognition in nature. Academic Press, New YorkGoogle Scholar
  43. Masataka N (1990) Handedness of capuchin monkeys. Folia Primatol 55:189–192CrossRefPubMedGoogle Scholar
  44. Mulcahy NJ, Call J (2006) How great apes perform on a modified trap-tube task. Anim Cogn 9:193–199CrossRefPubMedGoogle Scholar
  45. Murray EA, Kralik JD, Wise SP (2005) Learning to inhibit prepotent responses: successful performance by rhesus macaques, Macaca mulatta, on the reversed-contingency task. Anim Behav 69:991–998CrossRefGoogle Scholar
  46. Pepperberg IM, Hartsfield LA (2014) Can Grey parrots (Psittacus erithacus) succeed on a “complex” foraging task failed by nonhuman primates (Pan troglodytes, Pongo abelii, Sapajus apella) but solved by wrasse fish (Labroides dimidiatus)? J Comp Psychol 128:298–306CrossRefPubMedGoogle Scholar
  47. Richardson WK, Washburn DA, Hopkins WD, Savage-Rumbaugh ES, Rumbaugh DM (1990) The NASA/LRC computerized test system. Behav Res Methods Instrum Comput 22:127–131CrossRefPubMedGoogle Scholar
  48. Rijksen HD (1978) A field study on Sumatran orangutans (Pongo pygmaeus abelii Lesson 1827): ecology, behaviour and conservation. H. Veenman Zonen BV, WageningenGoogle Scholar
  49. Rosenthal R (1991) Meta-analytic procedures for social research, 2nd edn. Sage, Newbury Park, p 19CrossRefGoogle Scholar
  50. Rumbaugh DM (1971) Evidence of qualitative differences in learning processes among primates. J Comp Physiol Psychol 76:250–255CrossRefPubMedGoogle Scholar
  51. Rumbaugh DM (1997) Competence, cortex, and primate models: a comparative primate perspective. In: Krasnegor NA, Lyon GR, Goldman-Rakic PS (eds) Development of the prefrontal cortex: evolution, neurobiology, and behavior. Paul H. Brookes, Baltimore, pp 117–139Google Scholar
  52. Salwiczek LH, Prétôt L, Demarta L, Proctor D, Essler J, Pinto AI, Wismer S, Stoinski T, Brosnan SF, Bshary R (2012) Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner-client reef fish cooperation. PLoS ONE 7:e49068CrossRefPubMedPubMedCentralGoogle Scholar
  53. Saverino C, Gerlai R (2008) The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav Brain Res 191:77–87CrossRefPubMedPubMedCentralGoogle Scholar
  54. Schrier AM (1984) Learning how to learn: the significance and current status of learning-set formation. Primates 25:95–102CrossRefGoogle Scholar
  55. Siebeck UE, Litherland L, Wallis GM (2009) Shape learning and discrimination in reef fish. J Exp Biol 212:2112–2118CrossRefGoogle Scholar
  56. Siebeck UE, Parker AN, Sprenger D, Mäthger LM, Wallis G (2010) A species of reef fish that uses ultraviolet patterns for covert face recognition. Curr Biol 20:407–410CrossRefPubMedGoogle Scholar
  57. Timberlake W, Gawley DJ, Lucas GA (1987) Time horizons in rats foraging for food in temporally separated patches. J Exper Anim Behav Proc 13:302–309CrossRefGoogle Scholar
  58. Washburn DA, Rumbaugh DM (1992) Testing primates with joystick-based automated apparatus: lessons from the Language Research Center’s Computerized Test System. Behav Res Methods Instrum Comput 24:157–164CrossRefPubMedGoogle Scholar
  59. Westergaard GC, Suomi SJ (1997) Capuchin monkey (Cebus apella) grips for the use of stone tools. Am J Phys Anthropol 103:131–135CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Laurent Prétôt
    • 1
    Email author
  • Redouan Bshary
    • 2
  • Sarah F. Brosnan
    • 1
    • 3
  1. 1.Department of Psychology, Language Research CenterGeorgia State UniversityAtlantaUSA
  2. 2.Department of Behavioral EcologyUniversity of NeuchâtelNeuchâtelSwitzerland
  3. 3.Department of Philosophy and Neuroscience InstituteGeorgia State UniversityAtlantaUSA

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