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Capuchin monkeys’ use of human and conspecific cues to solve a hidden object-choice task

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Abstract

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.

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References

  • An YS, Buddhamas K, Newman AE, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2011) Social rank, neophobia and observational learning in black-capped chickadees. Behaviour 148:55–69. doi:10.1163/000579510X545829

    Article  Google Scholar 

  • Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49:201–208. doi:10.1016/0003-3472(95)80168-5

    Article  Google Scholar 

  • Call J (2001) Chimpanzee social cognition. Trends Cogn Sci 5:388–393. doi:10.1016/S1364-6613(00)01728-9

    Article  CAS  PubMed  Google Scholar 

  • Call J, Tomasello M (2005) What chimpanzees know about seeing, revisited: an explanation of the third kind. In: Eilan N, Hoerl C, McCormack T, Roessler J (eds) Joint attention: communication and other minds: issues in philosophy and psychology. Oxford University Press, Oxford, pp 46–64

    Google Scholar 

  • Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3:23–34

    Article  Google Scholar 

  • Clary D, Kelly DM (2013) Are Clark’s nutcrackers (Nucifraga columbiana) able to discriminate knowledge states of human experimenters during an object-choice task? Evol Psychol 11:628–646

    Article  PubMed  Google Scholar 

  • Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2011) Guide for the care and use of laboratory animals, 8th edn. The National Academies Press, Washington, DC

    Google Scholar 

  • Dindo M, Thierry B, Whiten A (2008) Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc Biol Sci 275:187–193. doi:10.1098/rspb.2007.1318

    Article  PubMed  Google Scholar 

  • Galef BG, Wigmore SW (1983) Transfer of information concerning distant foods: a laboratory investigation of the “information-centre” hypothesis. Anim Behav 31:748–758. doi:10.1016/S0003-3472(83)80232-2

    Article  Google Scholar 

  • Gazes RP, Brown EK, Basile BM, Hampton RR (2013) Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory based testing. Anim Cogn 16:445–458. doi:10.1007/s10071-012-0585-8

    Article  PubMed  Google Scholar 

  • Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psychol 113:173–177

    Article  Google Scholar 

  • Hare B, Addessi E, Call J et al (2003) Do capuchin monkeys, Cebus apella, know what conspecifics do and do not see? Anim Behav 65:131–142. doi:10.1006/anbe.2002.2017

    Article  Google Scholar 

  • Highfill LE, Schwammer H, Kuczaj SA (2007) A brief report: the use of experimenter-given cues by South American sea lions. Int J Comp Psychol 20:368–373

    Google Scholar 

  • Itakura S, Anderson JR (1996) Learning to use experimenter-given cues during an object-choice task by a capuchin monkey. Cah Psychol Cogn/Curr Psychol Cogn 15:103–112

    Google Scholar 

  • Itakura S, Agnetta B, Hare B, Tomasello M (1999) Chimpanzee use of human and conspecific social cues to locate hidden food. Dev Sci 2:448–456

    Article  Google Scholar 

  • Judge PG, Bruno S (2012) Transport of functionally appropriate tools by capuchin monkeys (Cebus apella). Am J Primatol 74:199–209. doi:10.1002/ajp.21987

    Article  PubMed  Google Scholar 

  • Judge PG, Essler JL (2013) Capuchin monkeys exercise self-control by choosing token exchange over an immediate reward. Int J Comp Psychol 26:256–266

    Google Scholar 

  • Krueger K, Farmer K, Heinze J (2013) The effects of age, rank and neophobia on social learning in horses. Anim Cogn 17:645–655. doi:10.1007/s10071-013-0696-x

    Article  PubMed  Google Scholar 

  • Marsh HL (2012) Orangutans’ use of contiguous versus distal social and non-social cues in an object-choice task. Int J Comp Psychol 25:299–308. doi:10.5811/westjem.2011.5.6700

    Google Scholar 

  • Mason WA, Hollis JH (1962) Communication between young rhesus monkeys. Anim Behav 10:211–221. doi:10.1016/0003-3472(62)90040-4

    Article  Google Scholar 

  • Miklósi A, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93. doi:10.1007/s10071-005-0008-1

    Article  PubMed  Google Scholar 

  • Mineka S, Cook M (1988) Social learning and the acquisition of snake fear in monkeys. In: Zentall TR, Galef BG (eds) Social learning: psychological and biological perspectives. Lawrence Erlbaum Associates Inc., Publishers, Mahwah, NJ, pp 51–74

    Google Scholar 

  • Morimoto Y, Fujita K (2012) Capuchin monkeys (Cebus apella) use conspecifics’ emotional expressions to evaluate emotional valence of objects. Anim Cogn 15:341–347. doi:10.1007/s10071-011-0458-6

    Article  PubMed  Google Scholar 

  • Nawroth C, Ebersbach M, von Borell E (2013) Juvenile domestic pigs (Sus scrofa domestica) use human-given cues in an object choice task. Anim Cogn 17:1–13. doi:10.1007/s10071-013-0702-3

    Google Scholar 

  • Paukner A, Suomi S, Visalberghi E, Ferrari PF (2009) Capuchin monkeys display affiliation toward humans who imitate them. Science 325:880–883. doi:10.1126/science.1176269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pongrácz P, Vida V, Bánhegyi P, Miklósi Á (2008) How does dominance rank status affect individual and social learning performance in the dog (Canis familiaris)? Anim Cogn 11:75–82. doi:10.1007/s10071-007-0090-7

    Article  PubMed  Google Scholar 

  • Pongrácz P, Bánhegyi P, Miklósi Á (2012) When rank counts—dominant dogs learn better from a human demonstrator in a two-action test. Behaviour 149:111–132. doi:10.1163/156853912X629148

    Article  Google Scholar 

  • Povinelli DJ, Bierschwale DT, Čech CG, Cech CG (1999) Comprehension of seeing as a referential act in young children, but not juvenile chimpanzees. Br J Dev Psychol 17:37–60. doi:10.1348/026151099165140

    Article  Google Scholar 

  • Smet AF, Byrne RW (2013) African elephants can use human pointing cues to find hidden food. Curr Biol 23:2033–2037. doi:10.1016/j.cub.2013.08.037

    Article  CAS  PubMed  Google Scholar 

  • Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New York

    Google Scholar 

  • Tomasello M, Call J, Gluckman A (1997) Comprehension of novel communicative signs by apes and human children. Child Dev 68:1067–1080

    Article  CAS  PubMed  Google Scholar 

  • Tornick JK, Gibson BM, Kispert D, Wilkinson M (2011) Clark’s nutcrackers (Nucifraga columbiana) use gestures to identify the location of hidden food. Anim Cogn 14:117–125. doi:10.1007/s10071-010-0349-2

    Article  PubMed  Google Scholar 

  • Vick SJ, Anderson JR (2000) Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task. J Comp Psychol 114:200–207. doi:10.1037/0735-7036.114.2.200

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The primate facility was supported by Bucknell University. Mary Gavitt and Gretchen Long provided animal care and technical support. Kate Albertini, Chelsea Burleson, Stephanie Casino, Morgan Ramos, Meg Rash, Evan Sloan, Mackenzie Smith, Amari Suskin-Sperry and Eden Wondra assisted with data collection. Jeremy Cain provided graphical and art support on the manuscript. Jennifer Essler was supported by a Bucknell University Graduate Summer Research Fellowship. Lindsay Schwartz was supported by a Bucknell University Undergraduate Summer Research Fellowship. Mattea Rossettie was supported by a Bucknell Geisinger Research Initiative grant: “Social–Cognitive Ability and the Autism Spectrum: Functional Imaging, EEG and Genetic Variation” and by the Bucknell Program for Undergraduate Research Fund.

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Correspondence to Peter G. Judge.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed involving animals were in accordance with the ethical standards of the institution at which the studies were conducted.

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Essler, J.L., Schwartz, L.P., Rossettie, M.S. et al. Capuchin monkeys’ use of human and conspecific cues to solve a hidden object-choice task. Anim Cogn 20, 985–998 (2017). https://doi.org/10.1007/s10071-017-1118-2

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