Skip to main content
SpringerLink
Log in

Tufted capuchins (Cebus apella) adapt their communicative behaviour to human’s attentional states

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Animal communication has become a widely studied field of research, especially because of the associated debates on the origin of human language. Due to their phylogenetic proximity with humans, non-human primates represent a suitable model to investigate the precursors of language. This study focuses on the perception of the attentional states of others, an important prerequisite to intentional communication. We investigated whether capuchins (Cebus apella) produce a learnt pointing gesture towards a hidden and unreachable food reward as a function of the attentional status of the human experimenter. For that purpose, we tested five subjects that we first trained to indicate by a pointing gesture towards the human partner the position of a reward hidden by an assistant. Then, capuchins were tested in two experimental conditions randomly ordered. In the first condition—motivation trial—the experimenter was attentive to the subject gestures and rewarded him immediately when it pointed towards the baited cylinder. During the second condition—test trial—the experimenter adopted one of the following attention states and the subject was rewarded after 10 s has elapsed, regardless of the subject’s behaviour. Five attentional states were tested: (1) experimenter absent, (2) experimenter back to the monkey, (3) experimenter’s head away, (4) experimenter watching above the monkey, and (5) experimenter watching the monkey face. Our results reveal a variation in our subjects’ communicative behaviours with a discrimination of the different postural clues (body and head orientation) available in our experimental conditions. This study suggests that capuchins can flexibly use a communicative gesture to adapt to the attentional state of their partner and provides evidence that acquired communicative gestures of monkeys might be used intentionally.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson JR, Kuwahata H, Fujita K (2007) Gaze alternation during ‘‘pointing’’ by squirrel monkeys (Saimiri sciureus)? Anim Cogn 10:267–271

    Article  PubMed  Google Scholar 

  • Anderson JR, Kuroshima H, Hattori Y, Fujita K (2010) Flexibility in the use of requesting gestures in squirrel monkeys (Saimiri sciureus). Am J Prim 72:707–714

    Article  Google Scholar 

  • Bates E (1976) Language and context: the acquisition of pragmatics. Academic Press, New York

    Google Scholar 

  • Bishop DVM, Ross VA, Daniels MS, Bright P (1996) The measurement of hand preference: a validation study comparing three groups. Br J Psychol 87:269–285

    Article  PubMed  Google Scholar 

  • Blaschke M, Ettlinger G (1987) Pointing as an act of social communication in monkeys. Anim Behav 35:1520–1523

    Article  Google Scholar 

  • Bulloch MJ, Boysen ST, Furlong EE (2008) Visual attention and its relation to knowledge states in chimpanzees, Pan troglodytes. Anim Behav 76(4):1147–1155

    Article  Google Scholar 

  • Butterworth G (2001) Joint visual attention in infancy. In: Bremner JG, Fogel A (eds) Blackwell handbook of infant development. Blackwell, Oxford, pp 213–240

    Google Scholar 

  • Butterworth G (2003) Pointing is the royal road to language for babies. In: Kita S (ed) Pointing: where language, culture, and cognition meet. Erlbaum, Mahwah, pp 9–33

    Google Scholar 

  • Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317

    Article  CAS  PubMed  Google Scholar 

  • Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Lawrence Erlbaum, Mahwah, p 256

    Google Scholar 

  • De Waal FBM (1982) Chimpanzee politics. Jonathan Cape, London

    Google Scholar 

  • 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 

  • Dufour V, Pascalis O, Petit O (2006) Species-specific face recognition in primates, a comparative study in brown capuchin monkeys, tonkean macaques and human. Behav Process 73:107–113

    Article  Google Scholar 

  • Gomez J-C (2007) Pointing behaviors in apes and human infants: a balanced interpretation. Child Dev 78:729–734

    Article  PubMed  Google Scholar 

  • Hattori Y, Kuroshima H, Fujita K (2007) I know you are not looking at me: capuchin monkeys’ (Cebus apella) sensitivity to human attentional states. Anim Cogn 10:141–148

    Article  PubMed  Google Scholar 

  • Hattori Y, Kuroshima H, Fujita K (2010) Tufted capuchin monkeys (Cebus apella) show understanding of human attentional states when requesting food held by a human. Anim Cogn 13:87–92

    Article  PubMed  Google Scholar 

  • Hostetter AB, Cantero M, Hopkins WD (2001) Differential use of vocal and gestural communication in response to the attentional status of a human. J Comp Psychol 115:337–343

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hostetter AB, Russell JL, Freeman H, Hopkins WD (2007) Now you see me, now you don’t: evidence that chimpanzees understand the role of the eyes in attention. Anim Cogn 10:55–62

    Article  PubMed Central  PubMed  Google Scholar 

  • Inoue-Nakamura N, Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psychol 111:159–173

    Article  CAS  PubMed  Google Scholar 

  • Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7:216–223

    Article  PubMed  Google Scholar 

  • Krause MA, Fouts RS (1997) Chimpanzee (Pan troglodytes) pointing: hand shapes, accuracy, and the role of eye gaze. J Comp Psychol 111:330–336

    Article  CAS  PubMed  Google Scholar 

  • Leavens DA (2004) Manual deixis in apes and humans. Interact Stud 5:387–408

    Article  Google Scholar 

  • Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leavens DA, Hopkins WD (1999) The whole-hand point: the structure and function of pointing from a comparative perspective. J Comp Psychol 113:417–425

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leavens DA, Hopkins WD, Bard KA (1996) Indexical and referential pointing in chimpanzees (Pan troglodytes). J Comp Psychol 110:346–353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Leavens DA, Hopkins WD, Thomas RK (2004) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57

    Article  PubMed  Google Scholar 

  • Leavens DA, Russell JL, Hopkins WD (2005) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76:291–306

    Article  PubMed Central  PubMed  Google Scholar 

  • Leavens DA, Russell JL, Hopkins WD (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40

    Article  PubMed Central  PubMed  Google Scholar 

  • Liebal K, Pika S, Call J, Tomasello M (2004) To move or not to move: how apes alter the attentional state of others. Interact Stud 5:199–219

    Article  Google Scholar 

  • Maille A, Engelhart L, Bourjade M, Blois-Heulin C (2012) To beg, or not to beg? That is the question: mangabeys modify their production of requesting gestures in response to human’s attentional states. PLoS ONE 7:e41197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Meunier H, Blois-Heulin C, Vauclair J (2011) A new tool for measuring hand preference in non-human primates: adaptation of Bishop’s quantifying hand preference task for olive baboons. Behav Brain Res 218:1–7

    Article  PubMed  Google Scholar 

  • Meunier H, Prieur J, Vauclair J (2013a) Olive baboons communicate intentionally by pointing. Anim Cogn 16:155–163

    Article  PubMed  Google Scholar 

  • Meunier H, Fagard J, Maugard A, Briseno M, Fizet J, Canteloup C, Defolie C, Vauclair J (2013b) Patterns of hemispheric specialization for a communicative gesture in different primate species. Dev Psychobiol 55:662–671

    Article  PubMed  Google Scholar 

  • Mitchell RW, Anderson JR (1997) Pointing, withholding information, and deception in capuchin monkeys (Cebus apella). J Comp Psychol 111:351–361

    Article  CAS  PubMed  Google Scholar 

  • Pika S (2008) Gestures of apes and pre-linguistic human children: similar or different? First Lang 28:116–140

    Article  Google Scholar 

  • Povinelli DJ, Davis DR (1994) Differences between chimpanzees (Pan troglodytes) and humans (Homo sapiens) in the resting state of the index finger: implications for pointing. J Comp Psychol 108:134–139

    Article  CAS  PubMed  Google Scholar 

  • Povinelli DJ, Bering J, Giambrone S (2003) Chimpanzee ‘pointing’: another error of the argument by analogy? In: Kita S (ed) Pointing: where language, culture, and cognition meet. Erlbaum, Hillsdale, pp 35–68

    Google Scholar 

  • 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 Lond B Biol Sci 273:179–184

    Article  CAS  Google Scholar 

  • Savage-Rumbaugh ES (1986) Ape language: from conditioned response to symbol. Columbia University Press, New York

    Google Scholar 

  • Tomasello M, Call J, Nagell K, Olguin R, Carpenter M (1994) The learning and use of gestural signals by young chimpanzees: a trans-generational study. Primates 37:137–154

    Article  Google Scholar 

  • Vea JJ, Sabater-Pi J (1998) Spontaneous pointing behaviour in the wild pygmy chimpanzee (Pan paniscus). Folia Primatol 69:289–290

    Article  PubMed  Google Scholar 

  • Werner H, Kaplan B (1963) Symbol formation: an organismic developmental approach to language and the expression of thought. Wiley, New York

    Google Scholar 

Download references

Acknowledgments

We thank Nicolas Herrenschmidt for permission to conduct the study at the Centre de Primatologie de l’Université de Strasbourg, France. The authors are grateful to Laurence Böes, Jean-Marc Woock, Adrien Panter and Steve Lapp for their logistical help. Comments on the manuscript from two anonymous referees and the Editor are also acknowledged.

Author information

Authors and Affiliations

  1. Centre de Primatologie de l’Université de Strasbourg, Fort Foch, 67207, Niederhausbergen, France

    Charlotte Defolie, Raphaëlle Malassis, Marion Serre & Hélène Meunier

  2. Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364, Université de Strasbourg, Strasbourg, France

    Hélène Meunier

Authors
  1. Charlotte Defolie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raphaëlle Malassis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marion Serre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hélène Meunier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hélène Meunier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Defolie, C., Malassis, R., Serre, M. et al. Tufted capuchins (Cebus apella) adapt their communicative behaviour to human’s attentional states. Anim Cogn 18, 747–755 (2015). https://doi.org/10.1007/s10071-015-0841-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-015-0841-9

Keywords

Search

Navigation