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.
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
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
Bates E (1976) Language and context: the acquisition of pragmatics. Academic Press, New York
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
Blaschke M, Ettlinger G (1987) Pointing as an act of social communication in monkeys. Anim Behav 35:1520–1523
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
Butterworth G (2001) Joint visual attention in infancy. In: Bremner JG, Fogel A (eds) Blackwell handbook of infant development. Blackwell, Oxford, pp 213–240
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
Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317
Call J, Tomasello M (2007) The gestural communication of apes and monkeys. Lawrence Erlbaum, Mahwah, p 256
De Waal FBM (1982) Chimpanzee politics. Jonathan Cape, London
Drapier M, Chauvin C, Dufour V, Uhlrich P, Thierry B (2005) Food-exchange with humans in brown capuchin monkeys. Primates 46:241–248
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
Gomez J-C (2007) Pointing behaviors in apes and human infants: a balanced interpretation. Child Dev 78:729–734
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
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
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
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
Inoue-Nakamura N, Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psychol 111:159–173
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
Krause MA, Fouts RS (1997) Chimpanzee (Pan troglodytes) pointing: hand shapes, accuracy, and the role of eye gaze. J Comp Psychol 111:330–336
Leavens DA (2004) Manual deixis in apes and humans. Interact Stud 5:387–408
Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822
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
Leavens DA, Hopkins WD, Bard KA (1996) Indexical and referential pointing in chimpanzees (Pan troglodytes). J Comp Psychol 110:346–353
Leavens DA, Hopkins WD, Thomas RK (2004) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57
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
Leavens DA, Russell JL, Hopkins WD (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40
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
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
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
Meunier H, Prieur J, Vauclair J (2013a) Olive baboons communicate intentionally by pointing. Anim Cogn 16:155–163
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
Mitchell RW, Anderson JR (1997) Pointing, withholding information, and deception in capuchin monkeys (Cebus apella). J Comp Psychol 111:351–361
Pika S (2008) Gestures of apes and pre-linguistic human children: similar or different? First Lang 28:116–140
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
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
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
Savage-Rumbaugh ES (1986) Ape language: from conditioned response to symbol. Columbia University Press, New York
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
Vea JJ, Sabater-Pi J (1998) Spontaneous pointing behaviour in the wild pygmy chimpanzee (Pan paniscus). Folia Primatol 69:289–290
Werner H, Kaplan B (1963) Symbol formation: an organismic developmental approach to language and the expression of thought. Wiley, New York
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
Corresponding author
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-015-0841-9