Abstract
We tested here whether Tonkean macaques (Macaca tonkeana), trained to produce a pointing gesture, modify their behaviour in response to different human’s attentional states. More specifically, we investigated the macaque’s ability to communicate intentionally about the location of an unreachable hidden food reward in several contexts which differ by the human partner’s attentional state. The experimenter displayed seven attentional states differing on the basis of body, head and gaze orientation. Our study validates several criteria of an intentional communication. We showed that macaques produce more pointing gestures when an audience, i.e. the human partner, is present than absent. We also revealed an adjustment of gaze alternation between the face of the experimenter and the hidden food reward according to several experimental conditions. However, in our study, macaques did not produce auditory attention-getting behaviours when the human partner was inattentive. Finally, only rough cues, i.e. presence, body and face orientation of the observer, seem to be taken into account by macaques. However, our results also supposed the importance of joint attention for macaques since they display more gaze alternation when the head and/or eyes of the human partner are mobile.
Similar content being viewed by others
References
Anderson JR, Kuwahata H, Fujita K (2007) Gaze alternation during “pointing” by squirrel monkeys (Saimiri sciureus)? Anim Cognit 10:267–271
Anderson JR, Kuroshima H, Hattori Y, Fujita K (2010) Flexibility in the use of requesting gestures in squirrel monkeys (Saïmiri sciureus). Am J Primatol 72:707–714
Barth J, Reaux JE, Povinelli DJ (2005) Chimpanzees’ (Pan troglodytes) use of gaze cues in object-choice tasks: different methods yield different results. Anim Cognit 8:84–92
Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (1979) The emergence of symbols: cognition and communication in infancy. Academic Press, New York
Bishop D, Ross V, Daniels M, Bright P (1996) The measurement of hand preference: a validation study comparing three groups of right handers. Br J Psychol 87:269–285
Blaschke M, Ettlinger G (1987) Pointing as an act of social communication by monkeys. Anim Behav 35(5):1520–1523
Bourjade M, Meguerditchian A, Maille A, Vauclair J (2013) Olive baboons, Papio anubis, adjust their visual and auditory intentional gestures to the visual attention of others. Anim Behav 87:121–128
Bourjade M, Canteloup C, Meguerditchian A, Vauclair J, Gaunet F (2014) Training experience in gestures affects the display of social gaze in baboons’ communication with a human. Anim Cognit. doi:10.1007/s10071-014-0793-5
Byrne RW (2000) Evolution of primate cognition. Cognit Sci 24:543–570
Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317
Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348
Cartmill EA, Byrne RW (2010) Semantics of primate gestures: intentional meaning of orangutan gestures. Anim Cognit 13:193–804
Chance MRA (1967) Attention structure as the basis of primate rank orders. Man 2(4):503–518
Corballis MC (2002) From hand to mouth. The origins of language. Princeton University Press, Princeton
Ferrari PF, Kohler E, Fogassi L, Gallese V (2000) The ability to follow eye gaze and its emergence during development in macaque monkeys. PNAS 97(25):13997–14002
Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452
Franco F, Butterworth G (1996) Pointing and social awareness: declaring and requesting in the second year. J Child Lang 23(2):307–336
Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cognit 12:527–546
Goodall J (1968) The behaviour of free-living chimpanzees in the Gombe stream reserve. Anim Behav Monogr 1:163–311
Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cognit 4:269–280
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 Cognit 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 Cognit 13:87–92
Hewes GW (1973) Primate communication and gestural origin of language. Curr Anthropol 14:5–24
Hobaiter C, Byrne RW (2011a) The gestural repertoire of the wild chimpanzee. Anim Cognit 14:745–767
Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cognit 14:827–838
Hobaiter C, Leavens DA, Byrne RW (2014) Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases. J Comp Psychol 128(1):82–87
Hopkins WD, Taglialatela JP, Leavens DA (2007) Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim Behav 73:281–286
Hostetter AB, Cantero M, Hopkins WD (2001) Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). J Comp Psychol 115(4):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 Cognit 10:55–62
Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behaviour from humans. Anim Cognit 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, 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(4):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 (2004a) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118(1):48–57
Leavens DA, Hostetter AB, Wisley MJ, Hopkins WD (2004b) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 67:467–476
Leavens DA, Hopkins WD, Bard KA (2005a) Understanding the point of Chimpanzee pointing. Curr Dir Psychol Sci 14:185–189
Leavens DA, Russell JA, Hopkins WD (2005b) Intentionality as measured in the persistence and elaboration of communication by chimpanzees (Pan troglodytes). Child Dev 76(1):296–306
Liebal K, Call J, Tomasello M (2004a) Use of gesture sequences in chimpanzees. Am J Primatol 64:377–396
Liebal K, Pika S, Call J, Tomasello M (2004b) To move or not to move: how apes alter the attentional state of humans when begging for food. Interact Stud 5:199–219
Liszkowski U, Albrecht K, Carpenter M, Tomasello M (2008) Infants’ visual and auditory communication when a partner is or not visually attending. Infant Behav Dev 31:157–167
Maestripieri D (1996a) Gestural communication and its cognitive implications in pigtail macaques (Macaca nemestrina). Behaviour 133:997–1022
Maestripieri D (1996b) Social communication among captive stump-tailed macaques (Macaca arctoides). Int J Primatol 17(5):785–802
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(7):e41197. doi:10.1371/journal.pone.0041197
Matsumoto-Oda A, Tomonaga M (2005) ‘Intentional’ control of sounds production found in the leaf-clipping display of Mahale chimpanzees. Jpn Ethol Soc 23:109–112
Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford
McGrew WC, Marchant LF, Scott S, Tutin CEG (2001) Intergroup differences in a social custom of wild chimpanzees: the grooming hand-clasp of the Mahale Mountains, Tanzanian. Curr Anthropol 42:148–153
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, Fizet J, Vauclair J (2013) Tonkean macaques communicate with their right hand. Brain Lang 126:181–187
Micheletta J, Waller BM (2012) Friendship affects gaze following in a tolerant species of macaque, Macaca nigra. Anim Behav 83:459–467
Nishida T (1980) The leaf-clipping display: a newly-discovered expressive gesture in wild chimpanzees. J Hum Evol 9:117–128
Partan S, Marler P (1999) Communication goes multimodal. Science 26(283):1272–1273
Perrett DI, Smith PAJ, Potter DD, Mistlin AJ, Head AS, Milner AD, Jeeves MA (1985) Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond Biol Sci 223:293–317
Pika S, Mitani JC (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16:R191–R192
Pika S, Liebal K, Tomasello M (2003) Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire, learning and use. Am J Primatol 60:95–111
Pika S, Liebal K, Tomasello M (2005) Gestural communication in subadults bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61
Povinelli DJ, Eddy TJ (1996) What young chimpanzees know about seeing. Monogr Soc Res Child Dev 61(3):1–152
Roberts AI, Vick SJ, Buchanan-Smith HM (2012a) Usage and comprehension of manual gestures in wild chimpanzees. Anim Behav 84:459–470
Roberts AI, Vick SJ, Roberts SGB, Buchanan-Smith HM, Zuberbühler K (2012b) A structure-based repertoire of manual gestures in wild chimpanzees: statistical analyses of a graded communication system. Evol Hum Behav 33:578–589
Roberts AI, Vick SJ, Buchanan-Smith HM (2013) Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signaling. Anim Cognit 16:187–196
Roberts AI, Roberts SGB, Vick SJ (2014a) The repertoire and intentionality of gestural communication in wild chimpanzees. Anim Cognit 17:317–336
Roberts AI, Vick SJ, Roberts SGB, Menzel CR (2014b) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun 5:1–8
Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51
Schel AM, Machanda Z, Townsend SW, Zuberbühler K, Slocombe KE (2013a) Chimpanzee food calls are directed at specific individuals. Anim Behav 86:955–965
Schel AM, Townsend SW, Machanda Z, Zuberbühler K, Slocombe KE (2013b) Chimpanzee alarm call production meets key criteria for intentionality. PLoS ONE 8(10):e76674. doi:10.1371/journal.pone.0076674
Tempelmann S, Kaminski J, Liebal K (2011) Focus on the essential: all great apes know when others are being attentive. Anim Cognit 14:433–439
Theall LA, Povinelli DJ (1999) Do chimpanzees tailor their gestural signals to fit the attentional states of others? Anim Cognit 2:207–214
Tomasello M, Call J (2007) The gestural communication of Apes and monkeys. Lawrence Erlbaum Associates, London
Tomasello M, Call J, Nagell K, Olguin R, Carpenter M (1994) The learning and the use of gestural signals by young chimpanzees: a trans-generational study. Primates 35(2):137–154
Tomasello M, Call J, Warren J, Frost GT, Carpenter M, Nagell K (1997) The ontogeny of chimpanzee gestural signals: a comparison across groups and generations. Evol Commun 1:223–259
Tomasello M, Call J, Hare B (1998) Five primate species follow the visual gaze of conspecifics. Anim Behav 55:1063–1069
Tomasello M, Hare B, Fogleman T (2001) The ontogeny of gaze following in chimpanzees, Pan troglodytes, and rhesus macaques, Macaca mulatta. Anim Behav 61:335–343
Tomasello M, Call J, Hare B (2003) Chimpanzees versus humans: it’s not that simple. Trends Cognit Sci 7:239–240
van Lawick-Goodall J (1967) Mother-offspring relationships in free-ranging chimpanzees. In: Morris D (ed) Primate ethology. Weidenfeld and Nicolson, London
Vauclair J (2004) Lateralization of communicative signals in nonhuman primates and the hypothesis of the gestural origin of language. Int Stud 5:363–384
Veà JJ, Sabater-Pi J (1998) Spontaneous pointing behaviour in the wild pygmy chimpanzee (Pan paniscus). Folia Primatol 69:289–290
Vick SJ, Anderson JR (2003) Use of human visual attention cues by olive baboons (Papio anubis) in a competitive task. J Comp Psychol 117(2):209–216
Zimmerman F, Zemke F, Call J, Gómez JC (2009) Orangutans (Pongo pygmaeus) and bonobos (Pan paniscus) point to inform a human about the location of a tool. Anim Cognit 12:347–358
Acknowledgments
This study was funded by the Primatology Centre of Strasbourg University. The authors are sincerely grateful to Nicolas Herrenschmidt and his whole team for allowing them to conduct this study at the Primatology Centre of Strasbourg University in France. The authors are particularly thankful to the assistant Myriam Gerardin for helping in data collection during the experiments and to Nicolas Poulin from CeStatS of Strasbourg University, Marie Bourjade from the Aix-Marseille University and Jonas Fizet from the Primatology Centre of Strasbourg University for statistical assistance. Sarah Lux is greatly thanked for her valuable proofreading and correction of the manuscript in English. Authors also thank, on one hand, Nadège Krebs from Noldus for her advices concerning the use of the software The Observer and, on the other hand, the “Conservation Sauvage Internationale” association for providing internship agreement to CC. Finally, the two anonymous reviewers are thanked for their valuable and helpful corrections and commentaries. All the experiments adhered to the current French laws concerning laboratory animal care and were approved by the French ethical committee CREMEAS (Number of agreement for conducting experiments on primates: AL/46/53/02/13).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Canteloup, C., Bovet, D. & Meunier, H. Do Tonkean macaques (Macaca tonkeana) tailor their gestural and visual signals to fit the attentional states of a human partner?. Anim Cogn 18, 451–461 (2015). https://doi.org/10.1007/s10071-014-0814-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-014-0814-4