Advertisement

Animal Cognition

, Volume 18, Issue 2, pp 451–461 | Cite as

Do Tonkean macaques (Macaca tonkeana) tailor their gestural and visual signals to fit the attentional states of a human partner?

  • Charlotte CanteloupEmail author
  • Dalila Bovet
  • Hélène Meunier
Original Paper

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.

Keywords

Intentional communication Social cognition Attention Cues Monkeys 

Notes

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.

References

  1. Anderson JR, Kuwahata H, Fujita K (2007) Gaze alternation during “pointing” by squirrel monkeys (Saimiri sciureus)? Anim Cognit 10:267–271CrossRefGoogle Scholar
  2. Anderson JR, Kuroshima H, Hattori Y, Fujita K (2010) Flexibility in the use of requesting gestures in squirrel monkeys (Saïmiri sciureus). Am J Primatol 72:707–714PubMedCrossRefGoogle Scholar
  3. 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 8:84–92CrossRefGoogle Scholar
  4. Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (1979) The emergence of symbols: cognition and communication in infancy. Academic Press, New YorkGoogle Scholar
  5. 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 87:269–285PubMedCrossRefGoogle Scholar
  6. Blaschke M, Ettlinger G (1987) Pointing as an act of social communication by monkeys. Anim Behav 35(5):1520–1523CrossRefGoogle Scholar
  7. 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 87:121–128Google Scholar
  8. 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
  9. Byrne RW (2000) Evolution of primate cognition. Cognit Sci 24:543–570CrossRefGoogle Scholar
  10. Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317PubMedCrossRefGoogle Scholar
  11. Cartmill EA, Byrne RW (2007) Orangutans modify their gestural signaling according to their audience’s comprehension. Curr Biol 17:1345–1348PubMedCrossRefGoogle Scholar
  12. Cartmill EA, Byrne RW (2010) Semantics of primate gestures: intentional meaning of orangutan gestures. Anim Cognit 13:193–804CrossRefGoogle Scholar
  13. Chance MRA (1967) Attention structure as the basis of primate rank orders. Man 2(4):503–518CrossRefGoogle Scholar
  14. Corballis MC (2002) From hand to mouth. The origins of language. Princeton University Press, PrincetonGoogle Scholar
  15. 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):13997–14002PubMedCentralPubMedCrossRefGoogle Scholar
  16. Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452PubMedCrossRefGoogle Scholar
  17. Franco F, Butterworth G (1996) Pointing and social awareness: declaring and requesting in the second year. J Child Lang 23(2):307–336PubMedCrossRefGoogle Scholar
  18. Genty E, Breuer T, Hobaiter C, Byrne RW (2009) Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cognit 12:527–546CrossRefGoogle Scholar
  19. Goodall J (1968) The behaviour of free-living chimpanzees in the Gombe stream reserve. Anim Behav Monogr 1:163–311Google Scholar
  20. Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cognit 4:269–280CrossRefGoogle Scholar
  21. 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 10:141–148CrossRefGoogle Scholar
  22. 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 13:87–92CrossRefGoogle Scholar
  23. Hewes GW (1973) Primate communication and gestural origin of language. Curr Anthropol 14:5–24CrossRefGoogle Scholar
  24. Hobaiter C, Byrne RW (2011a) The gestural repertoire of the wild chimpanzee. Anim Cognit 14:745–767CrossRefGoogle Scholar
  25. Hobaiter C, Byrne RW (2011b) Serial gesturing by wild chimpanzees: its nature and function for communication. Anim Cognit 14:827–838CrossRefGoogle Scholar
  26. Hobaiter C, Leavens DA, Byrne RW (2014) Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases. J Comp Psychol 128(1):82–87PubMedCrossRefGoogle Scholar
  27. Hopkins WD, Taglialatela JP, Leavens DA (2007) Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim Behav 73:281–286PubMedCentralPubMedCrossRefGoogle Scholar
  28. 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):337–343PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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 10:55–62CrossRefGoogle Scholar
  30. Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behaviour from humans. Anim Cognit 7:216–223CrossRefGoogle Scholar
  31. Krause MA, Fouts RS (1997) Chimpanzee (Pan troglodytes) pointing: hand shapes, accuracy, and the role of eye gaze. J Comp Psychol 111:330–336PubMedCrossRefGoogle Scholar
  32. Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822PubMedCentralPubMedCrossRefGoogle Scholar
  33. Leavens DA, Hopkins WD (1999) The whole-hand point: the structure and function of pointing from a comparative perspective. J Comp Psychol 113(4):417–425PubMedCentralPubMedCrossRefGoogle Scholar
  34. Leavens DA, Hopkins WD, Bard KA (1996) Indexical and referential pointing in Chimpanzees (Pan troglodytes). J Comp Psychol 110:346–353PubMedCentralPubMedCrossRefGoogle Scholar
  35. Leavens DA, Hopkins WD, Thomas RK (2004a) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118(1):48–57PubMedCrossRefGoogle Scholar
  36. Leavens DA, Hostetter AB, Wisley MJ, Hopkins WD (2004b) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 67:467–476CrossRefGoogle Scholar
  37. Leavens DA, Hopkins WD, Bard KA (2005a) Understanding the point of Chimpanzee pointing. Curr Dir Psychol Sci 14:185–189PubMedCentralPubMedCrossRefGoogle Scholar
  38. 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):296–306CrossRefGoogle Scholar
  39. Liebal K, Call J, Tomasello M (2004a) Use of gesture sequences in chimpanzees. Am J Primatol 64:377–396PubMedCrossRefGoogle Scholar
  40. 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 5:199–219CrossRefGoogle Scholar
  41. 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 31:157–167PubMedCrossRefGoogle Scholar
  42. Maestripieri D (1996a) Gestural communication and its cognitive implications in pigtail macaques (Macaca nemestrina). Behaviour 133:997–1022CrossRefGoogle Scholar
  43. Maestripieri D (1996b) Social communication among captive stump-tailed macaques (Macaca arctoides). Int J Primatol 17(5):785–802CrossRefGoogle Scholar
  44. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Matsumoto-Oda A, Tomonaga M (2005) ‘Intentional’ control of sounds production found in the leaf-clipping display of Mahale chimpanzees. Jpn Ethol Soc 23:109–112CrossRefGoogle Scholar
  46. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  47. 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 42:148–153CrossRefGoogle Scholar
  48. 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 218:1–7PubMedCrossRefGoogle Scholar
  49. Meunier H, Fizet J, Vauclair J (2013) Tonkean macaques communicate with their right hand. Brain Lang 126:181–187PubMedCrossRefGoogle Scholar
  50. Micheletta J, Waller BM (2012) Friendship affects gaze following in a tolerant species of macaque, Macaca nigra. Anim Behav 83:459–467CrossRefGoogle Scholar
  51. Nishida T (1980) The leaf-clipping display: a newly-discovered expressive gesture in wild chimpanzees. J Hum Evol 9:117–128CrossRefGoogle Scholar
  52. Partan S, Marler P (1999) Communication goes multimodal. Science 26(283):1272–1273CrossRefGoogle Scholar
  53. 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 223:293–317CrossRefGoogle Scholar
  54. Pika S, Mitani JC (2006) Referential gestural communication in wild chimpanzees (Pan troglodytes). Curr Biol 16:R191–R192PubMedCrossRefGoogle Scholar
  55. Pika S, Liebal K, Tomasello M (2003) Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire, learning and use. Am J Primatol 60:95–111PubMedCrossRefGoogle Scholar
  56. Pika S, Liebal K, Tomasello M (2005) Gestural communication in subadults bonobos (Pan paniscus): repertoire and use. Am J Primatol 65:39–61PubMedCrossRefGoogle Scholar
  57. Povinelli DJ, Eddy TJ (1996) What young chimpanzees know about seeing. Monogr Soc Res Child Dev 61(3):1–152CrossRefGoogle Scholar
  58. Roberts AI, Vick SJ, Buchanan-Smith HM (2012a) Usage and comprehension of manual gestures in wild chimpanzees. Anim Behav 84:459–470CrossRefGoogle Scholar
  59. 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 33:578–589CrossRefGoogle Scholar
  60. Roberts AI, Vick SJ, Buchanan-Smith HM (2013) Communicative intentions in wild chimpanzees: persistence and elaboration in gestural signaling. Anim Cognit 16:187–196CrossRefGoogle Scholar
  61. Roberts AI, Roberts SGB, Vick SJ (2014a) The repertoire and intentionality of gestural communication in wild chimpanzees. Anim Cognit 17:317–336CrossRefGoogle Scholar
  62. Roberts AI, Vick SJ, Roberts SGB, Menzel CR (2014b) Chimpanzees modify intentional gestures to coordinate a search for hidden food. Nat Commun 5:1–8CrossRefGoogle Scholar
  63. Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51PubMedCrossRefGoogle Scholar
  64. Schel AM, Machanda Z, Townsend SW, Zuberbühler K, Slocombe KE (2013a) Chimpanzee food calls are directed at specific individuals. Anim Behav 86:955–965CrossRefGoogle Scholar
  65. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  66. Tempelmann S, Kaminski J, Liebal K (2011) Focus on the essential: all great apes know when others are being attentive. Anim Cognit 14:433–439CrossRefGoogle Scholar
  67. Theall LA, Povinelli DJ (1999) Do chimpanzees tailor their gestural signals to fit the attentional states of others? Anim Cognit 2:207–214CrossRefGoogle Scholar
  68. Tomasello M, Call J (2007) The gestural communication of Apes and monkeys. Lawrence Erlbaum Associates, LondonGoogle Scholar
  69. 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):137–154CrossRefGoogle Scholar
  70. 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 1:223–259CrossRefGoogle Scholar
  71. Tomasello M, Call J, Hare B (1998) Five primate species follow the visual gaze of conspecifics. Anim Behav 55:1063–1069PubMedCrossRefGoogle Scholar
  72. Tomasello M, Hare B, Fogleman T (2001) The ontogeny of gaze following in chimpanzees, Pan troglodytes, and rhesus macaques, Macaca mulatta. Anim Behav 61:335–343CrossRefGoogle Scholar
  73. Tomasello M, Call J, Hare B (2003) Chimpanzees versus humans: it’s not that simple. Trends Cognit Sci 7:239–240CrossRefGoogle Scholar
  74. van Lawick-Goodall J (1967) Mother-offspring relationships in free-ranging chimpanzees. In: Morris D (ed) Primate ethology. Weidenfeld and Nicolson, LondonGoogle Scholar
  75. Vauclair J (2004) Lateralization of communicative signals in nonhuman primates and the hypothesis of the gestural origin of language. Int Stud 5:363–384Google Scholar
  76. Veà JJ, Sabater-Pi J (1998) Spontaneous pointing behaviour in the wild pygmy chimpanzee (Pan paniscus). Folia Primatol 69:289–290PubMedCrossRefGoogle Scholar
  77. 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):209–216PubMedCrossRefGoogle Scholar
  78. 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 12:347–358CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Charlotte Canteloup
    • 1
    • 2
    Email author
  • Dalila Bovet
    • 3
  • Hélène Meunier
    • 1
    • 2
  1. 1.Primatology Centre of Strasbourg UniversityNiederhausbergenFrance
  2. 2.Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364Strasbourg UniversityStrasbourgFrance
  3. 3.Laboratory of Ethology, Cognition, DevelopmentUniversity Paris Ouest Nanterre La DéfenseNanterre CedexFrance

Personalised recommendations