Advertisement

Animal Cognition

, Volume 16, Issue 2, pp 155–163 | Cite as

Olive baboons communicate intentionally by pointing

  • Hélène MeunierEmail author
  • J. Prieur
  • J. Vauclair
Original Paper

Abstract

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture’s recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner’s attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter’s attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons’ communicative signalling is discussed.

Keywords

Gestural communication Intentionality Social cognition Non-human primates Papio anubis 

Notes

Acknowledgments

This research was supported by French National Research Agency (ANR) grant number ANR-08-BLAN-0011_01. The authors are sincerely grateful to Anaïs Maugard, Margarita Briseño, Ameline Bardo, Nadège Lechevrel and Pauline Le Sommer for helping with the data collection. The authors would also like to thank Dr Guy Dubreuil for allowing them to conduct the study at the CNRS field station at Rousset-sur-Arc, Jo Di Grandi, Sebastien Guiol, David Pericat and Yannick Autier for their logistical assistance in designing and building the experimental set-up, and all the caretakers for their helpful assistance throughout the study. Thanks are extended to the two anonymous reviewers for their insightful comments on the manuscript and to Elizabeth Portier for correcting the English.

References

  1. Adamson LR (1996) Communication development during infancy. Westview, BoulderGoogle Scholar
  2. Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. An Behav 49:201–208CrossRefGoogle Scholar
  3. Anderson JR, Kuroshima H, Kuwahata H, Fujita K, Vick SJ (2001) Training squirrel monkeys (Saimiri sciureus) to deceive: acquisition and analysis of behavior toward cooperative and competitive trainers. J Comp Psychol 115:282–293PubMedCrossRefGoogle Scholar
  4. Anderson JR, Kuwahata H, Fujita K (2007) Gaze alternation during “pointing” by squirrel monkeys (Saimiri sciureus)? Anim Cogn 10:267–271PubMedCrossRefGoogle Scholar
  5. Anderson JR, Kuroshima H, Hattori Y, Fujita K (2010) Flexibility in the use of requesting gestures in squirrel monkeys (Saimiri sciureus). Am J Prim 72:707–714CrossRefGoogle Scholar
  6. Bakeman R, Adamson LB (1986) Infants’ conventionalized acts: gestures and words with mothers and peers. Infant Behav Dev 9:215–230CrossRefGoogle Scholar
  7. Bard KA (1992) Intentional behavior and intentional communication in young free-ranging orangutans. Child Dev 62:1186–1197CrossRefGoogle Scholar
  8. Bates E (1976) Language and context: the acquisition of pragmatics. Academic Press, New YorkGoogle Scholar
  9. Bates E, Camaioni L, Volterra V (1975) The acquisition of performatives prior to speech. Merrill-Palmer Quart 21:205–226Google Scholar
  10. 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
  11. Bates E, O’Connell B, Shore C (1987) Language and communication in infancy. In: Osofsky J (ed) Handbook of infant development. Wiley, New York, pp 149–203Google Scholar
  12. Bishop DVM, Ross VA, Daniels MS, Bright P (1996) The measurement of hand preference: a validation study comparing three groups. Br J Psychol 87:269–285PubMedCrossRefGoogle Scholar
  13. Blaschke M, Ettlinger G (1987) Pointing as an act of social communication in monkeys. An Behav 35:1520–1523CrossRefGoogle Scholar
  14. Bullinger AF, Zimmermann F, Kaminski J, Tomasello M (2011) Different social motives in the gestural communication of chimpanzees and human children. Dev Sci 14:58–68PubMedCrossRefGoogle Scholar
  15. Butterworth G (2001) Joint visual attention in infancy. In: Bremner JG, Fogel A (eds) Blackwell handbook of infant development. Blackwell, Oxford, pp 213–240Google Scholar
  16. 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 9–33Google Scholar
  17. Byrnit JT (2004) Non-enculturated orangutans’ (Pongo pygmaeus) use of experimenter-given manual and facial cues in an object choice task. J Comp Psychol 118:309–315PubMedCrossRefGoogle Scholar
  18. Byrnit JT (2009) Gorillas’ (Gorilla gorilla) use of experimenter-given manual and facial cues in an object-choice task. Anim Cogn 12:401PubMedCrossRefGoogle Scholar
  19. Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307–317PubMedCrossRefGoogle Scholar
  20. Call J, Tomasello M (1996) The effect of humans on the cognitive development of apes. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, Cambridge, pp 371–403Google Scholar
  21. De Waal FBM (1982) Chimpanzee politics. Jonathan Cape, LondonGoogle Scholar
  22. Franco F, Butterworth G (1996) Pointing and social awareness: declaring and requesting in the second year. J Child Lang 23:307–336PubMedCrossRefGoogle Scholar
  23. Golinkoff RM (1986) “I beg your pardon?”: the preverbal negotiation of failed messages. J Child Lang 13:455–476PubMedCrossRefGoogle Scholar
  24. Golinkoff RM (1993) When is communication a “meeting of minds”? J Child Lang 20:199–207PubMedCrossRefGoogle Scholar
  25. 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 10:141–148PubMedCrossRefGoogle Scholar
  26. 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 13:87–92PubMedCrossRefGoogle Scholar
  27. Hess J, Novak MA, Povinelli DJ (1993) ‘Natural pointing’ in a rhesus monkey, but no evidence of empathy. An Behav 46:1023–1025CrossRefGoogle Scholar
  28. Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802CrossRefGoogle Scholar
  29. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  30. Hopkins WD, Leavens DA (1998) Hand use and gestural communication in chimpanzees (Pan troglodytes). J Comp Psychol 112:95–99PubMedCrossRefGoogle Scholar
  31. 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 115:337–343PubMedCrossRefGoogle Scholar
  32. 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 10:55–62PubMedCrossRefGoogle Scholar
  33. Inoue-Nakamura N, Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pan troglodytes). J Comp Psychol 111:159–173PubMedCrossRefGoogle Scholar
  34. Itakura S, Tanaka M (1998) Use of experimenter-given cues during object-choice tasks by chimpanzees (Pan troglodytes), an orangutan (Pongo pygmaeus), and human infants (Homo sapiens). J Comp Psychol 112:119–126PubMedCrossRefGoogle Scholar
  35. Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7:216–223PubMedCrossRefGoogle Scholar
  36. 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
  37. Kumashiro M, Ishibashi H, Itakura S, Iriki A (2002) Bidirectional communication between a Japanese monkey and a human through eye gaze and pointing. Curr Psychol Cogn 21:3–32CrossRefGoogle Scholar
  38. Leavens DA, Hopkins WD (1998) Intentional communication by chimpanzees: a cross-sectional study of the use of referential gestures. Dev Psychol 34:813–822PubMedCrossRefGoogle Scholar
  39. Leavens DA, Hopkins WD (1999) The whole-hand point: the structure and function of pointing from a comparative perspective. J Comp Psychol 113:417–425PubMedCrossRefGoogle Scholar
  40. Leavens DA, Hopkins WD, Bard KA (1996) Indexical and referential pointing in chimpanzees (Pan troglodytes). J Comp Psychol 110:346–353PubMedCrossRefGoogle Scholar
  41. Leavens DA, Hostetter AB, Wesley MJ, Hopkins WD (2004a) Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Anim Behav 67:467–476CrossRefGoogle Scholar
  42. Leavens DA, Hopkins WD, Thomas RK (2004b) Referential communication by chimpanzees (Pan troglodytes). J Comp Psychol 118:48–57PubMedCrossRefGoogle Scholar
  43. Leavens DA, Russell JL, Hopkins WD (2010) Multimodal communication by captive chimpanzees (Pan troglodytes). Anim Cogn 13:33–40PubMedCrossRefGoogle Scholar
  44. Leung EHL, Rheingold HL (1981) Development of pointing as a social gesture. Dev Psychol 17:215–220CrossRefGoogle Scholar
  45. 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 5:199–219CrossRefGoogle Scholar
  46. Liszkowski U, Carpenter M, Henning A, Striano T, Tomasello M (2004) Twelve-month-olds point to share attention and interest. Dev Sci 7:297–307PubMedCrossRefGoogle Scholar
  47. Lock A (2001) Preverbal communication. In: Bremner JG, Fogel A (eds) Blackwell handbook of infant development. Blackwell, Oxford, pp 379–403Google Scholar
  48. Menzel EW Jr (1973) Leadership and communication in young chimpanzees. In: Menzel EW Jr (ed) Symposia of the Fourth international congress of primatology 1. Precultural primate behavior. Karger, Basel, pp 192–225Google Scholar
  49. 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
  50. Meunier H, Vauclair J, Fagard J (2012) Human infants and baboons show the same pattern of handedness for a communicative gesture. PLoS ONE 7:e33959. doi: 10.1371/journal.pone.0033959 PubMedCrossRefGoogle Scholar
  51. Mitchell RW, Anderson JR (1997) Pointing, withholding information, and deception in capuchin monkeys (Cebus apella). J Comp Psychol 111:351–361PubMedCrossRefGoogle Scholar
  52. Neiworth JJ, Burman MA, Basile BM, Lickteig MT (2002) Use of experimenter-given cues in visual co-orienting and in an object-choice task by a New World monkey species, cotton top tamarins (Saguinus oedipus). J Comp Psychol 116:3–11PubMedCrossRefGoogle Scholar
  53. O’Neill DK (1996) Two-year-old children’s sensitivity to a parent’s knowledge state when making requests. Child Dev 67:659–677CrossRefGoogle Scholar
  54. Peignot P, Anderson JR (1999) Use of experimenter-given manual and facial cues by gorillas (Gorilla gorilla) in an object-choice task. J Comp Psychol 113:253–260CrossRefGoogle Scholar
  55. Pika S (2008) Gestures of apes and pre-linguistic human children: similar or different? First Language 28:116–140CrossRefGoogle Scholar
  56. 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
  57. 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 108:134–139PubMedCrossRefGoogle Scholar
  58. Povinelli DJ, Eddy TJ (1996) Chimpanzees: joint visual attention. Psychol Sci 7:129–135CrossRefGoogle Scholar
  59. 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 35–68Google Scholar
  60. Rolfe L (1999) Theoretical stages in the prehistory of grammar. In: Lock A, Peters CR (eds) Handbook of human symbolic evolution. Blackwell, Oxford, pp 776–792Google Scholar
  61. Russell JL, Braccini S, Buehler N, Kachin MJ, Schapiro SJ, Hopkins WD (2005) Chimpanzee (Pan troglodytes) intentional communication is not contingent upon food. Anim Cogn 8:263–274PubMedCrossRefGoogle Scholar
  62. Savage-Rumbaugh ES (1986) Ape language: from conditioned response to symbol. Columbia University Press, New YorkGoogle Scholar
  63. Sugarman S (1984) The development of preverbal communication: its contribution and limits in promoting the development of language. In: Scheifelbush RL, Pickar J (eds) The acquisition of communicative competence. University Park Press, Baltimore, pp 23–67Google Scholar
  64. Tomasello M (1995) Joint attention as social cognition. In: Moore C, Dunham PJ (eds) Joint attention: its origins and role in development. Erlbaum, Hillsdale, pp 103–130Google Scholar
  65. Tomasello M (1996) Do apes ape? In: Galef BG, Heyes C (eds) Social learning in animals: the roots of culture. Academic Press, New YorkGoogle Scholar
  66. Tomasello M (1999) The cultural origins of human cognition. Harvard University Press, CambridgeGoogle Scholar
  67. 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 37:137–154CrossRefGoogle Scholar
  68. 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. Evolution of Communication 1:223–259CrossRefGoogle Scholar
  69. Veà JJ, Sabater-Pi J (1998) Spontaneous pointing behaviour in the wild pygmy chimpanzee (Pan paniscus). Folia Primatol 69:289–290PubMedCrossRefGoogle Scholar
  70. Vick SJ, Anderson JR (2003) The use of visual orientation cues in a competitive task by Olive baboons (Papio anubis). J Comp Psychol 117:209–216PubMedCrossRefGoogle Scholar
  71. Vick S, Bovet D, Anderson J (2001) Discrimination of gaze cues by olive baboons (Papio anubis). An Cogn 4:1–10CrossRefGoogle Scholar
  72. Werner H, Kaplan B (1963) Symbol formation: an organismic-developmental approach to language and the expression of thought. Wiley, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Primatology Centre of Strasbourg UniversityNiederhausbergenFrance
  2. 2.Research Center in the Psychology of Cognition, Language and EmotionAix-Marseille UniversityAix-en-Provence Cedex 1France
  3. 3.UMR 6552 ETHOSUniversity of Rennes 1PaimpontFrance

Personalised recommendations