Animal Cognition

, Volume 21, Issue 5, pp 715–728 | Cite as

Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention

  • Fumihiro KanoEmail author
  • Richard Moore
  • Christopher Krupenye
  • Satoshi Hirata
  • Masaki Tomonaga
  • Josep Call
Original Paper


The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.


Domestication Gaze following Great ape Ostensive signals Referential communication 



We thank Naruki Morimura, Yutaro Sato, Ruiting Song and the staff at Kumamoto Sanctuary, Primate Research Institute, Kyoto University Institute for Advanced Study, and Wolfgang Kohler Primate Research Center for their assistance in conducting the series of experiments. We also thank two anonymous reviewers for their helpful comments. Financial support came from Ministry of Education, Culture, Sports, Science and Technology [K-CONNEX to FK], Japan Society for Promotion of Science KAKENHI 26885040, 16K21108, and 18H05072 to FK, 26245069, 16H06301, 16H06283, and 18H05524 to SH, 15H05709, 16H06238, and JSPS-CCSN to MT, and JSPS-LGP-U04 and Great Ape Information Network to SH and MT, and the European Research Council [SOMICS 609819 to JC].

Supplementary material

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  1. Behne T, Carpenter M, Tomasello M (2005) One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Dev Sci 8:492–499. CrossRefPubMedGoogle Scholar
  2. Behne T, Liszkowski U, Carpenter M, Tomasello M (2012) Twelve-month-olds’ comprehension and production of pointing. Br J Dev Psychol 30:359–375. CrossRefPubMedGoogle Scholar
  3. Bräuer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119:145–154. CrossRefPubMedGoogle Scholar
  4. Bugnyar T, Stöwe M, Heinrich B (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc R Soc Lond Ser B Biol Sci 271:1331–1336. CrossRefGoogle Scholar
  5. Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307. CrossRefPubMedGoogle Scholar
  6. 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, New York, pp 371–403Google Scholar
  7. Call J, Tomasello M (2008) Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12:187–192. CrossRefPubMedGoogle Scholar
  8. Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3:23–34. CrossRefGoogle Scholar
  9. Cooper RP, Aslin RN (1990) Preference for infant directed speech in the first month after birth. Child Dev 61:1584–1595. CrossRefPubMedGoogle Scholar
  10. Csibra G (2010) Recognizing communicative intentions in infancy. Mind Lang 25:141–168. CrossRefGoogle Scholar
  11. Csibra G, Gergely G (2009) Natural pedagogy. Trends Cogn Sci 13:148–153. CrossRefPubMedGoogle Scholar
  12. De Waal FB (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251. CrossRefGoogle Scholar
  13. De Waal FBM (1990) Peacemaking among primates. Harvard University Press, CambridgeGoogle Scholar
  14. Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. CrossRefPubMedGoogle Scholar
  15. Farroni T, Csibra G, Simion F, Johnson MH (2002) Eye contact detection in humans from birth. Proc Nat Acad Sci 99:9602. CrossRefPubMedGoogle Scholar
  16. Gergely G, Csibra G (2006) Sylvia’s recipe: the role of imitation and pedagogy in the transmission of cultural knowledge. In: Enfield N, Levenson SC (eds) Roots of human sociality: culture, cognition, and human interaction. Berg, Oxford, pp 229–255Google Scholar
  17. Gergely G, Egyed K, Király I (2007) On pedagogy. Dev Sci 10:139–146. CrossRefPubMedGoogle Scholar
  18. Gomez JC (1996) Ostensive behavior in great apes: the role of eye contact. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, New York, pp 131–151Google Scholar
  19. Gredebäck G, Astor K, Fawcett C (2018) Gaze following is not dependent on ostensive cues: a critical test of natural pedagogy. Child dev. (in press) PubMedCrossRefGoogle Scholar
  20. Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psychol 113:173. CrossRefGoogle Scholar
  21. Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581. CrossRefGoogle Scholar
  22. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. CrossRefPubMedGoogle Scholar
  23. Hattori Y, Kano F, Tomonaga M (2010) Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study. Biology Lett 6:610–613. CrossRefGoogle Scholar
  24. Herrmann E, Tomasello M (2006) Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Dev Sci 9:518–529. CrossRefPubMedGoogle Scholar
  25. Heyes C (2016) Born pupils? Natural pedagogy and cultural pedagogy. Perspect Psychol Sci 11:280–295. CrossRefPubMedGoogle Scholar
  26. Hirata S, Fuwa K, Sugama K, Kusunoki K, Fujita S (2010) Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes. Anim Cogn 13:679–688. CrossRefPubMedGoogle Scholar
  27. Hoicka E (2016) Parents and toddlers distinguish joke, pretend and literal intentional contexts through communicative and referential cues. J Pragmat 95:137–155. CrossRefGoogle Scholar
  28. Kaminski J, Schulz L, Tomasello M (2012) How dogs know when communication is intended for them. Dev Sci 15:222–232. CrossRefPubMedGoogle Scholar
  29. Kano F, Call J (2014a) Cross-species variation of gaze following and conspecific preference among great apes human infants adults. Anim Behav 91:137–150. CrossRefGoogle Scholar
  30. Kano F, Call J (2014b) Great apes generate goal-based action predictions: an eye-tracking study. Psychol Sci 25:1691–1698. CrossRefPubMedGoogle Scholar
  31. Kano F, Tomonaga M (2009) How chimpanzees look at pictures: a comparative eye-tracking study. Proc Roy Soc B 276:1949–1955. CrossRefGoogle Scholar
  32. Kano F, Hirata S, Call J, Tomonaga M (2011) The visual strategy specific to humans among hominids: a study using the gap-overlap paradigm. Vis Res 51:2348–2355. CrossRefPubMedGoogle Scholar
  33. Kano F, Call J, Tomonaga M (2012) Face and eye scanning in gorillas, orangutans, and humans: unique eye-viewing patterns in humans among hominids. J Comp Psychol 126:388–398. CrossRefPubMedGoogle Scholar
  34. Kano F, Hirata S, Call J (2015) Social attention in Pan: bonobos exhibit more eye contacts than chimpanzees. PLoS One 10:e0129684. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kano F, Krupenye C, Hirata S, Call J (2017) Eye tracking uncovered great apes’ ability to anticipate that other individuals will act according to false beliefs. Commun Integr Biol 10:e1299836. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kano F, Shepherd SV, Hirata S, Call J (2018) Primate social attention: species differences and effects of individual experience in humans, great apes, and macaques. PLoS One 13:e0193283. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Krupenye C, Kano F, Hirata S, Call J, Tomasello M (2016) Great apes anticipate that other individuals will act according to false beliefs. Science 354:110–114. CrossRefPubMedGoogle Scholar
  38. Liebal K, Call J (2012) The origins of non-human primates’ manual gestures. Philos Trans R Soc Lond B Biol Sci 367:118–128. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lyn H, Russell JL, Hopkins WD (2010) The impact of environment on the comprehension of declarative communication in apes. Psychol Sci 21:360–365. CrossRefPubMedGoogle Scholar
  40. Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121. CrossRefPubMedGoogle Scholar
  41. Moore R (2016) Meaning and ostension in great ape gestural communication. Anim Cogn 19:223–231. CrossRefPubMedGoogle Scholar
  42. Moore R (2017) Gricean communication and cognitive development. Philos Q 67:303–326. CrossRefGoogle Scholar
  43. Moore R, Liebal K, Tomasello M (2013) Three-year-olds understand communicative intentions without language, gestures or gaze. Interact Stud 14:62–80. CrossRefGoogle Scholar
  44. Moore R, Call J, Tomasello M (2015a) Production and comprehension of gestures between orang-utans (Pongo pygmaeus) in a referential communication game. PloS One 10:e0129726. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Moore R, Mueller B, Kaminski J, Tomasello M (2015b) Two-year-old children but not domestic dogs understand communicative intentions without language, gestures or gaze. Dev Sci 18:232–242. CrossRefPubMedGoogle Scholar
  46. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:113–124. CrossRefGoogle Scholar
  47. Okamoto-Barth S, Call J, Tomasello M (2007) Great apes’ understanding of other individuals’ line of sight. Psychol Sci 18:462–468. CrossRefPubMedGoogle Scholar
  48. Parr LA, Dove T, Hopkins WD (1998) Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn Neurosci 10:615–622. CrossRefPubMedGoogle Scholar
  49. Riedel J, Schumann K, Kaminski J, Call J, Tomasello M (2008) The early ontogeny of human–dog communication. Anim Behav 75:1003–1014. CrossRefGoogle Scholar
  50. Scott-Phillips TC (2015a) Meaning in animal and human communication. Anim Cogn 18:801–805. CrossRefPubMedGoogle Scholar
  51. Scott-Phillips TC (2015b) Nonhuman primate communication, pragmatics, and the origins of language. Curr Anthropol 56:56–80. CrossRefGoogle Scholar
  52. Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18:668–671. CrossRefPubMedGoogle Scholar
  53. Senju A, Csibra G (2014) A commentary by Csibra, Senju, et al. on gaze following. Retrieved 1 Jul 2018
  54. Sperber D, Wilson D (1995) Relevance: communication and cognition, 2nd edn. Blackwell, OxfordGoogle Scholar
  55. Szufnarowska J, Rohlfing KJ, Fawcett C, Gredebäck G (2014) Is ostension any more than attention? Sci Rep 4:5304. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Téglás E, Gergely A, Kupán K, Miklósi Á, Topál J (2012) Dogs’ gaze following is tuned to human communicative signals. Curr Biol 22:209–212. CrossRefPubMedGoogle Scholar
  57. Tennie C, Call J, Tomasello M (2009) Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans R Soc B Biol Sci 364:2405–2415. CrossRefGoogle Scholar
  58. Tomasello M (1999) The cultural origins of human cognition. Harvard University Press, CambridgeGoogle Scholar
  59. Tomasello M (2006) Why don’t apes point? In: Enfield N, Levinson SC (eds) Roots of human sociality: culture, cognition, and interaction, vol 197. Berg, London, pp 506–524Google Scholar
  60. Tomasello M, Hare B, Lehmann H, Call J (2007) Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis. J Hum Evol 52:314–320. CrossRefPubMedGoogle Scholar
  61. Tomonaga M (1999) Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes). Primates 40:417–438. CrossRefGoogle Scholar
  62. Topál J, Gergely G, Erdőhegyi Á, Csibra G, Miklósi Á (2009) Differential sensitivity to human communication in dogs wolves human infants. Science 325:1269–1272. CrossRefPubMedGoogle Scholar
  63. Topál J, Kis A, Oláh K (2014) Dogs’ sensitivity to human ostensive cues: a unique adaptation. In: Kaminski J, Marshall-Pescini S (eds) The social dog: behavior and cognition. Elsevier, New York, pp 319–346Google Scholar
  64. Ueno A et al (2010) Brain activity in an awake chimpanzee in response to the sound of her own name. Biol Lett 6:311–313. CrossRefPubMedGoogle Scholar
  65. Virányi Z, Gácsi M, Kubinyi E, Topál J, Belényi B, Ujfalussy D, Miklósi Á (2008) Comprehension of human pointing gestures in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373. CrossRefPubMedGoogle Scholar
  66. Vorms M (2012) A-not-B errors: testing the limits of natural pedagogy theory. Rev Philos Psychol 3:525–545. CrossRefGoogle Scholar
  67. Whiten A, McGuigan N, Marshall-Pescini S, Hopper LM (2009) Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Philos Trans R Soc Lond B Biol Sci 364:2417–2428. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yamagiwa J (1992) Functioinal analysis of social staring behavior in an all-male group of mountain gorillas. Primates 33:523–544. CrossRefGoogle Scholar
  69. Yamamoto S, Humle T, Tanaka M (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc Natl Acad Sci 109:3588–3592. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Kumamoto SanctuaryKyoto UniversityKumamotoJapan
  2. 2.Berlin School of Mind and BrainHumboldt-Universität zu BerlinBerlinGermany
  3. 3.Department of Developmental and Comparative PsychologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany
  4. 4.School of Psychology and NeuroscienceUniversity of St. AndrewsSt. AndrewsUK
  5. 5.Primate Research InstituteKyoto UniversityInuyamaJapan

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