Abstract
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.
This is a preview of subscription content, access via your institution.
References
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. https://doi.org/10.1111/j.1467-7687.2005.00440.x
Behne T, Liszkowski U, Carpenter M, Tomasello M (2012) Twelve-month-olds’ comprehension and production of pointing. Br J Dev Psychol 30:359–375. https://doi.org/10.1111/j.2044-835X.2011.02043.x
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. https://doi.org/10.1037/0735-7036.119.2.145
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. https://doi.org/10.1098/rspb.2004.2738
Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307. https://doi.org/10.1037//0735-7036.108.4.307
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 371–403
Call J, Tomasello M (2008) Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12:187–192. https://doi.org/10.1016/j.tics.2008.02.010
Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3:23–34. https://doi.org/10.1007/s100710050047
Cooper RP, Aslin RN (1990) Preference for infant directed speech in the first month after birth. Child Dev 61:1584–1595. https://doi.org/10.1111/j.1467-8624.1990.tb02885.x
Csibra G (2010) Recognizing communicative intentions in infancy. Mind Lang 25:141–168. https://doi.org/10.1111/j.1468-0017.2009.01384.x
Csibra G, Gergely G (2009) Natural pedagogy. Trends Cogn Sci 13:148–153. https://doi.org/10.1016/j.tics.2009.01.005
De Waal FB (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251. https://doi.org/10.1163/156853988X00269
De Waal FBM (1990) Peacemaking among primates. Harvard University Press, Cambridge
Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. https://doi.org/10.1016/S0149-7634(00)00025-7
Farroni T, Csibra G, Simion F, Johnson MH (2002) Eye contact detection in humans from birth. Proc Nat Acad Sci 99:9602. https://doi.org/10.1073/pnas.152159999
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 229–255
Gergely G, Egyed K, Király I (2007) On pedagogy. Dev Sci 10:139–146. https://doi.org/10.1111/j.1467-7687.2007.00576.x
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 131–151
Gredebäck G, Astor K, Fawcett C (2018) Gaze following is not dependent on ostensive cues: a critical test of natural pedagogy. Child dev. https://doi.org/10.1111/cdev.13026 (in press)
Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psychol 113:173. https://doi.org/10.1037//0735-7036.113.2.173
Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581. https://doi.org/10.1016/j.anbehav.2003.11.011
Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. https://doi.org/10.1126/science.1072702
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. https://doi.org/10.1098/rsbl.2010.0120
Herrmann E, Tomasello M (2006) Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Dev Sci 9:518–529. https://doi.org/10.1111/j.1467-7687.2006.00519.x
Heyes C (2016) Born pupils? Natural pedagogy and cultural pedagogy. Perspect Psychol Sci 11:280–295. https://doi.org/10.1177/1745691615621276
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. https://doi.org/10.1007/s10071-010-0316-y
Hoicka E (2016) Parents and toddlers distinguish joke, pretend and literal intentional contexts through communicative and referential cues. J Pragmat 95:137–155. https://doi.org/10.1016/j.pragma.2015.10.010
Kaminski J, Schulz L, Tomasello M (2012) How dogs know when communication is intended for them. Dev Sci 15:222–232. https://doi.org/10.1111/j.1467-7687.2011.01120.x
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. https://doi.org/10.1016/j.anbehav.2014.03.011
Kano F, Call J (2014b) Great apes generate goal-based action predictions: an eye-tracking study. Psychol Sci 25:1691–1698. https://doi.org/10.1177/0956797614536402
Kano F, Tomonaga M (2009) How chimpanzees look at pictures: a comparative eye-tracking study. Proc Roy Soc B 276:1949–1955. https://doi.org/10.1098/rspb.2008.1811
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. https://doi.org/10.1016/j.visres.2011.09.006
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. https://doi.org/10.1037/a0029615
Kano F, Hirata S, Call J (2015) Social attention in Pan: bonobos exhibit more eye contacts than chimpanzees. PLoS One 10:e0129684. https://doi.org/10.1371/journal.pone.0129684
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. https://doi.org/10.1080/19420889.2017.1299836
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. https://doi.org/10.1371/journal.pone.0193283
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. https://doi.org/10.1126/science.aaf8110
Liebal K, Call J (2012) The origins of non-human primates’ manual gestures. Philos Trans R Soc Lond B Biol Sci 367:118–128. https://doi.org/10.1098/rstb.2011.0044
Lyn H, Russell JL, Hopkins WD (2010) The impact of environment on the comprehension of declarative communication in apes. Psychol Sci 21:360–365. https://doi.org/10.1177/0956797610362218
Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121. https://doi.org/10.1007/s100710050016
Moore R (2016) Meaning and ostension in great ape gestural communication. Anim Cogn 19:223–231. https://doi.org/10.1007/s10071-015-0905-x
Moore R (2017) Gricean communication and cognitive development. Philos Q 67:303–326. https://doi.org/10.1093/pq/pqw049
Moore R, Liebal K, Tomasello M (2013) Three-year-olds understand communicative intentions without language, gestures or gaze. Interact Stud 14:62–80. https://doi.org/10.1075/is.14.1.05moo
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. https://doi.org/10.1371/journal.pone.0129726
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. https://doi.org/10.1111/desc.12206
Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:113–124. https://doi.org/10.1016/S0010-0277(03)00071-4
Okamoto-Barth S, Call J, Tomasello M (2007) Great apes’ understanding of other individuals’ line of sight. Psychol Sci 18:462–468. https://doi.org/10.1111/j.1467-9280.2007.01922.x
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. https://doi.org/10.1162/089892998563013
Riedel J, Schumann K, Kaminski J, Call J, Tomasello M (2008) The early ontogeny of human–dog communication. Anim Behav 75:1003–1014. https://doi.org/10.1016/j.anbehav.2007.08.010
Scott-Phillips TC (2015a) Meaning in animal and human communication. Anim Cogn 18:801–805. https://doi.org/10.1007/s10071-015-0845-5
Scott-Phillips TC (2015b) Nonhuman primate communication, pragmatics, and the origins of language. Curr Anthropol 56:56–80. https://doi.org/10.1086/679674
Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18:668–671. https://doi.org/10.1016/j.cub.2008.03.059
Senju A, Csibra G (2014) A commentary by Csibra, Senju, et al. on gaze following. http://cognitionandculture.net/blog/icci-blog/for-the-record-a-commentary-by-csibra-senju-et-al-on-gaze-following. Retrieved 1 Jul 2018
Sperber D, Wilson D (1995) Relevance: communication and cognition, 2nd edn. Blackwell, Oxford
Szufnarowska J, Rohlfing KJ, Fawcett C, Gredebäck G (2014) Is ostension any more than attention? Sci Rep 4:5304. https://doi.org/10.1038/srep05304
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. https://doi.org/10.1016/j.cub.2011.12.018
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. https://doi.org/10.1098/rstb.2009.0052
Tomasello M (1999) The cultural origins of human cognition. Harvard University Press, Cambridge
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 506–524
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. https://doi.org/10.1016/j.jhevol.2006.10.001
Tomonaga M (1999) Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes). Primates 40:417–438. https://doi.org/10.1007/BF02557579
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. https://doi.org/10.1126/science.1176960
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 319–346
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. https://doi.org/10.1098/rsbl.2009.0864
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. https://doi.org/10.1007/s10071-007-0127-y
Vorms M (2012) A-not-B errors: testing the limits of natural pedagogy theory. Rev Philos Psychol 3:525–545. https://doi.org/10.1007/s13164-012-0113-4
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. https://doi.org/10.1016/j.anbehav.2007.08.010
Yamagiwa J (1992) Functioinal analysis of social staring behavior in an all-male group of mountain gorillas. Primates 33:523–544. https://doi.org/10.1007/BF02381153
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. https://doi.org/10.1073/pnas.1108517109
Acknowledgements
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].
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kano, F., Moore, R., Krupenye, C. et al. Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention. Anim Cogn 21, 715–728 (2018). https://doi.org/10.1007/s10071-018-1205-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-018-1205-z
Keywords
- Domestication
- Gaze following
- Great ape
- Ostensive signals
- Referential communication