Skip to main content
Log in

Primates’ Socio-Cognitive Abilities: What Kind of Comparisons Makes Sense?

  • Regular Article
  • Published:
Integrative Psychological and Behavioral Science Aims and scope Submit manuscript

Abstract

Referential gestures are of pivotal importance to the human species. We effortlessly make use of each others’ referential gestures to attend to the same things, and our ability to use these gestures show themselves from very early in life. Almost 20 years ago, James Anderson and colleagues presented an experimental paradigm with which to examine the use of referential gestures in non-human primates: the object-choice task. Since then, numerous object-choice studies have been made, not only with primates but also with a range of other animal taxa. Surprisingly, several non-primate species appear to perform better in the object-choice task than primates do. Different hypotheses have been offered to explain the results. Some of these have employed generalizations about primates or subsets of primate taxa that do not take into account the unparalleled diversity that exists between species within the primate order on parameters relevant to the requirements of the object-choice task, such as social structure, feeding ecology, and general morphology. To examine whether these broad primate generalizations offer a fruitful organizing framework within which to interpret the results, a review was made of all published primate results on the use of gazing and glancing cues with species ordered along the primate phylogenetic tree. It was concluded that differences between species may be larger than differences between ancestry taxa, and it is suggested that we need to start rethinking why we are testing animals on experimental paradigms that do not take into account what are the challenges of their natural habitat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Notes

  1. Rearing categories (after Call and Tomasello (1996). Captive: Many zoo animals and some from laboratories. Have interacted directly with humans only minimally such as, for instance, during feeding and cleaning situations; Nursery-raised: Have been raised from an early age in a nursery setting with peer conspecifics and much contact with human caretakers; Laboratory-trained: Have been raised in captivity and trained in particular tasks, often many kinds, over the years; Home-raised: Also termed enculturated. Have been raised by humans and have participated extensively and intensively in interactions with them and their artifacts in a home-like cultural environment. Many home-raised individuals have also been exposed to some kind of language-training.

References

  • Amici, F., Aureli, F., Visalberghi, E., & Call, J. (2009). Spider monkeys (Ateles geoffroyi) and capuchin monkeys (Cebus apella) follow gaze around barriers: evidence for perspective taking? Journal of Comparative Psychology, 123, 368–374.

    Article  PubMed  Google Scholar 

  • Anderson, J. R., Sallaberry, P., & Barbier, H. (1995). Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Animal Behaviour, 49, 201–208.

    Article  Google Scholar 

  • Anderson, J. R., Montant, M., & Schmitt, D. (1996). Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behavioural Processes, 37, 47–55.

    Article  PubMed  Google Scholar 

  • Barth, J., Reaux, J. E., & Povinelli, D. J. (2005). Chimpanzees’ (Pan troglodytes) use of Gaze cues in object-choice tasks: different methods yield different results. Animal Cognition, 8, 84–92.

    Article  PubMed  Google Scholar 

  • Behne, T., Carpenter, M., & Tomasello, M. (2005). One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Developmental Science, 8, 492–499.

    Article  PubMed  Google Scholar 

  • Bering, J. M. (2004). A critical review of the “enculturation hypothesis”: the effects of human rearing on great ape social cognition. Animal Cognition, 7, 201–212.

    Article  PubMed  Google Scholar 

  • Bräuer, J., Call, J., & Tomasello, M. (2005). All great ape species follow gaze to distant locations and around barriers. Journal of Comparative Psychology, 119, 145–154.

    Article  PubMed  Google Scholar 

  • Bräuer, J., Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2006). Making inferences about the location of hidden food: social dog, causal ape. Journal of Comparative Psychology, 120, 38–47.

    Article  PubMed  Google Scholar 

  • Bretherton, I., & Beeghly, M. (1982). Talking about internal states. Developmental Psychology, 18, 906–921.

    Article  Google Scholar 

  • Burkart, J., & Heschl, A. (2006). Geometrical gaze following in common marmosets (Callithrix jacchus). Journal of Comparative Psychology, 120, 120–130.

    Article  PubMed  Google Scholar 

  • Butterworth, G., & Cochran, E. (1980). Towards a mechanism of joint visual attention in human infancy. International Journal of Behavioral Development, 3, 253–272.

    Article  Google Scholar 

  • Byrnit, J. T. (2004). Nonenculturated orangutans’ (Pongo pygmaeus) use of experimenter-given manual and facial cues in an object-choice task. Journal of Comparative Psychology, 118, 309–315.

    Article  PubMed  Google Scholar 

  • Byrnit, J.T. (2005). Primate theory of mind: a comparative psychological analysis. Published Ph.D. monograph. Department of Psychology, Aarhus University, 2005, 3.

  • Byrnit, J. T. (2009). Gorillas’ (Gorilla gorilla) use of experimenter-given manual and facial cues in an object-choice task. Animal Cognition, 12, 401–404.

    Article  PubMed  Google Scholar 

  • Byrnit, J.T., Høgh-Olesen, H., Makransky, G. (2015). Chimpanzee (Pan troglodytes) and bonobo (Pan paniscus) willingness to share highly attractive, monopolizable food sources. J of Comp Psych. doi:10.1037/a0039351

  • Call, J., & Tomasello, M. (1996). The effect of humans on the cognitive development of apes. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into thought: The minds of the great apes. Cambridge: Cambridge University Press.

    Google Scholar 

  • Call, J., Hare, B. A., & Tomasello, M. (1998). Chimpanzee gaze following in an object-choice task. Animal Cognition, 1, 89–99.

    Article  PubMed  Google Scholar 

  • Call, J., Agnetta, B., & Tomasello, M. (2000). Cues that chimpanzees do and do not use to find hidden objects. Animal Cognition, 3, 23–34.

    Article  Google Scholar 

  • Corkum, V., & Moore, C. (1995). Development of joint visual attention in infants. In C. Moore & P. Dunham (Eds.), Joint attention: Its origin and role in development. New Jersey: Erlbaum.

    Google Scholar 

  • Deaner, R. O., van Schaik, C. P., & Johnson, V. (2006). Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology, 4, 149–196.

    Google Scholar 

  • Dorey, N. R., Udell, M. A. R., & Wynne, C. D. L. (2010). When do domestic dogs, Canis familiaris, start to understand human pointing? The role of ontogeny in the development of interspecies communication. Animal Behaviour, 79, 37–41.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1988). Primate social systems. Ithaca: Cornell University Press.

    Book  Google Scholar 

  • Dunbar, R. I. M. (1992). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 20, 469–493.

    Article  Google Scholar 

  • Emery, N. J. (2000). The eyes have it: the neuroethology, function and evolution of social gaze. Neuroscience & Biobehavioral Reviews, 24, 581–604.

    Article  Google Scholar 

  • Giret, N., Miklósi, Á., Kreutzer, M., & Bovet, D. (2008). Use of experimenter-given cues by African gray parrots (Psittacus erithacus). Animal Cognition. doi:10.1007/s 10071-008-0163-2.

    Google Scholar 

  • Hall, N. J., Udell, M. A. R., Dorey, N. R., Walsh, A. L., & Wynne, C. D. L. (2011). Megachiropteran bats (Pteropus) utilize human referential stimuli to locate hidden food. Journal of Comparative Psychology, 125, 341–346.

    Article  PubMed  Google Scholar 

  • Hare, B., & Tomasello, M. (1999). Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. Journal of Comparative Psychology, 113, 173–177.

    Article  Google Scholar 

  • Hare, B., & Tomasello, M. (2004). Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Animal Behaviour, 68, 571–581.

    Article  Google Scholar 

  • Hare, B., Call, J., & Tomasello, M. (2001). Do chimpanzees know what conspecifics know? Animal Behaviour, 61, 139–151.

    Article  PubMed  Google Scholar 

  • Hare, B., Brown, M., Williamson, C., & Tomasello, M. (2002). The domestication of social cognition in dogs. Science, 298, 1634–1636.

    Article  PubMed  Google Scholar 

  • Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., & Trut, L. (2005). Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Current Biology, 15, 226–230.

    Article  PubMed  Google Scholar 

  • Hare, B., Melis, A. P., Woods, V., Hastings, S., & Wrangham, R. (2007). Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Current Biology, 17, 619–623.

    Article  PubMed  Google Scholar 

  • Hare, B., Rosati, A., Kaminski, J., Bräuer, J., Call, J., & Tomasello, M. (2010). The domestication hypothesis for dogs’ skills with human communication: a response to Udell et al. (2008) and Wynne et al. (2008). Animal Behaviour, 79, e1–e6.

    Article  Google Scholar 

  • Hauser, M. D., Glynn, D., & Wood, J. (2007). Rhesus monkeys correctly read the goal-relevant gestures of a human agent. Proceedings of the Royal Society of London B: Biological Sciences, 274, 1913–1918.

    Article  Google Scholar 

  • Heilbronner, S. R., Rosati, A. G., Stevens, J. R., Hare, B., & Hauser, M. D. (2008). A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biology Letters, 4, 246–249.

    Article  PubMed Central  PubMed  Google Scholar 

  • Herrmann, E., & Tomasello, M. (2006). Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Developmental Science, 9, 518–529.

    Article  PubMed  Google Scholar 

  • Herrmann, E., Call, J., Hernández-Lloreda, M. V., Hare, B., & Tomasello, M. (2007). Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science, 317, 1360–1366.

  • Hostetter, A. B., Russell, J. L., Freeman, H., & Hopkins, W. D. (2007). Now you see me, now you don’t: evidence that chimpanzees understand the role of the eyes in attention. Animal Cognition, 10, 55–62.

    Article  PubMed Central  PubMed  Google Scholar 

  • Inoue, Y., Inoue, E., & Itakura, S. (2004). Use of experimenter-given directional cues by a young white-handed gibbon (Hylobates lar). Japanese Psychological Research, 46, 262–267.

    Article  Google Scholar 

  • Itakura, S., & Anderson, J. R. (1996). Learning to use experimenter-given cues during an object-choice task by a capuchin monkey. Cahiers de Psychologie Cognitive, 15, 103–112.

    Google Scholar 

  • 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). Journal of Comparative Psychology, 112, 119–126.

    Article  PubMed  Google Scholar 

  • Itakura, S., Agnetta, B., Hare, B., & Tomasello, M. (1999). Chimpanzee use of human and conspecific social cues to locate hidden food. Developmental Science, 2, 448–456.

    Article  Google Scholar 

  • Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2005). Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task. Animal Behaviour, 69, 11–18.

    Article  Google Scholar 

  • Kaplan, G., & Rogers, L. J. (2002). Patterns of gazing in orangutans (Pongo pygmaeus). International Journal of Primatology, 23, 501–526.

    Article  Google Scholar 

  • Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707–740.

    Article  Google Scholar 

  • Kirchhofer, K. C., Zimmermann, F., Kaminski, J., & Tomasello, M. (2012). Dogs (Canis familiaris), but not chimpanzees (Pan troglodytes), understand imperative pointing. PLoS ONE, 7, 2.

    Article  Google Scholar 

  • Liebal, K., & Kaminski, J. (2012). Gibbons (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) follow human gaze, but do not take the visual perspective of others. Animal Cognition. doi:10.1007/s10071-012-0543-5.

    PubMed  Google Scholar 

  • Lyn, H., Russell, J. L., & Hopkins, W. D. (2010). The impact of environment on the comprehension of declarative communication in apes. Psychological Science, 21, 360–365.

    Article  PubMed  Google Scholar 

  • MacLean, E. L., Matthews, L. J., Hare, B. A., et al. (2011). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15, 223–238.

    Article  PubMed Central  PubMed  Google Scholar 

  • Maros, K., Gácsi, M., & Miklósi, A. (2008). Comprehension of human pointing gestures in horses (Equus caballus). Animal Cognition, 11, 457–466.

    Article  PubMed  Google Scholar 

  • Melis, A. P., Hare, B., & Tomasello, M. (2006). Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Animal Behaviour, 72, 275–286.

    Article  Google Scholar 

  • Miklósi, Á., & Soproni, K. (2006). A comparative analysis of animals’ understanding of the human pointing gesture. Animal Cognition, 9, 81–93.

    Article  PubMed  Google Scholar 

  • Miklósi, A., Pongrácz, P., Lakatos, G., Topál, J., & Csányi, V. (2005). A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans. Journal of Comparative Psychology, 119, 179–186.

    Article  PubMed  Google Scholar 

  • Morissette, P., Ricard, M., & Décarie, T. G. (1995). Joint visual attention and pointing in infancy: a longitudinal study of comprehension. British Journal of Developmental Psychology, 13, 163–175.

    Article  Google Scholar 

  • Mulcahy, N., & Call, J. (2009). The performance of bonobos (Pan paniscus), chimpanzees (Pan troglodytes), and orangutans (Pongo pygmaeus) in two versions of an object-choice task. Journal of Comparative Psychology, 123, 304–309.

    Article  PubMed  Google Scholar 

  • Mulcahy, N. J., & Hedge, N. J. (2012). Are great apes tested with an abject object-choice task? Animal Behaviour, 83, 313–321.

    Article  Google Scholar 

  • Mulcahy, N., & Suddendorf, T. (2011). An obedient orangutan (Pongo abelii) performs perfectly in peripheral object-choice tasks but fails the standard centrally presented versions. Journal of Comparative Psychology, 125, 112–115.

    Article  PubMed  Google Scholar 

  • Neiworth, J. J., Burman, M. A., Basile, B. M., & Lickteig, M. T. (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). Journal of Comparative Psychology, 116, 3–11.

    Article  PubMed  Google Scholar 

  • Okamoto-Barth, S., Tomonaga, M., Tanaka, M., & Matsuzawa, T. (2008). Development of using experimenter-given cues in infant chimpanzees: longitudinal changes in behavior and cognitive development. Developmental Science, 11, 98–108.

    Article  PubMed  Google Scholar 

  • Pack, A. A., & Herman, L. M. (2004). Bottlenosed dolphins (Tursiops truncatus) comprehend the referent of both static and dynamic human gazing and pointing in an object-choice task. Journal of Comparative Psychology, 118, 160–171.

    Article  PubMed  Google Scholar 

  • Peignot, P., & Anderson, J. R. (1999). Use of experimenter-given manual and facial cues by gorillas (Gorilla gorilla) in an object-choice task. Journal of Comparative Psychology, 113, 253–260.

    Article  Google Scholar 

  • Plotnik, J. M., Shaw, R. C., Brubaker, D. L., Tiller, L. N., & Clayton, N. S. (2014). Thinking with their trunks: elephants use smell but not sound to locate food and exclude nonrewarding alternatives. Animal Behaviour, 88, 91–98.

    Article  Google Scholar 

  • Povinelli, D. J., & Eddy, T. J. (1996a). Chimpanzees: joint visual attention. Psychological Science, 7, 129–135.

    Article  Google Scholar 

  • Povinelli, D. J., & Eddy, T. J. (1996b). What young chimpanzees know about seeing. Monographs of the Society for Research in Child Development, 61, 3.

    Article  Google Scholar 

  • Povinelli, D. J., Reaux, J. E., Bierschwale, D. T., Allain, A. D., & Simon, B. B. (1997). Exploitation of pointing as a referential gesture in young children, but not adolescent chimpanzees. Cognitive Development, 12, 423–461.

    Article  Google Scholar 

  • Povinelli, D. J., Bierschwale, D. T., & Cech, C. G. (1999). Comprehension of seeing as a referential act in young children, but not juvenile chimpanzees. British Journal of Developmental Psychology, 17, 37–60.

    Article  Google Scholar 

  • Rosati, A. G., & Hare, B. (2009). Looking past the model species: diversity in gaze- following skills across primates. Current Opinion in Neurobiology, 19, 45–51.

    Article  PubMed  Google Scholar 

  • Ruiz, A., Gómez, J. C., Roeder, J. J., & Byrne, R. W. (2009). Gaze following and gaze priming in lemurs. Animal Cognition, 12, 427–434.

    Article  PubMed  Google Scholar 

  • Scheumann, M., & Call, J. (2004). The use of experimenter-given cues by South African fur seals (Arctocephalus pusillus). Animal Cognition, 7, 224–230.

    Article  PubMed  Google Scholar 

  • Schloegl, C., Kotrschal, K., & Bugnyar, T. (2007). Gaze following in common ravens, Corvus corax: ontogeny and habituation. Animal Behaviour, 74, 769–778.

    Article  Google Scholar 

  • Schmitt, V., Pankau, B., & Fischer, J. (2012). Old World Monkeys compare to apes in the primate cognition test battery. PLoS ONE, 7, e32024. doi: 10.13/1/journal.pone.0032024.

    Article  PubMed Central  PubMed  Google Scholar 

  • Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., & Struhsaker, T. T. (Eds.). (1987). Primate societies. Chicago: University of Chicago Press.

    Google Scholar 

  • Tan, J., Ruoting, T., & Yanjie, S. (2013). Testing the cognition of the forgotten colobines: a first look at golden snub-nosed monkeys (Rhinopithecus roxellana). International Journal of Primatology. doi:10.1007/s10764-013-9741-5.

    Google Scholar 

  • Tomasello, M., & Call, J. (1997). Primate cognition. New York: Oxford University Press.

    Google Scholar 

  • Tomasello, M., & Call, J. (2004). The role of humans in the cognitive development of apes revisited. Animal Cognition, 7, 213–215.

    Article  PubMed  Google Scholar 

  • Tomasello, M., Call, J., & Hare, B. (1998). Five primate species follow the visual gaze of conspecifics. Animal Behaviour, 55, 1063–1069.

    Article  PubMed  Google Scholar 

  • 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. Journal of Human Evolution, 52, 314–320.

    Article  PubMed  Google Scholar 

  • Udell, M. A. R., Dorey, N. R., & Wynne, C. D. (2008). Wolves outperform dogs in following human social cues. Animal Behaviour, 76, 1767–1773.

    Article  Google Scholar 

  • Udell, M. A. R., Dorey, N. R., & Wynne, C. D. L. (2010). What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biological Reviews, 85, 327–345.

    Article  PubMed  Google Scholar 

  • Verhulst, J. (2003). Developmental dynamics in human and other primates. New York: Adonis Press.

    Google Scholar 

  • Vick, S.-J., & Anderson, J. R. (2000). Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task. Journal of Comparative Psychology, 114, 200–207.

    Article  PubMed  Google Scholar 

  • Vick, S.-J., & Anderson, J. R. (2003). Use of human visual attention cues by olive baboons (Papio anubis) in a competitive task. Journal of Comparative Psychology, 117, 209–216.

    Article  PubMed  Google Scholar 

  • Vick, S.-J., Bovet, D., & Anderson, J. R. (2001). Gaze discrimination learning in olive baboons (Papio anubis). Animal Cognition, 4, 1–10.

    Article  Google Scholar 

  • Vlamings, P. H. J. M., Hare, B., & Call, J. (2009). Reaching around barriers: the performance of the great apes and 3-5-year-old children. Animal Cognition. doi:10.1007/s10071-009-0265-5.

    PubMed Central  PubMed  Google Scholar 

  • Wilkinson, A., Mandl, I., Bugnyar, T., & Huber, L. (2010). Gaze-following in the red-footed tortoise (Geochelone carbonaria). Animal Cognition, 13, 765–769.

    Article  PubMed  Google Scholar 

  • Wynne, C. D. L., Udell, M. A. R., & Lord, K. A. (2008). Ontogeny’s impacts on human-dog communication. Animal Behaviour. doi:10.1016/j.anbehav.2008.03.010.

    Google Scholar 

Download references

Acknowledgments

I would like to thank the anonymous reviewers for helpful comments on this paper. Furthermore, as usual, many thanks to Henriette Westh, Timothy Wooller, and Jennifer Nevile for dedicated proofreading, and inspiring and insightful suggestions on my work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jill T. Byrnit.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Byrnit, J.T. Primates’ Socio-Cognitive Abilities: What Kind of Comparisons Makes Sense?. Integr. psych. behav. 49, 485–511 (2015). https://doi.org/10.1007/s12124-015-9312-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12124-015-9312-8

Keywords

Navigation