Abstract
How much nonhuman animals understand about seeing has been the focus of comparative cognition research for decades. Many social primates (and other species) are sensitive to cues about what others can and cannot see. Whether this sensitivity evolved in primates through shared descent or convergent evolution remains unclear. The current study tested gibbons—the apes that are least studied yet most distantly related to humans and one of the less social primates—in two food-competition tasks. Specifically, we presented eastern hoolock gibbons, Hoolock leuconedys, and silvery gibbons, Hylobates moloch, with a choice between a contested piece of food visible to both themselves and a human competitor and an uncontested piece visible only to themselves. Subjects successfully stole the uncontested food when the competitor turned away his body (N = 10, experiment 1) and his head (N = 9, experiment 2). However, when the head of the experimenter was oriented towards the contested piece of food, whether the competitor opened or closed his eyes made no difference. Subjects’ sensitivity to body- and head-orientation cues was comparable to that of chimpanzees, rhesus macaques, and ring-tailed lemurs—species living in much larger groups than gibbons. These findings support the continuity hypothesis that sensitivity to body- and head-orientation cues is a product of shared descent among primates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
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? J Comp Psychol 123:368–374. https://doi.org/10.1037/a0017079
Amici F, Aureli F, Call J (2010) Monkeys and apes: are their cognitive skills really so different? Am J Phys Anthropol 143:188–197. https://doi.org/10.1002/ajpa.21305
Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49:201–208. https://doi.org/10.1016/0003-3472(95)80168-5
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
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
Bräuer J, Call J, Tomasello M (2007) Chimpanzees really know what others can see in a competitive situation. Anim Cogn 10:439–448. https://doi.org/10.1007/s10071-007-0088-1
Bray J, Krupenye C, Hare B (2014) Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear. Anim Cogn 17:735–744. https://doi.org/10.1007/s10071-013-0705-0
Brooks R, Meltzoff AN (2005) The development of gaze following and its relation to language. Dev Sci 8:535–543
Bugnyar T (2011) Knower-guesser differentiation in ravens: others’ viewpoints matter. Proc R Soc B Biol Sci 278:634–640. https://doi.org/10.1098/rspb.2010.1514
Bugnyar T, Stöwe M, Heinrich B (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc R Soc B Biol Sci 271:1331–1336. https://doi.org/10.1098/rspb.2004.2738
Bugnyar T, Reber SA, Buckner C (2016) Ravens attribute visual access to unseen competitors. Nat Commun. https://doi.org/10.1038/ncomms10506
Burkart J, Heschl A (2006) Geometrical gaze following in common marmosets (Callithrix jacchus). J Comp Psychol 120:120–130. https://doi.org/10.1037/0735-7036.120.2.120
Burkart JM, Heschl A (2007) Understanding visual access in common marmosets, Callithrix jacchus: perspective taking or behaviour reading? Anim Behav 73:457–469. https://doi.org/10.1016/j.anbehav.2006.05.019
Butterworth G, Jarrett N (1991) What minds have in common is space: spatial mechanisms serving joint visual attention in infancy. Br J Dev Psychol 9:55–72. https://doi.org/10.1111/j.2044-835x.1991.tb00862.x
Call J, Hare BA, Tomasello M (1998) Chimpanzee gaze following in an object-choice task. Anim Cogn 1:89–99. https://doi.org/10.1007/s100710050013
Call J, Bräuer J, Kaminski J, Tomasello M (2003) Domestic dogs (Canis familiaris) are sensitive to the attentional state of humans. J Comp Psychol 117:257–263. https://doi.org/10.1037/0735-7036.117.3.257
Canteloup C, Piraux E, Poulin N, Meunier H (2016) Do Tonkean macaques (Macaca tonkeana) perceive what conspecifics do and do not see? PeerJ 4:e1693. https://doi.org/10.7717/peerj.1693
Carter J, Lyons NJ, Cole HL, Goldsmith AR (2008) Subtle cues of predation risk: starlings respond to a predator’s direction of eye-gaze. Proc R Soc B Biol Sci 275:1709–1715. https://doi.org/10.1098/rspb.2008.0095
Caspar KR, Mader L, Pallasdies F et al (2018) Captive gibbons (Hylobatidae) use different referential cues in an object-choice task: insights into lesser ape cognition and manual laterality. PeerJ 6:e5348. https://doi.org/10.7717/peerj.5348
Chetry D, Chetry R, Ghosh K, Singh AK (2011) Status and distribution of the eastern hoolock gibbon (Hoolock leuconedys) in Mehao Wildlife Sanctuary, Arunachal Pradesh, India. Primate Conserv 25:87–94. https://doi.org/10.1896/052.025.0113
Clark H, Elsherif MM, Leavens DA (2019) Ontogeny vs. phylogeny in primate/canid comparisons: a meta-analysis of the object choice task. Neurosci Biobehav Rev 105:178–189
Clayton NS, Dally JM, Emery NJ (2007) Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist. Philos Trans R Soc Lond B Biol Sci 362:507–522. https://doi.org/10.1098/rstb.2006.1992
Cunningham C, Mootnick A (2009) Quick guide to the gibbons. Curr Biol 19(14):543–544
D’Entremont B, Hains SMJ, Muir DW (1997) A demonstration of gaze following in 3-to 6-month-olds. Infant Behav Dev 20:569–572
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
Emery NJ, Clayton NS (2009) Comparative social cognition. Annu Rev Psychol 60:87–113. https://doi.org/10.1146/annurev.psych.60.110707.163526
Fan P-F, Xiao W, Huo S et al (2011) Distribution and conservation status of the vulnerable eastern hoolock gibbon Hoolock leuconedys in China. Oryx 45:129–134. https://doi.org/10.1017/s003060531000089x
Flavell JH, Shipstead SG, Croft K (1978) Young children’s knowledge about visual perception: hiding objects from others. Child Dev 49:1208–1211
Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452
Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks
Fuentes A (2000) Hylobatid communities: changing views on pair bonding and social organization in hominoids. Am J Phys Anthropol Suppl 31:33–60
Goossens BMA, Dekleva M, Reader SM et al (2008) Gaze following in monkeys is modulated by observed facial expressions. Anim Behav 75:1673–1681. https://doi.org/10.1016/j.anbehav.2007.10.020
Grueneisen S, Duguid S, Saur H, Tomasello M (2017) Children, chimpanzees, and bonobos adjust the visibility of their actions for cooperators and competitors. Sci Rep 7:1–10. https://doi.org/10.1038/s41598-017-08435-7
Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4:269–280. https://doi.org/10.1007/s100710100084
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, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785. https://doi.org/10.1006/anbe.1999.1377
Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151. https://doi.org/10.1006/anbe.2000.1518
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
Hare B, Addessi E, Call J et al (2003) Do capuchin monkeys, Cebus apella, know what conspecifics do and do not see? Anim Behav 65:131–142. https://doi.org/10.1006/anbe.2002.2017
Hare B, Call J, Tomasello M (2006) Chimpanzees deceive a human competitor by hiding. Cognition 101:495–514. https://doi.org/10.1016/j.cognition.2005.01.011
Herrmann E, Tomasello M (2006) Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Dev Sci 5:518–529
Heyes C (2015) Animal mindreading: what’s the problem? Psychon Bull Rev 22:313–327. https://doi.org/10.3758/s13423-014-0704-4
Horton KE, Caldwell CA (2006) Visual co-orientation and expectations about attentional orientation in pileated gibbons (Hylobates pileatus). Behav Process 72:65–73. https://doi.org/10.1016/j.beproc.2005.12.004
Hu N, Guan Z, Huang B et al (2018) Dispersal and female philopatry in a long-term, stable, polygynous gibbon population: evidence from 16 years field observation and genetics. Am J Primatol 80:1–12. https://doi.org/10.1002/ajp.22922
Inoue Y, Inoue E, Itakura S (2004) Use of experimenter-given directional cues by a young white-handed gibbon (Hylobates lar). Jpn Psychol Res 46:262–267. https://doi.org/10.1111/j.1468-5584.2004.00258.x
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. Anim Behav 69:11–18. https://doi.org/10.1016/j.anbehav.2004.05.008
Kaminski J, Call J, Tomasello M (2008) Chimpanzees know what others know, but not what they believe. Cognition 109:224–234. https://doi.org/10.1016/j.cognition.2008.08.010
Karg K, Schmelz M, Call J, Tomasello M (2015a) The goggles experiment: can chimpanzees use self-experience to infer what a competitor can see? Anim Behav 105:211–221. https://doi.org/10.1016/j.anbehav.2015.04.028
Karg K, Schmelz M, Call J, Tomasello M (2015b) Chimpanzees strategically manipulate what others can see. Anim Cogn. https://doi.org/10.1007/s10071-015-0875-z
Krupenye C, Call J (2019) Theory of mind in animals: current and future directions. Wiley Interdiscip Rev Cogn Sci e1503:1–25. https://doi.org/10.1002/wcs.1503
Lenth RV (2016) Least-squares means: the R package {lsmeans}. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Liebal K (2016) Communication and cognition of small apes. In: Reichard UH, Hirai H, Barelli C (eds) Evolution of gibbons and siamang: phylogeny, morphology, and cognition. Springer, New York, NY, pp 313–347
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. Anim Cogn 15:1211–1216. https://doi.org/10.1007/s10071-012-0543-5
Liebal K, Pika S, Tomasello M (2004) Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45:41–57. https://doi.org/10.1007/s10329-003-0063-7
Loretto MC, Schloegl C, Bugnyar T (2010) Northern bald ibises follow others’ gaze into distant space but not behind barriers. Biol Lett 6:14–17. https://doi.org/10.1098/rsbl.2009.0510
MacLean EL, Hare B (2012) Bonobos and chimpanzees infer the target of another’s attention. Anim Behav 83:345–353. https://doi.org/10.1016/j.anbehav.2011.10.026
MacLean EL, Sandel AA, Bray J et al (2013) Group size predicts social but not nonsocial cognition in lemurs. PLoS One 8:1–9. https://doi.org/10.1371/journal.pone.0066359
Malone N, Fuentes A, White FJ (2012) Variation in the social systems of extant hominoids: comparative insight into the social behavior of early hominins. Int J Primatol 33:1251–1277. https://doi.org/10.1007/s10764-012-9617-0
Melis AP, Call J, Tomasello M (2006) Chimpanzees (Pan troglodytes) conceal visual and auditory information from others. J Comp Psychol 120:154–162. https://doi.org/10.1037/0735-7036.120.2.154
Met A, Miklósi Á, Lakatos G (2014) Gaze-following behind barriers in domestic dogs. Anim Cogn 17:1401–1405. https://doi.org/10.1007/s10071-014-0754-z
Morino L (2012) Behavioral endocrinology of wild male siamangs (Symphalangus syndactylus). Rutgers University
Okamoto-barth S, Call J, Tomasello M (2007) Great apes’ understanding of others’ line of sight. Psychol Sci 18:1–20
Overduin-de Vries AM, Spruijt BM, Sterck EHM (2014) Long-tailed macaques (Macaca fascicularis) understand what conspecifics can see in a competitive situation. Anim Cogn 17:77–84. https://doi.org/10.1007/s10071-013-0639-6
Penn DC, Povinelli DJ (2007) On the lack of evidence that non-human animals possess anything remotely resembling a “theory of mind”. Philos Trans R Soc B Biol Sci 362:731–744. https://doi.org/10.1098/rstb.2006.2023
Pongrácz P, Szapu JS, Faragó T (2018) Cats (Felis silvestris catus) read human gaze for referential information. Intelligence 74:43–52
Povinelli DJ, Eddy TJ (1996) Chimpanzees: joint visual attention. Psychol Sci 7:129–136
Range F, Virányi Z (2011) Development of gaze following abilities in wolves (Canis lupus). PLoS One 6:e16888. https://doi.org/10.1371/journal.pone.0016888
Reichard UH, Ganpanakngan M, Barelli C (2013) White-handed gibbons of Khao Yai: social flexibility, complex reproductive strategies, and a slow life history. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 1–460
Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51. https://doi.org/10.1016/j.conb.2009.03.002
Sandel AA, MacLean EL, Hare B (2011) Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81:925–931. https://doi.org/10.1016/j.anbehav.2011.01.020
Scerif G, Gomez J-CC, Byrne RW (2004) What do diana monkeys know about the focus of attention of a conspecific? Anim Behav 68:1239–1247. https://doi.org/10.1016/j.anbehav.2004.01.011
Schloegl C, Kotrschal K, Bugnyar T (2007) Gaze following in common ravens, Corvus corax: ontogeny and habituation. Anim Behav 74:769–778. https://doi.org/10.1016/j.anbehav.2006.08.017
Schloegl C, Kotrschal K, Bugnyar T (2008) Do common ravens (Corvus corax) rely on human or conspecific gaze cues to detect hidden food? Anim Cogn 11:231–241. https://doi.org/10.1007/s10071-007-0105-4
Simpson J, O’Hara SJ (2019) Gaze following in an asocial reptile (Eublepharis macularius). Anim Cogn 22:145–152. https://doi.org/10.1007/s10071-018-1230-y
Sommer V, Reichard U (2000) 14• Rethinking monogamy: the gibbon case. Primate males Causes consequences Var Gr Compos 159
Srikosamatara S, Brockelman WY (1987) Polygyny in a group of pileated gibbons via a familial route. Int J Primatol 8:389–393. https://doi.org/10.1007/BF02737390
Tan J, Tao R, Su Y (2014) Testing the cognition of the forgotten colobines: a first look at golden snub-nosed monkeys (Rhinopithecus roxellana). Int J Primatol 35:376–393. https://doi.org/10.1007/s10764-013-9741-5
Téglás E, Gergely A, Kupán K et al (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
Tomasello M, Hare B, Agnetta B (1999) Chimpanzees, Pan troglodytes, follow gaze direction geometrically. Anim Behav 58:769–777. https://doi.org/10.1006/anbe.1999.1192
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
von Bayern AMP, Emery NJ (2009) Jackdaws respond to human attentional states and communicative cues in different contexts. Curr Biol 19:602–606. https://doi.org/10.1016/j.cub.2009.02.062
Watve M, Thakar J, Kale A et al (2002) Bee-eaters (Merops orientalis) respond to what a predator can see. Anim Cogn 5:253–259. https://doi.org/10.1007/s10071-002-0155-6
Werhahn G, Virányi Z, Barrera G et al (2016) Wolves (Canis lupus) and dogs (Canis familiaris) differ in following human gaze into distant space but respond similar to their packmates’ gaze. J Comp Psychol 130:288–298. https://doi.org/10.1037/com0000036
Wilkinson A, Mandl I, Bugnyar T, Huber L (2010) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769. https://doi.org/10.1007/s10071-010-0320-2
Yocom AM (2010) Physical and social cognition in the white-handed gibbon (Hylobates lar). The Ohio State University
Acknowledgements
We are grateful to Gabriella Skollar, Alma Rodriguez, Jodi Kleier, and other staff at GCC for hosting the current research and for their tremendous support. We want to thank Barbara Perez, Ergin Ozyazgan, Robert Ball, Emma Parker, Yuwei Zhang, and Catherine Hallsten for assistance with data collection. We thank Amelia Harrison for reliability coding.
Funding
The project was supported by a UCSD Academic Senate grant RG073623.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interests.
Ethical approval
The current research has been approved by the IACUC committee of the Gibbon Conservation Center (GCC) and complied with the rules of the IACUC office at University of California, San Diego.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sánchez-Amaro, A., Tan, J., Kaufhold, S.P. et al. Gibbons exploit information about what a competitor can see. Anim Cogn 23, 289–299 (2020). https://doi.org/10.1007/s10071-019-01333-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-019-01333-7