Gibbons exploit information about what a competitor can see

  • Alejandro Sánchez-AmaroEmail author
  • Jingzhi TanEmail author
  • Stephan P. Kaufhold
  • Federico Rossano
Original Paper


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.


Gibbon Hylobatidae Social cognition Perspective taking Social intelligence hypothesis Attention 



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.


The project was supported by a UCSD Academic Senate grant RG073623.

Compliance with ethical standards

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.

Supplementary material

10071_2019_1333_MOESM1_ESM.docx (855 kb)
Supplementary material 1 (DOCX 855 kb)


  1. 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. CrossRefPubMedGoogle Scholar
  2. Amici F, Aureli F, Call J (2010) Monkeys and apes: are their cognitive skills really so different? Am J Phys Anthropol 143:188–197. CrossRefPubMedGoogle Scholar
  3. Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49:201–208. CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  5. 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
  6. Bräuer J, Call J, Tomasello M (2007) Chimpanzees really know what others can see in a competitive situation. Anim Cogn 10:439–448. CrossRefPubMedGoogle Scholar
  7. 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. CrossRefPubMedGoogle Scholar
  8. Brooks R, Meltzoff AN (2005) The development of gaze following and its relation to language. Dev Sci 8:535–543CrossRefGoogle Scholar
  9. Bugnyar T (2011) Knower-guesser differentiation in ravens: others’ viewpoints matter. Proc R Soc B Biol Sci 278:634–640. CrossRefGoogle Scholar
  10. 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. CrossRefGoogle Scholar
  11. Bugnyar T, Reber SA, Buckner C (2016) Ravens attribute visual access to unseen competitors. Nat Commun. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Burkart J, Heschl A (2006) Geometrical gaze following in common marmosets (Callithrix jacchus). J Comp Psychol 120:120–130. CrossRefPubMedGoogle Scholar
  13. Burkart JM, Heschl A (2007) Understanding visual access in common marmosets, Callithrix jacchus: perspective taking or behaviour reading? Anim Behav 73:457–469. CrossRefGoogle Scholar
  14. 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. CrossRefGoogle Scholar
  15. Call J, Hare BA, Tomasello M (1998) Chimpanzee gaze following in an object-choice task. Anim Cogn 1:89–99. CrossRefPubMedGoogle Scholar
  16. 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. CrossRefPubMedGoogle Scholar
  17. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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. CrossRefGoogle Scholar
  21. 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 105:178–189CrossRefGoogle Scholar
  22. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cunningham C, Mootnick A (2009) Quick guide to the gibbons. Curr Biol 19(14):543–544CrossRefGoogle Scholar
  24. D’Entremont B, Hains SMJ, Muir DW (1997) A demonstration of gaze following in 3-to 6-month-olds. Infant Behav Dev 20:569–572CrossRefGoogle Scholar
  25. Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. CrossRefPubMedGoogle Scholar
  26. Emery NJ, Clayton NS (2009) Comparative social cognition. Annu Rev Psychol 60:87–113. CrossRefPubMedGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. Flavell JH, Shipstead SG, Croft K (1978) Young children’s knowledge about visual perception: hiding objects from others. Child Dev 49:1208–1211CrossRefGoogle Scholar
  29. Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452CrossRefGoogle Scholar
  30. Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand OaksGoogle Scholar
  31. Fuentes A (2000) Hylobatid communities: changing views on pair bonding and social organization in hominoids. Am J Phys Anthropol Suppl 31:33–60CrossRefGoogle Scholar
  32. Goossens BMA, Dekleva M, Reader SM et al (2008) Gaze following in monkeys is modulated by observed facial expressions. Anim Behav 75:1673–1681. CrossRefGoogle Scholar
  33. 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. CrossRefGoogle Scholar
  34. Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4:269–280. CrossRefPubMedGoogle Scholar
  35. Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581. CrossRefGoogle Scholar
  36. Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785. CrossRefPubMedGoogle Scholar
  37. Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151. CrossRefPubMedGoogle Scholar
  38. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. CrossRefPubMedGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. Hare B, Call J, Tomasello M (2006) Chimpanzees deceive a human competitor by hiding. Cognition 101:495–514. CrossRefPubMedGoogle Scholar
  41. Herrmann E, Tomasello M (2006) Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Dev Sci 5:518–529CrossRefGoogle Scholar
  42. Heyes C (2015) Animal mindreading: what’s the problem? Psychon Bull Rev 22:313–327. CrossRefPubMedGoogle Scholar
  43. Horton KE, Caldwell CA (2006) Visual co-orientation and expectations about attentional orientation in pileated gibbons (Hylobates pileatus). Behav Process 72:65–73. CrossRefGoogle Scholar
  44. 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. CrossRefGoogle Scholar
  45. 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. CrossRefGoogle Scholar
  46. 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. CrossRefGoogle Scholar
  47. Kaminski J, Call J, Tomasello M (2008) Chimpanzees know what others know, but not what they believe. Cognition 109:224–234. CrossRefPubMedGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. Karg K, Schmelz M, Call J, Tomasello M (2015b) Chimpanzees strategically manipulate what others can see. Anim Cogn. CrossRefPubMedGoogle Scholar
  50. Krupenye C, Call J (2019) Theory of mind in animals: current and future directions. Wiley Interdiscip Rev Cogn Sci e1503:1–25. CrossRefGoogle Scholar
  51. Lenth RV (2016) Least-squares means: the R package {lsmeans}. J Stat Softw 69:1–33. CrossRefGoogle Scholar
  52. 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 313–347CrossRefGoogle Scholar
  53. 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. CrossRefPubMedGoogle Scholar
  54. Liebal K, Pika S, Tomasello M (2004) Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates 45:41–57. CrossRefPubMedGoogle Scholar
  55. 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. CrossRefPubMedGoogle Scholar
  56. MacLean EL, Hare B (2012) Bonobos and chimpanzees infer the target of another’s attention. Anim Behav 83:345–353. CrossRefGoogle Scholar
  57. MacLean EL, Sandel AA, Bray J et al (2013) Group size predicts social but not nonsocial cognition in lemurs. PLoS One 8:1–9. CrossRefGoogle Scholar
  58. 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. CrossRefGoogle Scholar
  59. Melis AP, Call J, Tomasello M (2006) Chimpanzees (Pan troglodytes) conceal visual and auditory information from others. J Comp Psychol 120:154–162. CrossRefPubMedGoogle Scholar
  60. Met A, Miklósi Á, Lakatos G (2014) Gaze-following behind barriers in domestic dogs. Anim Cogn 17:1401–1405. CrossRefPubMedGoogle Scholar
  61. Morino L (2012) Behavioral endocrinology of wild male siamangs (Symphalangus syndactylus). Rutgers UniversityGoogle Scholar
  62. Okamoto-barth S, Call J, Tomasello M (2007) Great apes’ understanding of others’ line of sight. Psychol Sci 18:1–20CrossRefGoogle Scholar
  63. 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. CrossRefPubMedGoogle Scholar
  64. 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. CrossRefGoogle Scholar
  65. Pongrácz P, Szapu JS, Faragó T (2018) Cats (Felis silvestris catus) read human gaze for referential information. Intelligence 74:43–52CrossRefGoogle Scholar
  66. Povinelli DJ, Eddy TJ (1996) Chimpanzees: joint visual attention. Psychol Sci 7:129–136CrossRefGoogle Scholar
  67. Range F, Virányi Z (2011) Development of gaze following abilities in wolves (Canis lupus). PLoS One 6:e16888. CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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 1–460Google Scholar
  69. Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19:45–51. CrossRefPubMedGoogle Scholar
  70. 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. CrossRefGoogle Scholar
  71. 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. CrossRefGoogle Scholar
  72. Schloegl C, Kotrschal K, Bugnyar T (2007) Gaze following in common ravens, Corvus corax: ontogeny and habituation. Anim Behav 74:769–778. CrossRefGoogle Scholar
  73. 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. CrossRefPubMedGoogle Scholar
  74. Simpson J, O’Hara SJ (2019) Gaze following in an asocial reptile (Eublepharis macularius). Anim Cogn 22:145–152. CrossRefPubMedGoogle Scholar
  75. Sommer V, Reichard U (2000) 14 Rethinking monogamy: the gibbon case. Primate males Causes consequences Var Gr Compos 159Google Scholar
  76. Srikosamatara S, Brockelman WY (1987) Polygyny in a group of pileated gibbons via a familial route. Int J Primatol 8:389–393. CrossRefGoogle Scholar
  77. 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. CrossRefGoogle Scholar
  78. Téglás E, Gergely A, Kupán K et al (2012) Dogs’ gaze following is tuned to human communicative signals. Curr Biol 22:209–212. CrossRefPubMedGoogle Scholar
  79. Tomasello M, Hare B, Agnetta B (1999) Chimpanzees, Pan troglodytes, follow gaze direction geometrically. Anim Behav 58:769–777. CrossRefPubMedGoogle Scholar
  80. 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
  81. von Bayern AMP, Emery NJ (2009) Jackdaws respond to human attentional states and communicative cues in different contexts. Curr Biol 19:602–606. CrossRefGoogle Scholar
  82. 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. CrossRefPubMedGoogle Scholar
  83. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wilkinson A, Mandl I, Bugnyar T, Huber L (2010) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769. CrossRefPubMedGoogle Scholar
  85. Yocom AM (2010) Physical and social cognition in the white-handed gibbon (Hylobates lar). The Ohio State UniversityGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Cognitive ScienceUniversity of California San DiegoSan DiegoUSA

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