Social attention in the two species of pan: Bonobos make more eye contact than chimpanzees

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Kano, Fumihiro ^a,b,c   Hirata, Satoshi ^a   Call, Josep ^b,d  

^a KYOTO UNIVERSITY   (Japan)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PAN; PRIMATES;

ANIMAL; ANIMAL BEHAVIOR; ATTENTION; FEMALE; MALE; PAN PANISCUS; PAN TROGLODYTES; SOCIAL BEHAVIOR;

ANIMALS; ATTENTION; BEHAVIOR, ANIMAL; FEMALE; MALE; PAN PANISCUS; PAN TROGLODYTES; SOCIAL BEHAVIOR;

EID: 84936867417     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129684     Document Type: Article

References (68)

1. Furuichi T. Female contributions to the peaceful nature of bonobo society. Evol Anthropol. 2011; 20(4):131-42. doi: 10.1002/evan.20308 PMID: 22038769
2. Wilson ML, Boesch C, Fruth B, Furuichi T, Gilby IC, Hashimoto C, et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature. 2014; 513(7518):414-7. doi: 10.1038/nature13727 PMID: 25230664
3. Hare B, Wobber V, Wrangham R. The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Anim Behav. 2012; 83(3):573.
4. Palagi E. Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implicationsfor natural social systems and interindividual relationships. Am J Phys Anthropol. 2006; 129(3):418-26. PMID: 16323189
5. de Waal FBM. Sociosexual behavior used for tension regulation in all age and sex combinations among bonobos. Pedophilia. New York: Springer; 1990. p. 378-93.
6. Tan J, Hare B. Bonobos share with strangers. PLOS ONE. 2013; 8(1):e51922. doi: 10.1371/journal.pone.0051922 PMID: 23300956
7. Argyle M, Dean J. Eye-contact, distance and affiliation. Sociometry. 1965:289-304. PMID: 14341239
8. Kleinke CL. Gaze and eye contact: A research review. Psychol Bullet. 1986; 100(1):78-100. PMID: 3526377
9. Blais C, Jack RE, Scheepers C, Fiset D, Caldara R. Culture shapes how we look at faces. PLOS ONE. 2008; 3(8):e3022. doi: 10.1371/journal.pone.0003022 PMID: 18714387
10. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiatry. 2002; 59(9):809-16. PMID: 12215080
11. Gomez JC. Ostensive behavior in great apes: The role of eye contact. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: The minds of the great apes. New York: Cambridge University Press; 1996. p. 131-51.
12. Farroni T, Csibra G, Simion F, Johnson MH. Eye contact detection in humans from birth. Proc Nat Acad Sci. 2002; 99(14):9602. PMID: 12082186
13. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T. Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition. 2003; 89(2):113-24.
14. Conty L, Tijus C, Hugueville L, Coelho E, George N. Searching for asymmetries in the detection of gaze contact versus averted gaze under different head views: A behavioural study. Spatial vision. 2006; 19(6):529-46. PMID: 17278526
15. Tomonaga M, Imura T. Visual search for human gaze direction by a chimpanzee (Pan troglodytes). PLOS ONE. 2010; 5(2):e9131. doi: 10.1371/journal.pone.0009131 PMID: 20161750
16. Kano F, Call J, Tomonaga M. Face and eye scanning in gorillas, orangutans, and humans: Unique eyeviewing patterns in humans among hominids. J Comp Psychol. 2012; 126(4):388-98. doi: 10.1037/a0029615 PMID: 22946925
17. Kano F, Tomonaga M. Face scanning in chimpanzees and humans: Continuity and discontinuity. Anim Behav. 2010; 79(1):227-35.
18. Keating CF, Keating EG. Visual scan patterns of rhesus monkeys viewing faces. Perception. 1982; 11(2):211-9. PMID: 7155774
19. Gothard KM, Erickson CA, Amaral DG. How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim Cogn. 2004; 7(1):25-36. PMID: 14745584
20. Guo K, Robertson RG, Mahmoodi S, Tadmor Y, Young MP. How do monkeys view faces? A study of eye movements. Exp Brain Res. 2003; 150(3):363-74. PMID: 12707744
21. Hirata S, Fuwa K, Sugama K, Kusunoki K, Fujita S. Facial perception of conspecifics: Chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes. Anim Cogn. 2010; 13(5):679-88. doi: 10.1007/s10071-010-0316-y PMID: 20213188
22. Bard KA, Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Costall A, Matsuzawa T. Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Dev Psychol. 2005; 41(4):616-24. PMID: 16060808
23. Ferrari PF, Paukner A, Ionica C, Suomi SJ. Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol. 2009; 19(20):1768-72. doi: 10.1016/j.cub.2009.08.055 PMID: 19818617
24. Yamagiwa J. Functioinal analysis of social staring behavior in an all-male group of mountain gorillas. Primates. 1992; 33(4):523-44.
25. de Waal FBM. Peacemaking among primates. Cambridge: Harvard University Press; 1990.
26. Thomsen CE. Eye contact by non-human primates toward a human observer. Anim Behav. 1974; 22:144-9.
27. Senju A, Johnson MH. The eye contact effect: Mechanisms and development. Trends Cogn Sci. 2009; 13(3):127-34. doi: 10.1016/j.tics.2008.11.009 PMID: 19217822
28. Jones W, Klin A. Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature. 2013; 504:427-31. doi: 10.1038/nature12715 PMID: 24196715
29. Happé F. Autism: cognitive deficit or cognitive style? Trends Cogn Sci. 1999; 3(6):216-22. PMID: 10354574
30. Baron-Cohen S. Autism: the empathizing-systemizing (E-S) theory. Ann N Y Acad Sci. 2009; 1156(1):68-80. doi: 10.1111/j.1749-6632.2009.04419.x PMID: 19338500
31. Herrmann E, Hare B, Call J, Tomasello M. Differences in the cognitive skills of bonobos and chimpanzees. PLOS ONE. 2010; 5(8):e12438. doi: 10.1371/journal.pone.0012438 PMID: 20806062
32. Kano F, Call J. Cross-species variation of gaze following and conspecific preference among great apes, human infants and adults. Anim Behav. 2014; 91:137-50.
33. Hare B, Melis AP, Woods V, Hastings S, Wrangham R. Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol. 2007; 17(7):619-23. PMID: 17346970
34. Rosati AG, Hare B. Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci. 2012; 15(6):840-53. doi: 10.1111/j.1467-7687.2012.01182.x PMID: 23106738
35. Rosati AG, Stevens JR, Hare B, Hauser MD. The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults. Curr Biol. 2007; 17(19):1663-8. PMID: 17900899
36. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, et al. Cultures in chimpanzees. Nature. 1999; 399(6737):682-5. PMID: 10385119
37. Matsuzawa T, Tomonaga M, Tanaka M. Cognitive development in chimpanzees. Tokyo: Springer; 2006.
38. van Schaik CP, Deaner RO, Merrill MY. The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol. 1999; 36(6):719-41. PMID: 10330335
39. Hohmann G, Fruth B. Culture in bonobos? Between-species and within-species variation in behavior. Current Anthropology. 2003; 44(4):563-71.
40. Kano T. The use of leafy twigs for rain cover by the pygmy chimpanzees of Wamba. Primates. 1982; 23(3):453-7.
41. Jordan C. Object manipulation and tool-use in captive pygmy chimpanzees (Pan paniscus). J Hum Evol. 1982; 11(1):35-9.
42. Gruber T, Clay Z, Zuberbühler K. A comparison of bonobo and chimpanzee tool use: evidence for a female bias in the Pan lineage. Anim Behav. 2010; 80(6):1023-33.
43. Takeshita H, Walraven V. A comparative study of the variety and complexity of object manipulation in captive chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Primates. 1996; 37(4):423-41.
44. Schick KD, Toth N, Garufi G, Savage-Rumbaugh ES, Rumbaugh D, Sevcik R. Continuing investigations into the stone tool-making and tool-using capabilities of a bonobo (Pan paniscus). Journal of Archaeological Science. 1999; 26(7):821-32. PMID: 10628563
45. Hare B, Call J, Agnetta B, Tomasello M. Chimpanzees know what conspecifics do and do not see. Anim Behav. 2000; 59(4):771-85. PMID: 10792932
46. Koops K, Furuichi T, Hashimoto C. Chimpanzees and bonobos differ in intrinsic motivation for tool use. under review.
47. Deaner RO, Khera AV, Platt ML. Monkeys pay per view: Adaptive valuation of social images by rhesus macaques. Curr Biol. 2005; 15(6):543-8. PMID: 15797023
48. Kano F, Hirata S, Call J, Tomonaga M. The visual strategy specific to humans among hominids: A study using the gap-overlap paradigm. Vision Res. 2011; 51(23):2348-55. doi: 10.1016/j.visres.2011.09.006 PMID: 21951519
49. Myowa-Yamakoshi M, Scola C, Hirata S. Humans and chimpanzees attend differently to goal-directed actions. Nat Commun. 2012; 3:693. doi: 10.1038/ncomms1695 PMID: 22353723
50. Hershler O, Hochstein S. At first sight: A high-level pop out effect for faces. Vision Res. 2005; 45(13):1707-24. PMID: 15792845
51. Fletcher-Watson S, Findlay JM, Leekam SR, Benson V. Rapid detection of person information in a naturalistic scene. Perception. 2008; 37:571-83. PMID: 18546664
52. Guo K. Initial fixation placement in face images is driven by top-down guidance. Exp Brain Res. 2007; 181(4):673-7. PMID: 17619183
53. Kano F, Tomonaga M. Head-Mounted Eye Tracking of a Chimpanzee under Naturalistic Conditions. PLOS ONE. 2013; 8(3):e59785. doi: 10.1371/journal.pone.0059785 PMID: 23544099
54. van de Waal E, Renevey N, Favre CM, Bshary R. Selective attention to philopatric models causes directed social learning in wild vervet monkeys. Proc Roy Soc B. 2010; 277(1691):2105-11. doi: 10.1098/rspb.2009.2260 PMID: 20236972
55. Ruiz A, Gómez JC, Roeder JJ, Byrne RW. Gaze following and gaze priming in lemurs. Anim Cogn. 2009; 12(3):427-34. doi: 10.1007/s10071-008-0202-z PMID: 19107531
56. MacLean EL, Hare B. Bonobos and chimpanzees exploit helpful but not prohibitive gestures. Behaviour. 2014:in press.
57. Herrmann E, Hare B, Cissewski J, Tomasello M. A comparison of temperament in nonhuman apes and human infants. Dev Sci. 2011; 14(6):1393-405. doi: 10.1111/j.1467-7687.2011.01082.x PMID: 22010898
58. Guastella AJ, Mitchell PB, Dadds MR. Oxytocin increases gaze to the eye region of human faces. Biol Psychiatry. 2008; 63(1):3-5. PMID: 17888410
59. Ebitz RB, Watson KK, Platt ML. Oxytocin blunts social vigilance in the rhesus macaque. Proc Nat Acad Sci. 2013; 110(28):11630-5. doi: 10.1073/pnas.1305230110 PMID: 23798448
60. Staes N, Stevens JM, Helsen P, Hillyer M, Korody M, Eens M. Oxytocin and vasopressin receptor gene variation as a proximate base for inter-and intraspecific behavioral differences in bonobos and chimpanzees. PLOS ONE. 2014; 9(11):e113364. doi: 10.1371/journal.pone.0113364 PMID: 25405348
61. Nagasawa M, Mitsui S, En S, Ohtani N, Ohta M, Sakuma Y, et al. Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science. 2015; 348(6232):333-6. doi: 10.1126/science.1261022 PMID: 25883356
62. Oliva J, Rault J- L, Appleton B, Lill A. Oxytocin enhances the appropriate use of human social cues by the domestic dog (Canis familiaris) in an object choice task. Anim Cogn. 2015; 18(3):767-75. doi: 10.1007/s10071-015-0843-7 PMID: 25647172
63. Lutchmaya S, Baron-Cohen S, Raggatt P. Foetal testosterone and eye contact in 12-month-old human infants. Infant Behav Dev. 2002; 25(3):327-35.
64. McIntyre MH, Herrmann E, Wobber V, Halbwax M, Mohamba C, de Sousa N, et al. Bonobos have a more human-like second-to-fourth finger length ratio (2D: 4D) than chimpanzees: a hypothesized indication of lower prenatal androgens. J Hum Evol. 2009; 56(4):361-5. doi: 10.1016/j.jhevol.2008.12.004 PMID: 19285708
65. Dalton KM, Nacewicz BM, Johnstone T, Schaefer HS, Gernsbacher MA, Goldsmith HH, et al. Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci. 2005; 8:519-26. PMID: 15750588
66. Kawashima R, Sugiura M, Kato T, Nakamura A, Hatano K, Ito K, et al. The human amygdala plays an important role in gaze monitoring A PET study. Brain. 1999; 122(4):779-83.
67. Mosher CP, Zimmerman PE, Gothard KM. Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr Biol. 2014; 24(20):2459-64. doi: 10.1016/j.cub.2014.08.063 PMID: 25283782
68. Rilling JK, Scholz J, Preuss TM, Glasser MF, Errangi BK, Behrens TE. Differences between chimpanzees and bonobos in neural systems supporting social cognition. Social cognitive and affective neuroscience. 2012; 7(4):369-79. doi: 10.1093/scan/nsr017 PMID: 21467047