Social bonds affect anti-predator behaviour in a tolerant species of macaque, Macaca nigra

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1744, 2012, Pages 4042-4050

  Micheletta, Jérôme ^a,b   Waller, Bridget M ^a   Panggur, Maria R ^b,c   Neumann, Christof ^b,d,e,f   Duboscq, Julie ^b,d,g   Agil, Muhammad ^c   Engelhardt, Antje ^b,d  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b GERMAN PRIMATE CENTER   (Germany)

^c BOGOR AGRICULTURAL UNIVERSITY   (Indonesia)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^f UNIVERSITY OF LEIPZIG   (Germany)

^g CNRS   (France)

Author keywords

Alarm calls; Anti predator behaviour; Cooperation; Primate communication; Relationship quality; Social bond

Indexed keywords

ALARM SIGNAL; ANTIPREDATOR DEFENSE; COOPERATIVE BEHAVIOR; DOMINANCE; EUSOCIALITY; EVOLUTIONARY BIOLOGY; PREDATION RISK; PRIMATE; SURVIVAL; TOLERANCE;

EID: 84865360166     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.1470     Document Type: Article

References (66)

1. Christakis, N. A. & Fowler, J. H. 2010 Connected: the surprising power of our social networks and how they shape our lives. New York, NY: Little, Brown and Co.
2. Holt-Lunstad, J., Smith, T. B. & Layton, J. B. 2010 Social relationships and mortality risk: a meta-analytic review. PLoS Med. 7, e1000316. (doi:10.1371/journal.pmed.1000316)
3. House, J., Landis, K. & Umberson, D. 1988 Social relationships and health. Science 241, 540-545. (doi:10.1126/science.3399889)
4. Seyfarth, R. M. & Cheney, D. L. 2011 The evolutionary origins of friendship. Annu. Rev. Psychol. 63, 153-177. (doi:10.1146/annurev-psych-120710-100337)
5. Massen, J. J. M., Sterck, E. H. M. & De Vos, H. 2010 Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147, 1379-1412. (doi:10.1163/000579510x528224)
6. Silk, J. B. 2007 Social components of fitness in primate groups. Science 317, 1347-1351. (doi:10.1126/science.1140734)
7. Call, J., Aureli, F. & deWaal, F. B. M. 1999 Reconciliation patterns among stumptailed macaques: a multivariate approach. Anim. Behav. 58, 165-172. (doi:10.1006/anbe.1999.1116)
8. Cooper, M. A., Bernstein, I. S. & Hemelrijk, C. K. 2005 Reconciliation and relationship quality in Assamese macaques (Macaca assamensis). Am. J. Primatol. 65, 269-282. (doi:10.1002/ajp.20114)
9. Fujisawa, K. K., Kutsukake, N. & Hasegawa, T. 2005 Reconciliation pattern after aggression among Japanese preschool children. Aggress. Behav. 31, 138-152. (doi:10.1002/ab.20076)
10. de Marco, A., Cozzolino, R., Dessi-Fulgheri, F. & Thierry, B. 2010 Conflicts induce affiliative interactions among bystanders in a tolerant species of macaque (Macaca tonkeana). Anim. Behav. 80, 197-203. (doi:10.1016/j.anbehav.2010.04.016)
11. Mitani, J. C. 2009 Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633-640. (doi:10.1016/j.anbehav.2008.11.021)
12. Lemasson, A., Palombit, R. A. & Jubin, R. 2008 Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav. Ecol. Sociobiol. 62, 1027-1035. (doi:10.1007/s00265-007-0530-z)
13. Cameron, E. Z., Setsaas, T. H. & Linklater, W. L. 2009 Social bonds between unrelated females increase reproductive success in feral horses. Proc. Natl Acad. Sci. USA 106, 13850-13853. (doi:10.1073/pnas.0900639106)
14. Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M. & Cheney, D. L. 2009 The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc. R. Soc. B 276, 3099-3104. (doi:10.1098/rspb.2009.0681)
15. Palombit, R. A., Seyfarth, R. M. & Cheney, D. L. 1997 The adaptive value of 'friendships' to female baboons: experimental and observational evidence. Anim. Behav. 54, 599-614. (doi:10.1006/anbe.1996.0457)
16. Sueur, C. & Petit, O. 2010 Signals use by leaders in Macaca tonkeana and Macaca mulatta: group-mate recruitment and behaviour monitoring. Anim. Cogn. 13, 239-248. (doi:10.1007/s10071-009-0261-9)
17. Soltis, J. 2010 Vocal communication in African Elephants (Loxodonta africana). Zoo Biol. 29, 192-209.
18. Ramos-Fernández, G. 2005 Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? Int. J. Primatol. 26, 1077-1092. (doi:10.1007/s10764-005-6459-z)
19. Micheletta, J. & Waller, B. M. 2012 Friendship affects gaze following in a tolerant species of macaque, Macaca nigra. Anim. Behav. 83, 459-467. (doi:10.1016/j.anbehav.2011.11.018)
20. Slocombe, K., Kaller, T., Turman, L., Townsend, S., Papworth, S., Squibbs, P. & Zuberbühler, K. 2010 Production of food-associated calls in wild male chimpanzees is dependent on the composition of the audience. Behav. Ecol. Sociobiol. 64, 1959-1966. (doi:10.1007/s00265-010-1006-0)
21. Curio, E. 1978 The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z. Tierpsychol. 48, 175-183. (doi:10.1111/j.1439-0310.1978.tb00254.x)
22. Zuberbuhler, K. 2009 Survivor signals: The biology and psychology of animal alarm calling. In Advances in the study of behavior (edsM. Naguib,K. Zuberbuhler, N. S. Clayton & V. M. Janik), pp. 277-322. London: Academic Press.
23. Graw, B. & Manser, M. B. 2007 The function of mobbing in cooperative meerkats. Anim. Behav. 74, 507-517. (doi:10.1016/j.anbehav.2006.11.021)
24. Cords, M. 1997 Friendship, alliances, reciprocity and repairs. In Machiavellian intelligence II (eds A. Whiten & R. Byrne), pp. 24-49. Cambridge, UK: Cambridge University Press.
25. Lima, S. L. & Dill, L. M. 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640. (doi:10.1139/z90-092)
26. Krause, J. & Ruxton, G. 2002 Living in groups, 240 p. New York, NY: Oxford University Press.
27. Janson, C. H. 1998 Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour 135, 389-410. (doi:10.1163/156853998793066177)
28. Stanford, C. B. 2002 Avoiding predators: expectations and evidence in primate antipredator behavior. Int. J. Primatol. 23, 741-757. (doi:10.1023/A:1015572814388)
29. Blumstein, D. T., Verneyre, L. & Daniel, J. C. 2004 Reliability and the adaptive utility of discrimination among alarm callers. Proc. R. Soc. Lond. B 271, 1851-1857. (doi:10.1098/rspb.2004.2808)
30. Pollard, K. A. 2010 Making the most of alarm signals: the adaptive value of individual discrimination in an alarm context. Behav. Ecol. 22, 93-100. (doi:10.1093/beheco/arq179)
31. Ramakrishnan, U. & Coss, R. G. 2000 Age differences in the responses to adult and juvenile alarm calls by bonnet macaques (Macaca radiata). Ethology 106, 131-144. (doi:10.1046/j.1439-0310.2000.00501.x)
32. Seyfarth, R. M. & Cheney, D. L. 1997 Some general features of vocal development in nonhuman primates. In Social influence on vocal development (eds C. T. Snowdon & M. Hausberger), pp. 249-273. Cambridge, UK: Cambridge University Press.
33. Blumstein, D. T. & Daniel, J. C. 2004 Yellow-bellied marmots discriminate between the alarm calls of individuals and are more responsive to calls from juveniles. Anim. Behav. 68, 1257-1265. (doi:10.1016/j.anbehav.2003.12.024)
34. Hanson, M. T. & Coss, R. G. 2001 Age differences in the response of California ground squirrels (Spermophilus beecheyi) to conspecific alarm calls. Ethology 107, 259-275. (doi:10.1046/j.1439-0310.2001.00659.x)
35. Cheney, D. L. & Seyfarth, R. M. 1985 Vervet monkey alarm calls: manipulation through shared information? Behaviour 94, 150-166. (doi:10.1163/156853985X00316)
36. Gouzoules, H., Gouzoules, S. & Miller, K. 1996 Skeptical responding in rhesus monkeys (Macaca mulatta). Int. J. Primatol. 17, 549-568. (doi:10.1007/bf02735191)
37. Thierry, B. 2007 Unity in diversity: lessons from macaque societies. Evol. Anthropol. 16, 224-238. (doi:10.1002/evan.20147)
38. Sueur, C., Petit, O., De Marco, A., Jacobs, A. T., Watanabe, K. & Thierry, B. 2011 A comparative network analysis of social style in macaques. Anim. Behav. 82, 845-852. (doi:10.1016/j.anbehav.2011.07.020)
39. Melfi, V. 2010 Selamatkan Yaki! Conservation of Sulawesi Crested Black Macaques Macaca nigra. In Indonesian primates (eds S. Gursky & J. Supriatna), pp. 343-356. New York, NY: Springer.
40. Kinnaird, M. 1997 Shadowing black macaques. Int. Wildl. 27, 28-33.
41. Manser, M. B., Bell, M. B. & Fletcher, L. B. 2001 The information that receirvers extract from alarm calls in suricates. Proc. R. Soc. Lond. B 268, 2485-2491. (doi:10.1098/rspb.2001.1772)
42. Rosenbaum, B., O'Brien, T. G., Kinnaird, M. F. & Supriatna, J. 1998 Population densities of Sulawesi crested black macaques (Macaca nigra) on Bacan and Sulawesi, Indonesia: effects of habitat disturbance and hunting. Am. J. Primatol. 44, 89-106. (doi:10.1002/(SICI)1098-2345(1998)44:2,89::AID-AJP1.3.0.CO;2-S)
43. Collins, N. M., Sayer, J. A. & Whitmore, T. C. 1991 The conservation atlas of tropical forests: Asia and the Pacific. New York, NY: Simon & Schuster.
44. Silk, J. B., Altmann, J. & Alberts, S. 2006 Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav. Ecol. Sociobiol. 61, 183-195. (doi:10.1007/s00265-006-0249-2)
45. Schrader, L. & Hammerschmidt, K. 1997 Computer-aided analysis of acoustic parameters in animal vocalizations: a multi-parametric approach. Bioacoustics 7, 247-265. (doi:10.1080/09524622.1997.9753338)
46. Neumann, C., Assahad, G., Hammerschmidt, K., Perwitasari-Farajallah, D. & Engelhardt, A. 2010 Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species. Anim. Behav. 79, 187-193. (doi:10.1016/j.anbehav.2009.10.026)
47. Pfefferle, D., Brauch, K., Heistermann, M., Hodges, J. K. & Fischer, J. 2008 Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome. Proc. R. Soc. B 275, 571-578. (doi:10.1098/rspb.2007.1499)
48. LeRoux, A. & Bergman, T. J. 2012 Indirect rival assessment in a social primate, Theropithecus gelada. Anim. Behav. 83, 249-255. (doi:10.1016/j.anbehav.2011.10.034)
49. Mundry, R. & Sommer, C. 2007 Discriminant function analysis with nonindependent data: consequences and an alternative. Anim. Behav. 74, 965-976. (doi:10.1016/j.anbehav.2006.12.028)
50. Quinn, G. P. & Keough, M. J. 2002 Experimental design and data analysis for biologists. Cambridge, UK: Cambridge University Press.
51. Venables, W. N. & Ripley, B. D. 2002 Modern applied statistics with S, 4th edn. New York, NY: Springer.
52. R Development Core Team 2007 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www.R-project.org.
53. Bergman, T. J., Beehner, J. C., Cheney, D. L. & Seyfarth, R. M. 2003 Hierarchical classification by rank and kinship in baboons. Science 302, 1234-1236. (doi:10.1126/science.1087513)
54. de Waal, F. B. M. 1991 Rank distance as a central feature of rhesus monkey social organization: a sociometric analysis. Anim. Behav. 41, 383-395. (doi:10.1016/S0003-3472(05)80839-5)
55. de Waal, F. B. M. 1989 Food sharing and reciprocal obligations among chimpanzees. J. Hum. Evol. 18, 433-459. (doi:10.1016/0047-2484(89)90074-2)
56. de Waal, F. B. M. 1997 Food transfers through mesh in brown capuchins. J. Comp. Psychol. 111, 370-378. (doi:10.1037/0735-7036.111.4.370)
57. Petit, O. 1996 L'influence des contraintes de structure dans les comportements d'aggression et de conciliation chez plusieurs especes de primates cercopithecines. PhD thesis. Universite Louis Pasteur, Strasbourg.
58. Chapais, B. & Berman, C. 2004 Kinship and behavior in primates. New York, NY: Oxford University Press.
59. Petit, O., Abegg, C. & Thierry, B. 1997 A comparative study of aggression and conciliation in three cercopithecine monkeys (Macaca fuscata, Macaca nigra, Papio papio). Behaviour 134, 415-432. (doi:10.1163/156853997X00610)
60. Thierry, B. 2000 Covariation of conflict management patterns across macaque species. In Natural conflict resolution (eds F. Aureli & F. B. M. de Waal), pp. 106-128. Berkely, CA: University of California Press.
61. Matsumura, S. 2001 The myth of despotism and nepotism: dominance and kinship in matrilineal societies of macaques. In Primate origins of human cognition and behavior (ed. T. Matsuzawa), pp. 441-462. New York, NY: Springer.
62. Petit, O., Bertrand, F. & Thierry, B. 2008 Social play in crested and Japanese macaques: testing the covariation hypothesis. Dev. Psychobiol. 50, 399-407. (doi:10.1002/dev.20305)
63. Dobson, S. D. 2012 Coevolution of facial expression and social tolerance in macaques. Am. J. Primatol. 74, 229-235. (doi:10.1002/ajp.21991)
64. Hare, B., Melis, A. P., Woods, V., Hastings, S. & Wrangham, R. W. 2007 Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr. Biol. 17, 619-623. (doi:10.1016/j.cub.2007.02.040)
65. Thierry, B., Aureli, F., Nunn, C. L., Petit, O., Abegg, C. & deWaal, F. B.M. 2008 A comparative study of conflict resolution in macaques: insights into the nature of trait covariation. Anim. Behav. 75, 847-860. (doi:10.1016/j.anbehav.2007.07.006)
66. Sapolsky, R. M., Alberts, S. C. & Altmann, J. 1997 Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch. Gen. Psychiatry 54, 1137-1143. (doi:10.1001/archpsyc.1997.01830240097014)