Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: Examining theories of reproductive skew

Behaviour

Volumn 146, Issue 9, 2009, Pages 1193-1215

  Stoinski, T S ^a,b   Rosenbaum, S ^a   Ngaboyamahina, T ^a   Vecellio, V ^a   Ndagijimana, F ^a   Fawcett, K ^a  

^a Dian Fossey Gorilla Fund International   (United States)

^b ZOO ATLANTA   (United States)

Author keywords

Demography; Dispersal; Flexibility; Great ape; Primate; Reproductive skew

Indexed keywords

GORILLA GORILLA BERINGEI; HOMINIDAE; LUINA; PRIMATES;

EID: 70149096441     PISSN: 00057959     EISSN: 1568539X     Source Type: Journal    
DOI: 10.1163/156853909X419992     Document Type: Article

References (68)

1. Alberts, S.C. & Altmann, J. (1995). Balancing costs and opportunities: dispersal in male baboons. - Am. Nat. 145: 279-306.
2. Alberts, S.C., Watts, H.E. & Altmann, J. (2003). Queuing the queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. - Anim. Behav. 65: 821-840.
3. Atlmann, S. (1962). A field study of the sociobiology of rhesus monkeys, Macca mulatta. - Ann. NY Acad. Sci. 102: 338-435.
4. Altmann, J. (1974). Observational study of behaviour: sampling methods. - Behaviour 48: 227-265.
5. Altmann, J., Alberts, S.C., Haines, S.A., Dubach, J., Muruthi, P., Coote, T., Geffen, E., Cheesman, D.J., Mututua, R.S., Saiyalel, S.N., Wayne, R.K., Lacy, R.C. & Bruford, M.W. (1996). Behaviour predicts genetic structure in a wild primate group. - Proc. Natl. Acad. Sci. USA 93: 5797-5801.
6. Bercovitch, F.B. (1986). Male rank and reproductive activity in savanna baboons. - Int. J. Primatol. 7: 533-550.
7. Bercovitch, F.B. & Nurnberg, P. (1996). Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). - J. Reproduct. Fert. 107: 59-68.
8. Bradley, B.B., Robbins, M.M., Williamson, E.A., Steklis, H.D., Steklis, N.G., Eckhardt, N., Boesch, C. & Vigilant, L. (2005). Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. - Proc. Natl. Acad. Sci. USA 102: 9418-9423.
9. Cant, M.A. (1998). A model for the evolution of reproductive skew without reproductive suppression. - Anim. Behav. 55: 163-169.
10. Charpentier, M., Peignot, P., Hossaert-McKey, M., Gimenez, O., Setchell, J.M. & Wickings, E.J. (2005). Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx). - Behav. Ecol. 16: 614-623.
11. Clutton-Brock, T.H. (ed.) (1988). Reproductive success. - University of Chicago Press, Chicago, IL.
12. Clutton-Brock, T.H. (1998). Reproductive skew, concessions and limited control. - Trends Ecol. Evol. 13: 288-292.
13. Clutton-Brock, T.H., Brotherton, P.N.M., Russell, A.F., O'Riain, M.J., Gaynor, D., Kan-sky, R., Griffin, R., Manser, M., Sharpe, L., McIlrath, G.M., Small, T., Moss, A. & Montfort, S. (2001). Cooperation, control, and concession in meerkat groups. - Science 291: 478-481.
14. Cowlishaw, G. & Dunbar, R.I.M. (1991). Dominance rank and mating success in male primates. - Anim. Behav. 41: 1045-1056.
15. Creel, S. & Creel, N.M. (2002). The African wild dog: behaviour, ecology and conservation. - Princeton University Press, Princeton, NJ.
16. Creel, S., Creel, N.M., Mills, M.G.L. & Montfort, S.L. (1997). Rank and reproduction in cooperatively breeding African wild dogs: behavioural and endocrine correlates. - Behav. Ecol. Sociobiol. 8: 298-306.
17. Creel, S.R. & Waser, P.M. (1991). Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation? - Behav. Ecol. 2: 7-15.
18. De Ruiter, J.R., Van Hooff, J.A.R.A.M. & Scheffrahn, W. (1994). Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). - Behaviour 129: 203-224.
19. De Vries, H., Netto, W.J. & Hanegraaf, P.L.H. (1993). Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. - Behaviour 125: 157-175.
20. Dunbar, R.I.M. (1988). Primate social systems. - Princeton University Press, Princeton, NJ.
21. Eisenberg, J.F., Muckenhirn, N.A. & Rudran, R. (1972). The relation between ecology and social structure in primates. - Science 176: 863-874.
22. Emlin, S. (1982). The evolution of helping. I and II. - Am. Nat. 119: 29-52.
23. Engh, A.L., Funk, S.M., van Horn, R.C., Scribner, K.T., Bruford, M.W., Libants, S., Szyk-man, M., Smale, L. & Holekamp, K.E. (2002). Reproductive skew among males in a female-dominated mammalian society. - Behav. Ecol. 13: 193-200.
24. Fossey, D. (1983). Gorillas in the Mist. - Houghton Mifflin, Boston, MA.
25. Girman, D.J., Mills, M.G.L., Geffen, E. & Wayne, R.K. (1997). A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). - Behav. Ecol. Sociobiol. 40: 187-198.
26. Gray, M., McNeilage, A., Fawcett, K., Robbins, M., Ssebide, J., Mbula, D. & Uwingeli, P. (in press). Censusing the mountain gorillas in the Virunga Volcanoes: complete sweep method versus monitoring. - J. Afr. Ecol.
27. Griffin, A.S. (1999). A genetic analysis of cooperative breeding in meerkats. - PhD Dissertation, University of Edinburgh, Edinburgh.
28. Griffith, S.C., Owens, I.P.F. & Thuman, K.A. (2002). Extra pair paternity in birds: a review of interspecific variation and adaptative function. - Mol. Ecol. 11: 2195-2212.
29. Hager, R. (2003). Models of reproductive skew applied to primates. - In: Sexual selection and reproductive competition in primates: new perspectives and directions (Jones, C.B., ed.). American Society of Primatologists, Norman, OK, p. 65-101.
30. Harcourt, A.H., Fossey, D. & Stewart, K.J. (1981). Gorilla reproduction in the wild. - In: Reproductive biology of the great apes (Graham, C.E., ed.). Academic Press, New York, NY, p. 265-279.
31. Harcourt, A.H., Fossey, D., Stewart, K.J. & Watts, D.P. (1980). Reproduction in wild gorillas and some comparisons with chimpanzees. - J. Reproduct. Fertil. S28: 59-70.
32. Heckel, G. & Von Helversen, O. (2003). Genetic mating system and the significance of harem associations in the bat Saccopteryx billneata. - Mol. Ecol. 112: 219-227.
33. Johnsen, A. & Lifjeld, J.T. (2003). Ecological constraints on extra-pair paternity in the blue-throat. - Oecologia 136: 476-483.
34. Johnstone, R.A. (2000). Models of reproductive skew: a review and synthesis. - Ethology 106: 526.
35. Keane, B., Waser, P.M., Creel, S.R., Creel, N.M., Elliot, L.F. & Minchella, D.J. (1994). Subordinate reproduction in dwarf mongooses. - Anim. Behav. 47: 65-75.
36. Klemme, I., Eccard, J.A., Gerlach, G., Horne, T. & Ylönen, H. (2006). Does it pay to be a dominant male in a promiscuous species? - Ann. Zool. Fenn. 43: 248-257.
37. Kutsukake, N. & Nunn, C. (2006). Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. - Behav. Ecol. Sociobiol. 60: 695-706.
38. Lebas, N.R. (2001). Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus. - Mol. Ecol. 10: 193-203.
39. Mee, A., Whitfield, D.P., Thompson, D.B.A. & Burke, T. (2004). Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting. - Anim. Behav. 67: 333-342.
40. Mitani, J.C., Gros-Louis, J. & Richard, A.F. (1996). Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. - Am. Nat. 147: 966-980.
41. Nonacs, P. (2003). Measuring the reliability of skew indices: is there one best index? - Anim. Behav. 65: 615-627.
42. Nunn, C.L. (1999). The number of males in primate social groups: a comparative test of the socioecological model. - Behav. Ecol. Sociobiol. 46: 1-13.
43. Pemberton, J.M., Albon, S.D., Guiness, F.E., Cluttonbrock, T.H. & Dover, G.A. (1992). Behavioural estimates of male mating success tested by DNA fingerprinting in a polygy-nous mammal. - Behav. Ecol. 3: 66-75.
44. Pusey, A. & Packer, C. (1987). Dispersal and philopatry. - In: Primate societies (Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W. & Struhsaker, T.T., eds). University of Chicago Press, Chicago, IL, p. 250-266.
45. Reeve, H.K., Emlen, S.T. & Keller, L. (1998). Reproductive sharing in animals societies: reproductive incentives or incomplete control by dominant breeders? - Behav. Ecol. 9: 267-278.
46. Robbins, M.M. (1995). A demographic analysis of male life history and social structure of mountain gorillas. - Behaviour 132: 21-47.
47. Robbins, M.M. (1996). Male-male interactions in heterosexual and all-male wild mountain gorilla groups. - Ethology 102: 942-965.
48. Robbins, M.M. (1999). Male mating patterns in wild multimale mountain gorilla groups. - Anim. Behav. 57: 1013-1020.
49. Robbins, M.M. (2001). Variation in the social system of mountain gorillas: the male perspective. - In: Mountain gorillas: three decades of research at Karisoke (Robbins, M.M., Sicotte, P. & Stewart, K.J., eds). Cambridge University Press, Cambridge, p. 29-58.
50. Robbins, A.M. & Robbins, M.M. (2005). Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei). - Behav. Ecol. Sociobiol. 58: 295-309.
51. Robbins, M.M., Robbins, A.M., Gerald-Steklis, N. & Steklis, H.D. (2007). Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). - Behav. Ecol. Sociobiol. 61: 919-931.
52. Robbins, A.M., Stoinski, T.S., Robbins, M.M. & Fawcett, K.A. (2009). Socioecological influences on the transfer of female mountain gorillas - evidence for a second folivore paradox. - Behav. Ecol. Sociobiol. 63: 477-498.
53. Sherman, P.W., Jarvis, J.U.M. & Alexander, R.D. (1991). The biology of the naked mole-rat. - Princeton University Press, Princeton, NJ.
54. Smith, D.G. (1993). A 15-year study of the association between dominance rank and reproductive success of male rhesus macaques. - Primates 34: 471-480.
55. Sterck, E.M.H., Watts, D.P. & van Schaik, C.P. (1997). The evolution of female social relationships in nonhuman primates. - Behav. Ecol. Sociobiol. 41: 291-309.
56. Stewart, K. & Harcourt, A. (1987). Gorillas: variation in female relationships. - In: Primate societies (Smuts, B., Cheney, C.L., Seyfarth, R.M., Wrangham, R.W. & Struhsaker, T.T., eds). University of Chicago Press, Chicago, IL, p. 155-164.
57. Stoinski, T.S., Rosenbaum, S., Vecellio, V., Ngaboyamahina, T., Ndagijimana, F., Fawcett, K. (in press). Proximate factors influencing dispersal decisions in male mountain gorillas. - Anim. Behav.
58. Trivers, R. (1972). Parental investment and sexual selection. - In: Sexual selection and the descent of man 1871-1971 (Campbell, B., ed.). Heinemann Educational Books, Chicago, p. 136-179.
59. Vehrencamp, S.L. (1979). The roles of individual, kin and group selection in the evolution of sociality. - In: Handbook of behavioural neurobiology, vol. 3. Social behaviour and communication (Marler, P. & Vandenbergh, J.G., eds). Plenum, New York, NY, p. 351-394.
60. Watts, D.P. (1984). Composition and variability of mountain gorilla diets in the central Virun-gas. - Am. J. Primatol. 7: 323-356.
61. Watts, D.P. (1989). Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. - Ethology 81: 1-18.
62. Watts, D.P. (1990). Mountain gorilla life histories, reproductive competition, and sociosexual behaviour and some implications for captive husbandry. - Zoo Biol. 9: 185-200.
63. Watts, D.P. (1991). Mountain gorilla reproduction and sexual behaviour. - Am. J. Primatol. 24: 211-225.
64. Watts, D.P. (2000). Causes and consequences of variation in male mountain gorilla life histories and group membership. - In: Primate males: causes and consequences of variation in group composition (Kappeler, P.M., ed.). Cambridge University Press, Cambridge, p. 169-179.
65. Watts, D.P. & Pusey, A.E. (1993). Behaviour of juvenile and adolescent great apes. - In: Juvenile primates (Pereira, M.E. & Fairbanks, L.A., eds). Oxford University Press, Oxford, p. 148-172.
66. Weber, A.W. & Vedder, A. (1983). Population dynamics of the Virunga gorillas: 1959-1978. - Biol. Cons. 26: 341-366.
67. Widdig, A., Bercovitch, F.B., Streich, W.J., Sauermann, U., Nürnberg, P. & Krawczak, M.A. (2004). Longitudinal analysis of reproductive skew in male rhesus macaques. - Proc. Roy. Soc. Lond. B Biol. 271: 819-826.
68. Yamagiwa, J. (1987). Male life history and the social structure of wild mountain gorillas (Gorilla gorilla beringei). - In: Evolution and coadaptation in biotic communities (Kawano, S., Connell, J.H. & Hidaka, T., eds). University of Tokyo Press, Tokyo, p. 31-51.