Infanticide risk and male quality influence optimal group composition for Colobus vellerosus

Behavioral Ecology

Volumn 23, Issue 6, 2012, Pages 1348-1359

  Teichroeb, Julie A ^a   Wikberg, Eva C ^b   Badescu, Iulia ^c   MacDonald, Lisa J ^b   Sicotte, Pascale ^b  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

black and white colobus; group composition; intersexual conflict; intrasexual conflict.

Indexed keywords

AGGREGATION BEHAVIOR; FEMALE; GROUP SIZE; INFANTICIDE; INTRASEXUAL INTERACTION; MALE; PRIMATE; SEXUAL CONFLICT;

BOABENG-FIEMA MONKEY SANCTUARY; BRONG-AHAFO; GHANA;

EID: 84867833937     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/ars128     Document Type: Article

References (114)

1. Alexander RD. 1974. The evolution of social behavior. Ann Rev Ecol Syst. 5:325-383.
2. Alberts SC, Altmann J. 1995. Balancing costs and opportunities: dispersal in male baboons. Am Nat. 145:279-306.
3. Altmann J. 1974. Observational study of behavior: sampling methods. Behaviour. 49:227-267.
4. Argell J, Wolff JO, Ylönen H. 1998. Counter-strategies to infanticide in mammals: costs and consequences. Oikos. 83:507-517.
5. Baird RW, Dill LM. 1996. Ecological and social determinants of group size in transient killer whales. Behav Ecol. 7:408-416.
6. Blumstein DT. 2000. The evolution of infanticide in rodents: a comparative analysis. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 178-197.
7. Blundell GM, Ben-David M, Bowyer RT. 2002. Sociality in risver otters: cooperative foraging or reproductive strategies? Behav Ecol. 13:134-141.
8. Borries C. 1997. Infanticide in seasonally breeding mulitmale groups of Hanuman langurs (Presybtis entellus) in Ramnagar (South Nepal). Behav Ecol Sociobiol. 41:139-150.
9. Borries C. 2000. Male dispersal and mating season influxes in Hanuman langurs living in multimale groups. In: Kapeller PM, editor. Primate males: causes and consequences of variation in group composition. Cambridge: Cambridge University Press. p. 146-158.
10. Borries C, Koenig A. 2000. Infanticide in hanuman langurs: social organization, male migration, and weaning age. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge; Cambridge University Press. p. 99-122.
11. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P. 1999. Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups-defence pattern, paternity and sexual behaviour. Behav Ecol Sociobiol. 46:350-356.
12. Broom M, Borries C, Koenig A. 2004. Infanticide and infant defence by males-modelling the conditions in primate multi-male groups. J Theor Biol. 231:261-270.
13. Cant MA, Otali E, Mwanguhya F. 2001. Eviction and dispersal in cooperatively breeding banded mongooses (Mungos mungo). J Zool. 254:155-162.
14. Chapman CA. 1990. Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol. 26:409-414.
15. Chapman CA, Pavelka MS. 2005. Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates. 46:1-9.
16. Clarke P, Pradhan G, van Schaik C. 2009. Intersexual conflict in primates: infanticide, paternity allocation, and the role of coercion. In: Muller MN, Wrangham RW, editors. Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Cambridge (MA): Harvard University Press. p. 42-77.
17. Clutton-Brock TH, Brotherton PN, Smith R, McIlrath GM, Kansky R, Gaynor D, O'Riain MJ, Skinner JD. 1998. Infanticide and expulsion of females in a cooperative mammal. Proc Biol Sci. 265:2291-2295.
18. Collins DA. 1984. Spatial pattern in a troop of yellow baboons (Papio cyncephalus) in Tanzania. Anim Behav. 32:536-553.
19. Craig AS, Herman LM, Pack AA. 2002. Male mate choice and male-male competition coexist in the humpback whale (Megaptera novaeangliae). Can J Zool. 80:745-755.
20. Creel S, Creel NM, Mills MGL, Monfort SL. 1997. Rank and reproductive success in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav Ecol. 8:298-306.
21. Crockett CM, Janson CH. 2000. Infanticide in red howlers: female group size, group composition, and a possible link to folivory. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 75-89.
22. Davies NB. 1985. Cooperation and conflict among dunnocks, Prunella modularis, in a variable mating system. Anim Behav. 33:628-648.
23. Davies NB. 1989. Sexual conflict and the polygamy threshold. Anim Behav. 38:226-234.
24. Davies NB. 2000. Multi-male breeding groups in birds: ecological causes and social conflicts. In: Kappeler PM, editor. Primate males: causes and consequences of variation in group composition. Cambridge: Cambridge University Press. p. 11-20.
25. Dunbar RIM. 1984. Reproductive decisions: an economic analysis of gelada baboon social strategies. Princeton (NJ): Princeton University Press.
26. Ebensperger LA. 1998. Strategies and counterstrategies to infanticide in mammals. Biol Rev. 73:321-346.
27. Fargey PJ. 1991. Assessment of the conservation status of the Boabeng-Fiema Monkey Sanctuary. University of Science and Technology, Kumasi, Ghana: Final report to the Flora and Fauna Preservation Society.
28. Fashing PJ. 2001. Male and female strategies during intergroup encounters in guerezas (Colobus guereza): evidence for resource defense mediated through males and a comparison with other primates. Behav Ecol Sociobiol. 50:219-230.
29. Fedigan LM, Jack KM. 2011. Two girls for every boy: the effects of group size and composition on the reproductive success of male and female white-faced capuchins. Am J Phys Anthropol. 144:317-326.
30. Fitzmaurice G, Verbeke G. 2009. Generalized estimating equations for longitudinal data analyses. In: Fitzmaurice G, Davidian M, Verbeke G, Molenberghs G, editors. Longitudinal data analysis. Boca Raton (FL): Chapman and Hall. p. 43-78.
31. Ghisletta P, Spini D. 2004. An introduction to Generalized Estimating Equations and an application to assess selectivity effects in a longitudinal study on very old individuals. J Ed Behav St. 29:421-437.
32. Hamilton WD. 1971. Geometry for the selfish herd. J Theor Biol. 31:295-311.
33. Hardin JW, Hilbe JM. 2002. Generalized estimating equations. Boca Raton (FL): Chapman and Hall.
34. Harris TR. 2005. Roaring, intergroup aggression, and feeding competition in black and white colobus monkeys (Colobus guereza) at Kanyawara, Kibale National Park. Ph.D. Dissertation, Yale University.
35. Harris TR. 2006. Between-group contest competition for food in a highly folivorous population of black and white colobus monkeys (Colobus guereza). Behav Ecol Sociobiol. 61:317-329.
36. Harris TR. 2010. Multiple resource values and fighting ability measures influence intergroup conflict in guerezas (Colobus guereza). Anim Behav. 79:89-98.
37. Harris TR, Monfort SL. 2003. Behavioral and endocrine dynamics associated with infanticide in a black and white colobus monkey (Colobus guereza). Am J Primatol. 61:135-142.
38. Harris TR, Fitch WT, Goldstein LM, Fashing PJ. 2006. Black and white colobus monkey (Colobus guereza) roars as a source of both honest and exaggerated information about body mass. Ethology. 112:911-920.
39. Heinsohn R, Packer C. 1995. Complex cooperative strategies in group-territorial African lions. Science. 269:1260-1262.
40. Henzi SP, Barrett L. 2003. Evolutionary ecology, sexual conflict, and behavioral differentiation among baboon populations. Evol Anth. 12:217-230.
41. Holmes TD. 2011. Dispersal in a fragmented habitat: the spatial genotypic structure of Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. Master's Thesis, University of Calgary, Canada.
42. Van Hooff JARAM, van Schaik CP. 1994. Male bonds: affiliative relationships among nonhuman primate males. Behaviour. 130:309-337.
43. Hrdy SB. 1974. Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol. 22:19-58.
44. Hrdy SB. 1979. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol. 1:13-40.
45. Hrdy SB, Hausfater G. 1984. Comparative and evolutionary perspectives on infanticide: introduction and overview. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine. p. xiii-xxxv.
46. Huchard E, Alvergne A, Féjan D, Knapp LA, Cowlishaw G, Raymond M. 2010. More than friends? Behavioral and genetic aspects of heterosexual associations in wild chacma baboons. Behav Ecol Sociobiol. 64:769-781.
47. Janson CH, van Schaik CP. 2000. Behavioral ecology of infanticide. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 469-494.
48. Kappeler PM, Schäffler L. 2008. The lemur syndrome unresolved: extreme reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol. 62:1007-1015.
49. King EDA, Banks PB, Brooks RC. 2011. Sexual conflict in mammals: consequences for mating systems and life history. Mammal Rev. doi:10.1111/j.1365-2907.2011.00200.x.
50. Le Boeuf BJ. 1974. Male-male competition and reproductive success in elephant seals. Amer Zool. 14:163-176.
51. Leland L, Struhsaker TT, Butynski TM. 1984. Infanticide by adult males of three primate species of Kibale forest, Uganda, a test of hypotheses. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine. p. 151-172.
52. Möller LM. 2012. Sociogenetic structure, kin associations and bonding in delphinids. Mol Ecol. 21:745-764.
53. Newton PN. 1986. Infanticide in an undisturbed forest population of hanuman langurs, Presbytis entellus. Anim Behav. 34:785-789.
54. Nguyen N, van Horn RC, Alberts SC, Altmann J. 2009. " Friendships" between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus). Behav Ecol Sociobiol. 63:1331-1344.
55. van Noordwijk MA, van Schaik CP. 2001. Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour. 138:359-395.
56. Nunn CL. 1999. The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol. 46:1-13.
57. Nunn CL. 2000. Collective benefits, free-riders, and male extra-group conflict. In: Kappeler PM, editor. Primate males. Cambridge: Cambridge University Press. p. 192-204.
58. Nunn CL, Deaner RO. 2004. Patterns of participation and free riding in territorial conflicts among ringtailed lemurs (Lemur catta). Behav Ecol Sociobiol. 57:50-61.
59. Nunn CL, van Schaik CP. 2000. Social evolution in primates: the relative roles of ecology and intersexual conflict. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 388-412.
60. Oates JF. 1977. The social life of a black-and-white Colobus monkey, Colobus guereza. Z Tierpsychol. 45:1-60.
61. Olson M. 1965. The logic of collective action. Cambridge: Harvard University Press.
62. Ostner J, Nunn CL, Schülke O. 2008. Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol. 19:1150-1158.
63. Packer C, Herbst L, Pusey AE, Bygott JD, Hanby JP, Cairns SJ, Mulder MB. 1988. Reproductive success of lions. In: Clutton-Brock TH, editor. Reproductive success of individual variation in contrasting breeding systems. Chicago: University of Chicago Press. p. 363-383.
64. Packer C, Pusey AE. 1983. Male takeovers and female reproductive parameters: a simulation of oestrous synchrony in lions (Panthera leo). Anim Behav. 31:334-340.
65. Packer C, Pusey AE. 1984. Infanticide in carnivores. In: Hausfater G, Hrdy SB, editors. Infanticide: comparative and evolutionary perspectives. New York: Aldine. p. 31-42.
66. Packer C, Scheel D, Pusey AE. 1990. Why lions form groups: food is not enough. Am Nat. 136:1-19.
67. Palombit RA. 2010. Conflict and bonding between the sexes. In: Kappeler PM, Silk JB, editors. Mind the gap: tracing the origins of human universals. Heidelberg: Springer. p. 53-83.
68. Palombit RA, Cheney DL, Fischer J, Johnson S, Rendell D, Seyfarth RM, Silk JB. 2000. Male infanticide and defense of infants in chacma baboons. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 123-151.
69. Parmigiani S, vom Saal FS. 1994. Infanticide and parental care. London: Harwood Academic Publishers.
70. Pradhan GR, van Schaik CP. 2008. Infanticide-driven intersexual conflict over matings in primates and its effect on social organization. Behaviour. 145:251-275.
71. Rasa OAE. 1994. Altruistic infant care or infanticide: the dwarf mongooses' dilemma. In: Parmigiani S, vom Saal FS, editors. Infanticide and parental care. London: Harwood Academic Publishers. p. 301-320.
72. Robbins AM, Stoinski TS, Fawcett KA, Robbins MM. 2009. Socioecological influences on the dispersal of female mountain gorillas-evidence of a second folivore paradox. Behav Ecol Sociobiol. 63:477-489.
73. Robbins MM. 1995. A demographic analysis of male life history and social structure of mountain gorillas. Behaviour. 132:21-47.
74. Robbins MM. 2001. Variation in the social system of mountain gorillas: the male perspective. In: Robbins MM, Sicotte P, StewartKJ, editors. Mountain gorillas: three decades of research at Karisoke . New York: Cambridge University Press. p. 29-58.
75. Robbins MM, Bermejo M, Cippolletta C, Magliolocca, F, Parnell RJ, Stokes E. 2004. Social structure and life history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol. 64:145-159.
76. Roberts EK, Lu A, Bergman TJ, Beehner JC. 2012. A Bruce effect in wild geladas. Science. 335:1222-1225.
77. Ryan SD, Starks PT, Milton K, Getz WM. 2008. Intersexual conflict and group size in Alouatta palliata: a 23-year evaluation. Int J Primatol. 29:405-420.
78. Saj TL, Sicotte P. 2005. Male takeover in Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, central Ghana. Primates. 46:211-214.
79. Saj TL, Teichroeb JA, Sicotte P. 2005. The population status of the ursine colobus (Colobus vellerosus) at Boabeng-Fiema, Ghana. In: Paterson JD, Wallis J, editors. Commensalism and conflict: the human primate interface. Norman (OK): American Society of Primatologists. p. 350-375.
80. van Schaik CP. 1983. Why are diurnal primates living in groups? Behaviour. 87:120-144.
81. van Schaik CP. 1989. The ecology of social relationships amongst female primates. In: Standen V, Foley RA, editors. Comparative socioecology: the behavioural ecology of humans and other mammals. Boston; Blackwell. p. 195-218.
82. van Schaik CP. 1996. Social evolution in primates: the role of ecological factors and male behavior. Proc Br Acad. 88:9-31.
83. van Schaik CP. 2000a. Vulnerability to infanticide by males: patterns among mammals. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 61-71.
84. van Schaik CP. 2000b. Social counterstrategies against infanticide by males in primates and other mammals. In: Kappeler PM, editor. Primate males. Cambridge: Cambridge University Press. p. 34-54.
85. van Schaik CP, Dunbar RIM. 1990. The evolution of monogamy in large primates: a new hypothesis and some crucial tests. Behaviour. 115:30-62.
86. van Schaik CP, Hodges JK, Nunn CL. 2000. Paternity confusion and the ovarian cycles of female primates. In: Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 361-387.
87. van Schaik CP, Pradhan GR, van Noordwijk MA. 2004. Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates: new and comparative perspectives. Cambridge: Cambridge University Press. p. 131-150.
88. Shultz S, Opie C, Atkinson QD. 2011. Stepwise evolution of stable sociality in primates. Nature. 479:219-222.
89. Sicotte P, MacIntosh AJ. 2004. Inter-group encounters and male incursions in Colobus vellerosus in central Ghana. Behaviour. 141:533-553.
90. Sicotte P, Teichroeb JA, Saj TL. 2007. Aspects of male competition in Colobus vellerosus: preliminary data on male and female loud calling, and infant deaths after a take-over. Int J Primatol. 28:627-636.
91. Sprague DS, Suzuki S, Takahashi H, Sato S. 1998. Male life history in natural populations of Japanese macaques: migration, dominance rank, and troop participation of males in two habitats. Primates. 39:351-363.
92. Steenbeek R. 1999a. Female choice and male coercion in wild Thomas langurs. PhD Thesis, Utrecht University.
93. Steenbeek R. 1999b. Tenure-related changes in wild Thomas's langurs I: between-group interactions. Behaviour. 136:595-625.
94. Steenbeek R. 2000. Infanticide by males and female choice in wild Thomas langurs. In: van Schaik CP, Janson CH, editors. Infanticide by males and its implications. Cambridge: Cambridge University Press. p. 153-177.
95. Steenbeek R, van Schaik CP. 2001. Competition and group size in Thomas's langurs (Presbytis thomasi): the folivore paradox revisited. Behav Ecol Sociobiol. 49:100-110.
96. Stevens EF. 1990. Instability of harems of feral horses in relation to season and presence of subordinate stallions. Behaviour. 112:149-161.
97. Teichroeb JA, Sicotte P. 2008a. Infanticide in ursine colobus monkeys (Colobus vellerosus): new cases and a test of the existing hypotheses. Behaviour. 145:727-755.
98. Teichroeb JA, Sicotte P. 2008b. Social correlates of fecal testosterone in male ursine colobus monkeys (Colobus vellerosus): the effect of male reproductive competition in aseasonal breeders. Horm Behav. 54:417-423.
99. Teichroeb JA, Sicotte P. 2010. The function of male agonistic displays in ursine colobus monkeys (Colobus vellerosus): male competition, female mate choice or sexual coercion? Ethology. 116:366-380.
100. Teichroeb JA, Sicotte P. 2012. Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk, scramble competition, and infanticide threat on vigilance in ursine colobus monkeys (Colobus vellerosus). Behav Ecol Sociobiol. 66:435-466.
101. Teichroeb JA, Marteinson S, Sicotte P. 2005. Individuals' behaviors following dye-marking in wild black-and-white colobus (Colobus vellerosus). Am J Primatol. 65:197-203.
102. Teichroeb JA, Wikberg EC, Sicotte P. 2009. Female dispersal patterns in six groups of ursine colobus (Colobus vellerosus): infanticide avoidance is important. Behaviour. 146:551-582.
103. Teichroeb JA, Wikberg EC, Sicotte P. 2011. Dispersal in male ursine colobus monkeys (Colobus vellerosus): influence of age, rank and contact with other groups on dispersal decisions. Behaviour. 148:765-793.
104. Thomas GH, Székely T, Reynolds JD. 2007. Sexual conflict and the evolution of breeding systems in shorebirds. Adv Stud Behav. 37:279-342.
105. Ting N. 2008. Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. J Hum Evol. 55:312-325.
106. Treves A. 2001. Reproductive consequences of variation in the composition of howler monkey (Alouatta spp.) groups. Behav Ecol Sociobiol. 50:61-71.
107. Trivers R. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. Chicago: Aldine Publishing Co. p. 136-179.
108. Van Belle S, Estrada A. 2008. Group size and composition influence male and female reproductive success in black howler monkeys (Alouatta pigra). Am J Primatol. 70:613-619.
109. Walker NJ, Zuur AF, Ward A, Saveliev AA, Ieno EN, Smith GM. 2009. A comparison of GLM, GEE, and GLMM applied to badger activity data. In: Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM, editors. Mixed effects modes and extensions in ecology with R. New York: Springer. p. 493-502.
110. Watts DP. 1989. Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology. 81:1-18.
111. Wong SNP, Sicotte P. 2006. Comparison of the habitat quality and diet of Colobus vellerosus in forest fragments in Ghana. Am J Primatol. 68:465-476.
112. Zahavi A. 1975. Mate selection: a selection for a handicap. J Theor Biol. 53:205-214.
113. Zahavi A. 1977. The cost of honesty (further remarks on the handicap principle). J Theor Biol. 67:603-605.
114. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects modes and extensions in ecology with R, Chapter 12, Generalized estimating equations. New York: Springer. p. 295-321.