The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)

International Journal of Primatology

Volumn 35, Issue 3-4, 2014, Pages 725-745

  Georgiev, A V ^a,e   Russell, A F ^b   Emery Thompson, M ^c,d   Otali, E ^d   Muller, M N ^c,d   Wrangham, R W ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF NEW MEXICO   (United States)

^d Kibale Chimpanzee Project   (Uganda)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

Dominance; Feeding costs; Reproduction; Sexual competition; Tradeoff

Indexed keywords

AGGRESSION; COPULATION; DOMINANCE; FEEDING; FITNESS; FORAGING EFFICIENCY; MALE; MATING BEHAVIOR; PRIMATE; REPRODUCTION;

KANYAWARA; KIBALE NATIONAL PARK; UGANDA;

MAMMALIA; PAN; PAN TROGLODYTES; PAN TROGLODYTES SCHWEINFURTHII; PRIMATES;

EID: 84906050930     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-014-9788-y     Document Type: Article

References (93)

1. Alberts, S. C., Altmann, J., & Wilson, M. L. (1996). Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269-1277.
2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-267.
3. Andersson, M. B. (1994). Sexual selection. Princeton, NJ: Princeton University Press.
4. Barelli, C., Reichard, U. H., & Mundry, R. (2011). Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar? Animal Behaviour, 82, 801-809.
5. Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68, 255-278.
6. Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). lme4: lme4: Linear mixed-effects models using Eigen and S4. R package version 1. 1-5. http://CRAN. R-project. org/package=lme4.
7. Bercovitch, F. B. (1983). Time budgets and consortships in olive baboons (Papio anubis). Folia Primatologica, 41, 180-190.
8. Bercovitch, F. B. (1997). Reproductive strategies of rhesus macaques. Primates, 38, 247-263.
9. Bercovitch, F. B., & Nurnberg, P. (1996). Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). Journal of Reproduction and Fertility, 107, 59-68.
10. Bissonnette, A., Franz, M., Schülke, O., & Ostner, J. (2014). Socioecology, but not cognition, predicts male coalitions across primates. Behavioral Ecology. doi: 10. 1093/beheco/aru054.
11. Boesch, C., Kohou, G., Nene, H., & Vigilant, L. (2006). Male competition and paternity in wild chimpanzees of the Tai forest. American Journal of Physical Anthropology, 130, 103-115.
12. Brockman, D. K., & van Schaik, C. P. (2005). Seasonality and reproductive function. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 269-305). Cambridge, U. K.: Cambridge University Press.
13. Bronikowski, A. M., Altmann, J., Brockman, D. K., Cords, M., Fedigan, L. M., Pusey, A., Stoinski, T., Morris, W. F., Strier, K. B., & Alberts, S. C. (2011). Aging in the natural world: Comparative data reveal similar mortality patterns across primates. Science, 331, 1325-1328.
14. Clutton-Brock, T. H. (1998). Reproductive skew, concessions and limited control. Trends in Ecology and Evolution, 13, 288-292.
15. Clutton-Brock, T. H., Guiness, F. E., & Albon, S. D. (1982). Red deer: Behavior and ecology of two sexes. Chicago: University of Chicago Press.
16. Clutton-Brock, T. H., & Isvaran, K. (2007). Sex differences in ageing in natural populations of vertebrates. Proceedings of the Royal Society of London B: Biological Sciences, 274, 3097-3104.
17. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2004). Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Hormones and Behavior, 46, 204-215.
18. 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, 159-175.
19. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans (2nd ed.). Oxford: Oxford University Press.
20. Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., Carré, G., Marquéz, J. R. G., Gruber, B., Lafourcade, B., Leitão, P. J., Münkemüller, T., McClean, C., Osborne, P. E., Reineking, B., Schröder, B., Skidmore, A. K., Zurell, D., & Lautenbach, S. (2012). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36, 27-46.
21. Duffy, K. G., Wrangham, R. W., & Silk, J. B. (2007). Male chimpanzees exchange political support for mating opportunities. Current Biology, 17, R586-R587.
22. Emery, M. A., & Whitten, P. L. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioral Ecology and Sociobiology, 54, 340-351.
23. Emery Thompson, M., Muller, M. N., Wrangham, R. W., Lwanga, J. S., & Potts, K. B. (2009). Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Hormones and Behavior, 55, 299-305.
24. Emery Thompson, M., & Wrangham, R. W. (2008). Male mating interest varies with female fecundity in Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park. International Journal of Primatology, 29, 885-905.
25. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 19, 215-223.
26. Fabiani, A., Galimberti, F., Sanvito, S., & Hoelzel, A. R. (2004). Extreme polygyny among southern elephant seals on Sea Lion Island, Falkland Islands. Behavioral Ecology, 15, 961-969.
27. Fox, J., & Weisberg, S. (2011). An R Companion to Applied Regression (2nd ed.). Thousand Oaks CA: SAGE. Available at: http://socserv. socsci. mcmaster. ca/jfox/Books/Companion.
28. Galimberti, F., Sanvito, S., Braschi, C., & Boitani, L. (2007). The cost of success: Reproductive effort in male southern elephant seals (Mirounga leonina). Behavioral Ecology and Sociobiology, 62, 159-171.
29. Georgiev, A. V. (2012). Energetic costs of reproductive effort in male chimpanzees. Ph. D. dissertation: Harvard University.
30. Georgiev, A. V., Klimczuk, A. C. E., Traficonte, D. M., & Maestripieri, D. (2013). When violence pays: A cost-benefit analysis of aggressive behavior in animals and humans. Evolutionary Psychology, 11, 678-699.
31. Gilby, I. C., Brent, L. J. N., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Goodall, J., & Pusey, A. E. (2012). Fitness benefits of coalitionary aggression in male chimpanzees. Behavioral Ecology and Sociobiology, 67, 373-381.
32. Gilby, I. C., Pokempner, A. A., & Wrangham, R. W. (2010). A direct comparison of scan and focal sampling methods for measuring wild chimpanzee feeding behaviour. Folia Primatologica, 81, 254-264.
33. Girard-Buttoz, C., Heistermann, M., Rahmi, E., Marzec, A., Agil, M., Fauzan, P. A., & Engelhardt, A. (2014). Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology, 68, 583-595.
34. Gogarten, J. F., Bonnell, T. R., Brown, L. M., Campenni, M., Wasserman, M. D., & Chapman, C. A. (2014). Increasing group size alters behavior of a folivorous primate. International Journal of Primatology, 35, 590-608.
35. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Harvard University Press.
36. Harcourt, A. H., Harvey, P. H., Larson, S. G., & Short, R. V. (1981). Testis weight, body weight and breeding system in primates. Nature, 293, 55-57.
37. Henzi, S. P., Clarke, P. M. R., van Schaik, C. P., Pradhan, G. R., & Barrett, L. (2010). Infanticide and reproductive restraint in a polygynous social mammal. Proceedings of the National Academy of Sciences of the USA, 107, 2130-2135.
38. Higham, J. P., Heistermann, M., & Maestripieri, D. (2011). The energetics of male-male endurance rivalry in free-ranging rhesus macaques, Macaca mulatta. Animal Behaviour, 81, 1001-1007.
39. Hoffman, C. L., Ruiz-Lambides, A., Davila, E., Maldonado, E., Gerald, M. S., & Maestripieri, D. (2008). Sex differences in survival costs of reproduction in a promiscuous primate. Behavioral Ecology and Sociobiology, 62, 1711-1718.
40. Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346-363.
41. Inoue, E., Inoue-Murayama, M., Vigilant, L., Takenaka, O., & Nishida, T. (2008). Relatedness in wild chimpanzees: Influence of paternity, male philopatry, and demographic factors. American Journal of Physical Anthropology, 137, 256-262.
42. Isabirye-Basuta, G. (1988). Food competition among individuals in a free-ranging chimpanzee community in Kibale Forest, Uganda. Behaviour, 105, 135-147.
43. Komdeur, J. (2001). Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proceedings of the Royal Society of London B: Biological Sciences, 268, 2103-2111.
44. Kraus, C., Eberle, M., & Kappeler, P. M. (2008). The costs of risky male behaviour: Sex differences in seasonal survival in a small sexually monomorphic primate. Proceedings of the Royal Society of London B: Biological Sciences, 275, 1635-1644.
45. Lane, J. E., Boutin, S., Speakman, J. R., & Humphries, M. M. (2010). Energetic costs of male reproduction in a scramble competition mating system. Journal of Animal Ecology, 79(1), 27-34.
46. Lindburg, D. G. (1987). Seasonality of reproduction in primates. In G. Mitchell & J. M. Erwin (Eds.), Comparative primate biology (Behavior, cognition, and motivation, Vol. 2B, pp. 167-218). New York: Alan R. Liss.
47. Lukas, D., & Clutton-Brock, T. (2014). Costs of mating competition limit male lifetime breeding success in polygynous mammals. Proceedings of the Royal Society of London B: Biological Sciences, 281(1786), 20140418-20140418. doi: 10. 1098/rspb. 2014. 0418.
48. Majolo, B., Lehmann, J., de Bortoli Vizio, A., & Schino, G. (2012). Fitness-related benefits of dominance in primates. American Journal of Physical Anthropology, 147, 652-660.
49. Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. International Journal of Primatology, 24, 1057-1075.
50. Miquelle, D. G. (1990). Why don't bull moose eat during the rut? Behavioral Ecology and Sociobiology, 27, 145-151.
51. Mitani, J. C., Gros-Louis, J., & Richards, A. F. (1996). Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. American Naturalist, 147, 966-980.
52. Muller, M. N. (2002). Agonistic relations among Kanyawara chimpanzees. In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 112-124). Cambridge, U. K.: Cambridge University Press.
53. Muller, M. N., Emery Thompson, M., Kahlenberg, S. M., & Wrangham, R. W. (2011). Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behavioral Ecology and Sociobiology, 65, 921-933.
54. Muller, M. N., Emery Thompson, M., & Wrangham, R. W. (2006). Male chimpanzees prefer mating with old females. Current Biology, 16, 2234-2238.
55. Muller, M. N., Kahlenberg, S. M., & Wrangham, R. W. (2009). Male aggression against females and sexual coercion in chimpanzees. In M. N. Muller & R. W. Wrangham (Eds.), Sexual coercion in primates and humans: An evolutionary perspective on male aggression against females. Cambridge, MA: Harvard University Press.
56. Muller, M. N., & Wrangham, R. W. (2004a). Dominance, aggression and testosterone in wild chimpanzees: A test of the 'challenge hypothesis'. Animal Behaviour, 67, 113-123.
57. Muller, M. N., & Wrangham, R. W. (2004b). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 55, 332-340.
58. Murray, C. M., Lonsdorf, E. V., Eberly, L. E., & Pusey, A. E. (2009). Reproductive energetics in free-living female chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology, 20, 1211-1216.
59. Mysterud, A., Bonenfant, C., Loe, L. E., Langvatn, R., Yoccoz, N. G., & Stenseth, N. C. (2008). Age-specific feeding cessation in male red deer during rut. Journal of Zoology, 275, 407-412.
60. Nakagawa, N. (2009). Feeding rate as valuable information in primate feeding ecology. Primates, 50, 131-141.
61. Neuhaus, P., & Pelletier, F. (2001). Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Canadian Journal of Zoology, 79, 465-470.
62. Nieuwenhuis, R., te Grotenhuis, M., & Pelzer, B. (2012). Influence. ME: Tools for detecting influential data in mixed effects models. R Journal, 4, 38-47.
63. Newton-Fisher, N. E., Thompson, M. E., Reynolds, V., Boesch, C., & Vigilant, L. (2010). Paternity and social rank in wild chimpanzees (Pan troglodytes) from the Budongo Forest, Uganda. American Journal of Physical Anthropology, 142, 417-428.
64. Nishida, T. (2012). Chimpanzees of the lakeshore: Natural history and culture at Mahale. Cambridge, U. K.: Cambridge University Press.
65. Ostner, J., Heistermann, M., & Schülke, O. (2008). Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior, 54(5), 613-619.
66. Packer, C. (1979). Male dominance and reproductive activity in Papio anubis. Animal Behavior, 27, 37-45.
67. Pelletier, F. (2005). Foraging time of rutting bighorn rams varies with individual behavior, not mating tactic. Behavioral Ecology, 16, 280-285.
68. Poole, J. H. (1989). Announcing intent: The aggressive state of musth in African elephants. Animal Behaviour, 37, 140-152.
69. Plavcan, J. M. (2012). Sexual size dimorphism, canine dimorphism, and male-male competition in primates. Human Nature, 23, 45-67.
70. Promislow, D. E. L. (1992). Costs of sexual selection in natural populations of mammals. Proceedings of the Royal Society of London B: Biological Sciences, 247, 203-210.
71. Pusey, A. E., Oehlert, G. W., Williams, J. M., & Goodall, J. (2005). Influence of ecological and social factors on body mass of wild chimpanzees. International Journal of Primatology, 26, 3-31.
72. R Development Core Team (2014). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://www. R-project. org/.
73. Rasmussen, K. L. R. (1985). Changes in the activity budgets of yellow baboons (Papio cynocephalus) during sexual consortships. Behavioral Ecology and Sociobiology, 17, 161-170.
74. Schülke, O., Bhagavatula, J., Vigilant, L., & Ostner, J. (2010). Social bonds enhance reproductive success in male macaques. Current Biology, 20, 2207-2210.
75. Schülke, O., Chalise, M. K., & Koenig, A. (2006). The importance of ingestion rates for estimating food quality and energy intake. American Journal of Primatology, 68, 951-965.
76. Schülke, O., Heistermann, M., & Ostner, J. (2014). Lack of evidence for energetic costs of mate-guarding in wild male Assamese macaques (Macaca assamensis). International Journal of Primatology, 35. doi: 10. 1007/s10764-013-9748-y.
77. Setchell, J. M., Charpentier, M., & Wickings, E. J. (2005). Mate guarding and paternity in mandrills: Factors influencing alpha male monopoly. Animal Behaviour, 70(5), 1105-1120.
78. Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to sex in primates. Advances in the Study of Behavior, 33, 87-173.
79. Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32, 523-559.
80. Sobolewski, M. E., Brown, J. L., & Mitani, J. C. (2012). Female parity, male aggression, and the challenge hypothesis in wild chimpanzees. Primates, 54, 81-88.
81. Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3, 259-268.
82. Stevenson, I. R., Marrow, P., Preston, B. T., Pemberton, J. M., & Wilson, K. (2004). Adaptive reproductive strategies. In T. H. Clutton-Brock & J. M. Pemberton (Eds.), Soay sheep: Dynamics and selection in an island population. Cambridge, U. K.: Cambridge University Press.
83. Stone, A. I. (2014). Is fatter sexier? Reproductive strategies of male squirrel monkeys (Saimiri sciureus). International Journal of Primatology, 35. doi: 10. 1007/s10764-014-9755-7.
84. Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology, 6, 29-38.
85. Watts, D. (1998). Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 44, 43-55.
86. Weckerly, F. W. (1998). Sexual-size dimorphism: Influence of mass and mating systems in the most dimorphic mammals. Journal of Mammalogy, 79, 33-52.
87. Weingrill, T., Lycett, J. E., Barrett, L., Hill, R. A., & Henzi, S. P. (2003). Male consortship behaviour in chacma baboons: The role of demographic factors and female conceptive probabilities. Behaviour, 140, 405-427.
88. Wrangham, R. W. (2002). The cost of sexual attraction: Is there a trade-off in female Pan between sex appeal and received coercion? In C. Boesch, G. Hohmann, & L. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 204-215). Cambridge, U. K.: Cambridge University Press.
89. Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., & Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies. Cambridge, U. K.: Cambridge University Press.
90. Wrangham, R. W., Conklin, N. L., Chapman, C. A., & Hunt, K. D. (1991). The significance of fibrous foods for Kibale Forest chimpanzees. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 334, 171-178.
91. Wroblewski, E. E., Murray, C. M., Keele, B. F., Schumacher-Stankey, J. C., Hahn, B. H., & Pusey, A. E. (2009). Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Animal Behaviour, 77, 873-885.
92. Zuur, A. F., Ieno, E. N., & Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1, 3-14.
93. Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extension in ecology with R. New York: Springer Science+Business Media.