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International Journal of Primatology

, Volume 35, Issue 3–4, pp 725–745 | Cite as

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

  • A. V. GeorgievEmail author
  • A. F. Russell
  • M. Emery Thompson
  • E. Otali
  • M. N. Muller
  • R. W. Wrangham
Article

Abstract

Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.

Keywords

Dominance Feeding costs Reproduction Sexual competition Tradeoff 

Notes

Acknowledgments

We thank the Ugandan Wildlife Authority, the Ugandan National Council for Science and Technology, and the Makerere University Biological Field Station at Kanyawara for research permission and field support. For discussion and comments we thank Charles Nunn, Peter Ellison, Karen Kramer, Pawel Fedurek, and members of the Behavioral Ecology Lab at the Department of Human Evolutionary Biology, Harvard University. Paco Bertolani wrote the software used for focal data collection and generously shared it. Field assistance was provided by Francis Mugurusi, Solomon Musana, James Kyomuhendo, Wilberforce Tweheyo, Sunday John, Christopher Irumba, Friday Charles, and Edgar Mugenyi. We thank Ian Gilby and Zarin Machanda for assistance with the long-term behavioral records of the Kibale Chimpanzee Project. Statistical advice and training was provided by the AnthroTree Workshop, Roger Mundry, Natalie Cooper, and Steven Worthington. We thank R. Mundry in particular for sharing his R-code. We also thank our two anonymous reviewers, James Higham, and Joanna Setchell for their very helpful comments on earlier versions of this manuscript. Funding for A. V. Georgiev was provided by the Wenner-Gren Foundation, the National Science Foundation (DDIG BCS-0925697), the International Primatological Society, the American Society of Primatologists, the Cora du Bois Trust, Harvard University, and the Institute for Mind and Biology at the University of Chicago. Long-term data-collection by the Kibale Chimpanzee Project was supported by grants from the National Science Foundation (BCS-0849380, BCS-0648481, and IOS-0416125).

References

  1. Alberts, S. C., Altmann, J., & Wilson, M. L. (1996). Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269–1277.CrossRefGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.PubMedCrossRefGoogle Scholar
  3. Andersson, M. B. (1994). Sexual selection. Princeton, NJ: Princeton University Press.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  8. Bercovitch, F. B. (1997). Reproductive strategies of rhesus macaques. Primates, 38, 247–263.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Clutton-Brock, T. H. (1998). Reproductive skew, concessions and limited control. Trends in Ecology and Evolution, 13, 288–292.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  19. Dixson, A. F. (2012). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and humans (2nd ed.). Oxford: Oxford University Press.Google Scholar
  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.CrossRefGoogle Scholar
  21. Duffy, K. G., Wrangham, R. W., & Silk, J. B. (2007). Male chimpanzees exchange political support for mating opportunities. Current Biology, 17, R586–R587.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  25. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 19, 215–223.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  29. Georgiev, A. V. (2012). Energetic costs of reproductive effort in male chimpanzees. Ph.D. dissertation: Harvard University.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  35. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Harvard University Press.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  42. Isabirye-Basuta, G. (1988). Food competition among individuals in a free-ranging chimpanzee community in Kibale Forest, Uganda. Behaviour, 105, 135–147.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  49. Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. International Journal of Primatology, 24, 1057–1075.CrossRefGoogle Scholar
  50. Miquelle, D. G. (1990). Why don’t bull moose eat during the rut? Behavioral Ecology and Sociobiology, 27, 145–151.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  54. Muller, M. N., Emery Thompson, M., & Wrangham, R. W. (2006). Male chimpanzees prefer mating with old females. Current Biology, 16, 2234–2238.PubMedCrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  60. Nakagawa, N. (2009). Feeding rate as valuable information in primate feeding ecology. Primates, 50, 131–141.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  64. Nishida, T. (2012). Chimpanzees of the lakeshore: Natural history and culture at Mahale. Cambridge, U.K.: Cambridge University Press.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  66. Packer, C. (1979). Male dominance and reproductive activity in Papio anubis. Animal Behavior, 27, 37–45.CrossRefGoogle Scholar
  67. Pelletier, F. (2005). Foraging time of rutting bighorn rams varies with individual behavior, not mating tactic. Behavioral Ecology, 16, 280–285.CrossRefGoogle Scholar
  68. Poole, J. H. (1989). Announcing intent: The aggressive state of musth in African elephants. Animal Behaviour, 37, 140–152.CrossRefGoogle Scholar
  69. Plavcan, J. M. (2012). Sexual size dimorphism, canine dimorphism, and male-male competition in primates. Human Nature, 23, 45–67.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  74. Schülke, O., Bhagavatula, J., Vigilant, L., & Ostner, J. (2010). Social bonds enhance reproductive success in male macaques. Current Biology, 20, 2207–2210.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  78. Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to sex in primates. Advances in the Study of Behavior, 33, 87–173.CrossRefGoogle Scholar
  79. Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32, 523–559.PubMedCrossRefGoogle Scholar
  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.PubMedCrossRefGoogle Scholar
  81. Stearns, S. C. (1989). Trade-offs in life-history evolution. Functional Ecology, 3, 259–268.CrossRefGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  85. Watts, D. (1998). Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 44, 43–55.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • A. V. Georgiev
    • 1
    • 5
    Email author
  • A. F. Russell
    • 2
  • M. Emery Thompson
    • 3
    • 4
  • E. Otali
    • 4
  • M. N. Muller
    • 3
    • 4
  • R. W. Wrangham
    • 1
    • 4
  1. 1.Department of Human Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.Centre for Ecology and Conservation, College of Life and Environmental SciencesUniversity of ExeterPenrynUK
  3. 3.Department of AnthropologyUniversity of New MexicoAlbuquerqueUSA
  4. 4.Kibale Chimpanzee ProjectFort PortalUganda
  5. 5.Institute for Mind and BiologyThe University of ChicagoChicagoUSA

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