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Primates

, Volume 55, Issue 4, pp 489–499 | Cite as

Variance in the reproductive success of dominant male mountain gorillas

  • Andrew M. Robbins
  • Maryke Gray
  • Prosper Uwingeli
  • Innocent Mburanumwe
  • Edwin Kagoda
  • Martha M. RobbinsEmail author
Original Article

Abstract

Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.

Keywords

Brown partitions Harem size Infanticide Intra-sexual competition Male quality Mate choice Mating success Offspring survival Sexual selection 

Notes

Acknowledgments

We thank the governments of Rwanda, Democratic Republic of Congo, and Uganda for their steadfast commitment to conserving the mountain gorillas and their transboundary collaboration. We are greatly indebted to the local rangers, guides, field assistants, and staff who have worked tirelessly to protect the gorillas as well as collect the data used in this study. These men and women have shown extraordinary commitment to work during dangerous times, and approximately 100 staff members have been killed while working to protect the gorillas. The International Gorilla Conservation Programme (IGCP), a consortium of the African Wildlife Foundation, Fauna and Flora International, and the World Wide Fund for Nature, thanks all of their contributors to the Ranger Based Monitoring program. We thank Ed Wright, Juichi Yamagiwa, and anonymous reviewers for their helpful comments about the manuscript. We thank Thomas Breuer for permission to include unpublished details from (Breuer et al. 2010). The Max Planck Society provided support for data analysis and write-up of the project.

References

  1. Alberts SC (2012) Magnitude and sources of variation in male reproductive performance. In: Mitani J, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 412–431Google Scholar
  2. Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock T (ed) Reproductive success. University of Chicago Press, Chicago, pp 403–418Google Scholar
  3. Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399CrossRefGoogle Scholar
  4. 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 46:350–356CrossRefGoogle Scholar
  5. Borries C, Larney E, Lu A, Ossi K, Koenig A (2008) Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behav Ecol 19:1186–1191CrossRefGoogle Scholar
  6. Boyko RH, Marshall AJ (2009) The willing cuckold: optimal paternity allocation, infanticide and male reproductive strategies in mammals. Anim Behav 77:1397–1407CrossRefGoogle Scholar
  7. Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, 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 102:9418–9423PubMedCrossRefPubMedCentralGoogle Scholar
  8. Breuer T, Robbins AM, Olejniczak C, Parnell RJ, Stokes EJ, Robbins MM (2010) Variance in the male reproductive success of western gorillas: acquiring females is just the beginning. Behav Ecol Sociobiol 64:515–528CrossRefGoogle Scholar
  9. Breuer T, Robbins AM, Boesch C, Robbins MM (2012) Phenotypic correlates of male reproductive success in western gorillas. J Hum Evol 62:466–472PubMedCrossRefGoogle Scholar
  10. Brommer JE, Gustafsson L, Pietiainen H, Merila J (2004) Single-generation estimates of individual fitness as proxies for long-term genetic contribution. Am Nat 163:505–517PubMedCrossRefGoogle Scholar
  11. Brown D (1988) Components of lifetime reproductive success. In: Clutton-Brock T (ed) Reproductive success. University of Chicago Press, Chicago, pp 439–453Google Scholar
  12. Cabana G, Kramer DL (1991) Random offspring mortality and variation in parental fitness. Evolution 45:228–234CrossRefGoogle Scholar
  13. Caillaud D, Levrero F, Gatti S, Menard N, Raymond M (2008) Influence of male morphology on male mating status and behavior during interunit encounters in western lowland gorillas. Am J Phys Anthropol 135:379–388PubMedCrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock T (ed) Reproductive success. University of Chicago Press, Chicago, pp 384–402Google Scholar
  15. Clutton-Brock T (ed) (1988) Reproductive success. University of Chicago Press, Chicago, p 538Google Scholar
  16. Clutton-Brock TH (2004) What is sexual selection? In: Kappeler PM, van Schaik C (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, New York, pp 24–36CrossRefGoogle Scholar
  17. Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Quart Rev Biol 84:3–27PubMedCrossRefGoogle Scholar
  18. Crockett C, Janson C (2000) Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In: van Schaik C, Janson C (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 75–98CrossRefGoogle Scholar
  19. Darwin C (1871) The descent of man and selection in relation to sex. Princeton University Press, PrincetonCrossRefGoogle Scholar
  20. Dunbar R (1984) Reproductive decisions: an economic analysis of Gelada baboon social strategies. Princeton University Press, PrincetonGoogle Scholar
  21. Eisenberg JF, Muckenhirn NA, Rudran R (1972) Relation between ecology and social structure in primates. Science 176:863–864PubMedCrossRefGoogle Scholar
  22. Fossey D (1984) Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. In: Hausfater G, Hrdy S (eds) Infanticide: comparative and evolutionary perspectives. Aldine, Hawthorne, New York, pp 217–236Google Scholar
  23. Gerald CN (1995) Demography of the Virunga mountain gorilla (Gorilla gorilla beringei). In: MS Thesis in the Department of Ecology and Evolutionary Biology. Princeton University, Princeton, p 81Google Scholar
  24. Gillespie TR, Chapman CA (2001) Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model. Behav Ecol Sociobiol 50:329–338CrossRefGoogle Scholar
  25. Gray M, Kalpers J (2005) Ranger based monitoring in the Virunga-Bwindi region of East-Central Africa: a simple data collection tool for park management. Biodivers Conserv 14:2723–2741CrossRefGoogle Scholar
  26. Gray M, Roy J, Vigilant L, Fawcett K, Basabose A, Cranfield M, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM (2013) Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol Conserv 158:230–238CrossRefGoogle Scholar
  27. Hamilton WD (1964) The genetical evolution of social behavior. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  28. Harcourt AH, Stewart KJ (2007) Gorilla society: conflict, compromise, and cooperation between the sexes. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  29. Hawkes K, O’Connell JF, Jones NGB, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95:1336–1339PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male–male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:13–26PubMedCrossRefGoogle Scholar
  31. Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior in primates. Behav Ecol 2:143–155CrossRefGoogle Scholar
  32. Janson CH, Goldsmith ML (1995) Predicting group size in primates—foraging costs and predation risks. Behav Ecol 6:326–336CrossRefGoogle Scholar
  33. Janson CH, van Schaik CP (2000) The behavioral ecology of infanticide by males. In: Janson CH, van Schaik CP (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 469–494CrossRefGoogle Scholar
  34. Kalpers J, Williamson EA, Robbins MM, McNeilage A, Nzamurambaho A, Lola N, Mugiri G (2003) Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37:326–337CrossRefGoogle Scholar
  35. Kappeler PM (ed) (2000) Primate males. Cambridge University Press, Cambridge, p 316Google Scholar
  36. Kelly CD (2008) The interrelationships between resource-holding potential, resource-value and reproductive success in territorial males: how much variation can we explain? Behav Ecol Sociobiol 62:855–871CrossRefGoogle Scholar
  37. Lawler RR (2007) Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989–1999. Am J Phys Anthropol 132:267–277Google Scholar
  38. Lawler RR, Richard AF, Riley MA (2005) Intrasexual selection in Verreauxʼs sifaka (Propithecus verreauxi verreauxi). J Hum Evol 48:259–277PubMedCrossRefGoogle Scholar
  39. Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body-size dimorphism in apes. Am J Primatol 36:37–60CrossRefGoogle Scholar
  40. Majolo B, Vizioli AD, Schino G (2008) Costs and benefits of group living in primates: group size effects on behaviour and demography. Anim Behav 76:1235–1247CrossRefGoogle Scholar
  41. Morris WF, Doak DF (2004) Buffering of life histories against environmental stochasticity: accounting for a spurious correlation between the variabilities of vital rates and their contributions to fitness. Am Nat 163:579–590PubMedCrossRefGoogle Scholar
  42. Packer C, Herbst L, Pusey AE, Bygott JD, Hanby JP, Cairns SJ, Borgerfoff-Muller M (1988) Reproductive success in lions. In: Clutton-Brock T (ed) Reproductive success. University of Chicago Press, Chicago, pp 363–383Google Scholar
  43. Palombit RA (2012) Infanticide: male strategies and female counterstrategies. In: Mitani J, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 432–468Google Scholar
  44. Parnell R (2002) The social structure and behaviour of western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. Department of Psychology. University of Stirling, Stirling, p 429Google Scholar
  45. Pradhan GR, van Schaik C (2008) Infanticide-driven intersexual conflict over matings in primates and its effects on social organization. Behaviour 145:251–275CrossRefGoogle Scholar
  46. Robbins MM (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47CrossRefGoogle Scholar
  47. Robbins MM (1996) Male–male interactions in heterosexual and all-male wild mountain gorilla groups. Ethology 102:942–965CrossRefGoogle Scholar
  48. Robbins MM (1999) Male mating patterns in wild multimale mountain gorilla groups. Anim Behav 57:1013–1020PubMedCrossRefGoogle Scholar
  49. Robbins MM (2003) Behavioral aspects of sexual selection in mountain gorillas. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 477–501Google Scholar
  50. Robbins MM (2010) Gorillas: diversity in ecology and behavior. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 326–339Google Scholar
  51. Robbins MM, Robbins AM (2004) Simulation of the population dynamics and social structure of the Virunga mountain gorillas. Am J Primatol 63:201–223PubMedCrossRefGoogle Scholar
  52. Robbins AM, Robbins MM (2005) Fitness consequences of dispersal decisions for male mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 58:295–309CrossRefGoogle Scholar
  53. Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD (2007) Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 61:919–931CrossRefGoogle Scholar
  54. Robbins AM, Stoinski TS, Fawcett KA, Robbins MM (2009a) Socioecological influences on the dispersal of female mountain gorillas—evidence of a second folivore paradox. Behav Ecol Sociobiol 63:477–489CrossRefGoogle Scholar
  55. Robbins MM, Gray M, Kagoda E, Robbins AM (2009b) Population dynamics of the Bwindi mountain gorillas. Biol Conserv 142:2886–2895Google Scholar
  56. Robbins AM, Stoinski T, Fawcett K, Robbins MM (2011a) Lifetime reproductive success of female mountain gorillas. Am J Phys Anthropol 146:582–593PubMedCrossRefGoogle Scholar
  57. Robbins MM, Gray M, Fawcett KA, Nutter FB, Uwingeli P, Mburanumwe I, Kagoda E, Basabose A, Stoinski TS, Cranfield MR, Byamukama J, Spelman LH, Robbins AM (2011b) Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One 6:e19788PubMedCrossRefPubMedCentralGoogle Scholar
  58. Robbins AM, Gray M, Basabose A, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM (2013) Impact of male infanticide on the social structure of mountain gorillas. Plos One 8(11):e87256. doi: 10.1371/journal.pone.0078256
  59. Roff DA (2008) Defining fitness in evolutionary models. J Genetics 87:339–348CrossRefGoogle Scholar
  60. Rosenbaum S, Silk JB, Stoinski TS (2011) Male-immature relationships in multi-male groups of mountain gorillas (Gorilla beringei beringei). Am J Primatol 73:356–365PubMedCrossRefGoogle Scholar
  61. Schaller GB (1963) The mountain gorilla: ecology and behavior. University of Chicago Press, ChicagoGoogle Scholar
  62. Schulke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani J, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 195–219Google Scholar
  63. Setchell JM, Charpentier MJE, Abbott KM, Wickings EJ, Knapp LA (2009) Is brightest best? Testing the Hamilton–Zuk hypothesis in mandrills. Int J Primatol 30:825–844CrossRefGoogle Scholar
  64. Sicotte P (1993) Intergroup encounters and female transfer in mountain gorillas—influence of group composition on male behavior. Am J Primatol 30:21–36CrossRefGoogle Scholar
  65. Sicotte P (2001) Female mate choice in mountain gorillas. In: Robbins M, Sicotte P, Stewart K (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 59–88CrossRefGoogle Scholar
  66. Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:131–177CrossRefGoogle Scholar
  67. Snyder-Mackler N, Alberts SC, Bergman TJ (2012) Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups. Proc Royal Soc B Biol Sci 279:3788–3795CrossRefGoogle Scholar
  68. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  69. Steenbeek R, van Schaik CP (2001) Competition and group size in Thomasʼs langurs (Presbytis thomasi): the folivore paradox revisited. Behav Ecol Sociobiol 49:100–110CrossRefGoogle Scholar
  70. Stoinski TS, Rosenbaum S, Ngaboyamahina T, Vecellio V, Ndagijimana F, Fawcett K (2009) Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: examining theories of reproductive skew. Behaviour 146:1193–1215CrossRefGoogle Scholar
  71. Teichroeb JA, Wikberg EC, Badescu I, Macdonald LJ, Sicotte P (2012) Infanticide risk and male quality influence optimal group composition for Colobus vellerosus. Behav Ecol 23:1348–1359CrossRefGoogle Scholar
  72. Thoren S, Lindenfors P, Kappeler PM (2006) Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size. Am J Phys Anthropol 130:50–59PubMedCrossRefGoogle Scholar
  73. van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standon V, Foley RA (eds) Comparative socioecology: the behavioural ecology of humans and other mammals. Blackwell Scientific Publications, Oxford, pp 195–218Google Scholar
  74. Wade MJ (1987) Measuring sexual selection. In: Bradbury JW, Andersson MB (eds) Sexual selection: testing the alternatives. Chichester, New York, pp 197–207Google Scholar
  75. Wade MJ, Shuster SM (2004) Sexual selection: harem size and the variance in male reproductive success. Am Nat 164:E83–E89PubMedCrossRefGoogle Scholar
  76. Watts DP (1984) Composition and variability of mountain gorilla diets in the central Virungas. Am J Primatol 7:323–356CrossRefGoogle Scholar
  77. Watts DP (1989a) Ant eating behavior of mountain gorillas. Primates 30:121–125CrossRefGoogle Scholar
  78. Watts DP (1989b) Infanticide in mountain gorillas—new cases and a reconsideration of the evidence. Ethology 81:1–18CrossRefGoogle Scholar
  79. Watts DP (1990) Ecology of gorillas and its relation to female transfer in mountain gorillas. Int J Primatol 11:21–45CrossRefGoogle Scholar
  80. Watts DP (1994) Agonistic relationships between female mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 34:347–358CrossRefGoogle Scholar
  81. Watts DP (2000) Causes and consequences of variation in male mountain gorilla life histories and group membership. In: Kappeler PM (ed) Primate males. Cambridge University Press, Cambridge, pp 169–180Google Scholar
  82. Weber B, Vedder A (1983) Population dynamics of the Virunga gorillas: 1959–1978. Biol Conserv 26:341–366CrossRefGoogle Scholar
  83. Williamson EA, Gerald-Steklis N (2003) Composition of Gorilla gorilla beringei groups monitored by Karisoke Research Centre, 2001. African Primates 5:48–51Google Scholar
  84. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300CrossRefGoogle Scholar
  85. Yamagiwa J, Kahekwa J, Basabose AK (2003) Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates 44:359–369PubMedCrossRefGoogle Scholar
  86. Yamagiwa J, Kahekwa J, Basabose AK (2009) Infanticide and social flexibility in the genus Gorilla. Primates 50:293–303PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2014

Authors and Affiliations

  • Andrew M. Robbins
    • 1
  • Maryke Gray
    • 2
  • Prosper Uwingeli
    • 3
  • Innocent Mburanumwe
    • 4
  • Edwin Kagoda
    • 5
  • Martha M. Robbins
    • 1
    Email author
  1. 1.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.International Gorilla Conservation ProgramNairobiKenya
  3. 3.Rwanda Development BoardParc National des VolcansKigaliRwanda
  4. 4.Institut Congolais pour la Conservation de la NatureParc National des Virunga-sudGisenyiRwanda
  5. 5.Mgahinga Gorilla National Park, Uganda Wildlife AuthorityKampalaUganda

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