Behavioral Ecology and Sociobiology

, Volume 61, Issue 6, pp 919–931 | Cite as

Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei)

  • Martha M. RobbinsEmail author
  • Andrew M. Robbins
  • Netzin Gerald-Steklis
  • H. Dieter Steklis
Original Paper


Over the past few decades, socioecological models have been developed to explain the relationships between the ecological conditions, social systems, and reproductive success of primates. Feeding competition, predation pressures, and risk of infanticide are predicted to influence how female reproductive success (FRS) depends upon their dominance rank, group size, and mate choices. This paper examines how those factors affected the reproductive success of female mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes, Rwanda from 1967–2004. Reproductive success was measured through analyses of interbirth intervals, infant survival, and surviving infant birth rates using data from 214 infants born to 67 females. Mountain gorillas were predicted to have “within-group scramble” feeding competition, but we found no evidence of lower FRS in larger groups, even as those groups became two to five times larger than the population average. The gorillas are considered to have negligible “within-group contest” competition, yet higher ranked mothers had shorter interbirth intervals. Infant survival was higher in multimale groups, which was expected because infanticide occurs when the male dies in a one-male group. The combination of those results led to higher surviving birth rates for higher ranking females in multimale groups. Overall, however, the socioecological factors accounted for a relatively small portion of the variance in FRS, as expected for a species that feeds on abundant, evenly distributed foliage.


Mountain gorilla Female reproductive success Dominance rank Group size Feeding competition Socioecological model 



We appreciate the long-term commitment of Rwanda National Office of Tourism (ORTPN) for supporting the research activities at the Karisoke Research Center. We are greatly indebted to the many researchers and field assistants, who are too numerous to mention here, for the contributions to the long-term demographic and behavioral databases of Karisoke. We thank Maryke Gray, the International Gorilla Conservation Program, and the Ranger Based Monitoring program for the use of the demographic data from the Susa Group. We thank Daniel Stahl for statistical advice and suggestions to improve the manuscript. We also thank Christophe Boesch, Oliver Schülke, Tara Stoinski, and David Watts for comments. We thank the various public and private agencies, foundations, and individuals that have provided support for the Karisoke Research Center over the last four decades. Max Planck Society provided support for data analysis and write up of the project.


  1. Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life history perspective in baboons. Am J Human Biol 15:401–409CrossRefGoogle Scholar
  2. Altmann SA, Altmann J (1977) Analysis of rates of behaviour. Anim Behav 25:364–372PubMedCrossRefGoogle Scholar
  3. Borries C, Sommer V, Srivastava A (1991) Dominance, age, and reproductive success in free ranging female Hanuman langurs (Presbytis entellus). Int J Primatol 12:231–257CrossRefGoogle Scholar
  4. Broom M, Borries C, Koenig A (2004) Infanticide and infant defence by males—modelling the conditions in primate multi-male groups. J Theor Biol 231:261–270PubMedCrossRefGoogle Scholar
  5. Chatterjee S, Price P (1991) Regression analysis by example, 2nd edn. Wiley-Interscience, New YorkGoogle Scholar
  6. Chism J, Rowell TE (1988) The natural history of patas monkeys. In: Gautier-Hion A, Bouilere F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, New York, pp 412–438Google Scholar
  7. Combes SL, Altmann J (2001) Status change during adulthood: life-history by-product or kin selection based on reproductive value? Proc R Soc Lond B Biol Sci 268:1367–1373CrossRefGoogle Scholar
  8. 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 75–98Google Scholar
  9. de Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843PubMedCrossRefGoogle Scholar
  10. Dias LG, Strier KB (2003) Effects of group size on ranging patterns in Brachyteles arachnoides hypoxanthus. Int J Primatol 24:209–221CrossRefGoogle Scholar
  11. Ellis L (1995) Dominance and reproductive success among nonhuman animals—a cross-species comparison. Ethol and Sociobiol 16:257–333CrossRefGoogle Scholar
  12. Fossey D (1983) Gorillas in the mist. Houghton Mifflin, New YorkGoogle Scholar
  13. 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
  14. Ganas J, Robbins MM (2005) Ranging behavior of the mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda: a test of the ecological constraints model. Behav Ecol Sociobiol 58:277–288CrossRefGoogle Scholar
  15. Gerald CN (1995) Demography of the Virunga mountain gorilla (Gorilla gorilla beringei). MSc thesis, Princeton University, PrincetonGoogle Scholar
  16. Gerald-Steklis CN, Steklis HD (2001) Reproductive benefits for female mountain gorillas in multi-male groups. Am J Primatol 54:60–61Google Scholar
  17. 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
  18. Gouzoules H, Gouzoules S, Fedigan L (1982) Behavioral dominance and reproductive success in female Japanese monkeys (Macaca fuscata). Anim Behav 30:1138–1150CrossRefGoogle Scholar
  19. Harcourt AH (1978) Strategies of emigration and transfer by primates, with particular reference to gorillas. Zeitschrift Fur Tierpsychologie 48:401–420PubMedGoogle Scholar
  20. Harcourt AH (1987) Dominance and fertility among female primates. J Zool Lond 213:471–487CrossRefGoogle Scholar
  21. Harcourt AH, Greenberg J (2001) Do gorilla females join males to avoid infanticide? A quantitative model. Anim Behav 62:905–915CrossRefGoogle Scholar
  22. Harcourt AH, Fossey D, Sabaterpi J (1981) Demography of Gorilla gorilla. J Zool 195:215–233CrossRefGoogle Scholar
  23. Hausfater G, Altmann J, Altmann S (1982) Long-term consistency of dominance relations among female baboons (Papio cynocephalus). Science 217:752–755CrossRefPubMedGoogle Scholar
  24. Hebblewhite M, Pletscher D (2002) Effects of elk group size on predation by wolves. Can J Zool-Revue Canadienne De Zoologie 80:800–809CrossRefGoogle Scholar
  25. Hill RA, Lee PC (1998) Predation risk as an influence on group size in cercopithecoid primates: implications for social structure. J Zool 245:447–456CrossRefGoogle Scholar
  26. Hill RA, Lycett JE, Dunbar RIM (2000) Ecological and social determinants of birth intervals in baboons. Behav Ecol 11:560–564CrossRefGoogle Scholar
  27. Holekamp KE, Smale L, Szykman M (1996) Rank and reproduction in the female spotted hyaena. J Reprod Fertil 108:229–237PubMedCrossRefGoogle Scholar
  28. Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior in primates. Behav Ecol 2:143–155CrossRefGoogle Scholar
  29. Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202CrossRefGoogle Scholar
  30. Izar P (2004) Female social relationships of Cebus apella nigritus in a southeastern Atlantic forest: an analysis through ecological models of primate social evolution. Behaviour 141:71–99CrossRefGoogle Scholar
  31. Janson CH (2000) Primate socio-ecology: the end of a golden age. Evol Anthropol 9:73–86CrossRefGoogle 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 (1988) Recognizing the many faces of primate food competition—methods. Behaviour 105:165–186Google Scholar
  34. Koenig A (2000) Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109CrossRefGoogle Scholar
  35. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783CrossRefGoogle Scholar
  36. Koenig A, Beise J, Chalise MK, Ganzhorn JU (1998) When females should contest for food—testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behav Ecol Sociobiol 42:225–237CrossRefGoogle Scholar
  37. Koenig A, Larney E, Lu A, Borries C (2004) Agonistic behavior and dominance relationships in female Phayre’s leaf monkeys—preliminary results. Am J Primatol 64:351–357PubMedCrossRefGoogle Scholar
  38. Leigh SR, Shea BT (1996) Ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43–65PubMedCrossRefGoogle Scholar
  39. McNeilage A (1995) Mountain gorillas in the Virunga volcanoes: ecology and carrying capacity. PhD thesis, University of Bristol, BristolGoogle Scholar
  40. Mori A, Watanabe K, Yamaguchi N (1989) Longitudinal changes of dominance rank among the females of the Koshima group of Japanese monkeys. Primates 30:147–173CrossRefGoogle Scholar
  41. Packer C, Collins DA, Eberly LE (2000) Problems with primate sex ratios. Philos Trans R Soc Lond B Biol Sci 355:1627–1635PubMedCrossRefGoogle Scholar
  42. Pazol K, Cords M (2005) Seasonal variation in feeding behavior, competition and female social relationships in a forest dwelling guenon, the blue monkey (Cercopithecus mitis stuhlmanni), in the Kakamega Forest, Kenya. Behav Ecol Sociobiol 58:566–577CrossRefGoogle Scholar
  43. Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831PubMedCrossRefGoogle Scholar
  44. Pusey AE, Oehlert GW, Williams JM, Goodall J (2005) Influence of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:3–31CrossRefGoogle Scholar
  45. Rhine RJ, Cox RL, Costello MB (1989) A 20-year study of long-term and temporary dominance relations among stumptailed macaques (Macaca arctoides). Am J Primatol 19:69–82CrossRefGoogle Scholar
  46. Robbins MM (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47Google Scholar
  47. Robbins MM (2001) Variation in the social system of mountain gorillas: the male perspective. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 29–58Google Scholar
  48. 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
  49. Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD (2005) Long-term dominance relationships in female mountain gorillas: strength, stability and determinants of rank. Behaviour 142:779–809CrossRefGoogle Scholar
  50. Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD (2006) Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131:511–521PubMedCrossRefGoogle Scholar
  51. Robinson JG (1988) Group size in wedge-capped capuchin monkeys, Cebus olivaceus, and the reproductive success of males and females. Behav Ecol Sociobiol 23:187–197CrossRefGoogle Scholar
  52. Rogovin K, Randall JA, Kolosova I, Moshkin M (2004) Predation on a social desert rodent, Rhombomys opimus: effect of group size, composition, and location. J Mammal 85:723–730CrossRefGoogle Scholar
  53. Samuels A, Silk JB, Altmann J (1987) Continuity and change in dominance relations among female baboons. Anim Behav 35:785–793CrossRefGoogle Scholar
  54. Schaller GB (1963) The mountain gorilla: ecology and behavior. University of Chicago Press, ChicagoGoogle Scholar
  55. Schülke O (2003) To breed or not to breed—food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55:11–21CrossRefGoogle Scholar
  56. Setchell JM, Lee PC, Wickings EJ, Dixson AF (2002) Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). Int J Primatol 23:51–68CrossRefGoogle Scholar
  57. 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
  58. 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 59–88Google Scholar
  59. Smith AC, Buchanan-Smith HM, Surridge AK, Mundy NI (2005) Factors affecting group spread within wild mixed-species troops of saddleback and mustached tamarins. Int J Primatol 26:337–355CrossRefGoogle Scholar
  60. Sokal R, Rohlf F (1995) Biometry, 3rd edn. Freeman, New YorkGoogle Scholar
  61. Srivastava A, Dunbar RIM (1996) The mating system of Hanuman langurs: a problem in optimal foraging. Behav Ecol Sociobiol 39:219–226CrossRefGoogle Scholar
  62. Steenbeek R, van Schaik CP (2001) Competition and group size in Thomas’s langurs (Presbytis thomasi): the folivore paradox revisited. Behav Ecol Sociobiol 49:100–110CrossRefGoogle Scholar
  63. Sterck EHM (1997) Determinants of female dispersal in Thomas langurs. Am J Primatol 42:179–198PubMedCrossRefGoogle Scholar
  64. Sterck EHM (1998) Female dispersal, social organization, and infanticide in langurs: are they linked to human disturbance? Am J Primatol 44:235–254PubMedCrossRefGoogle Scholar
  65. Sterck EHM, Steenbeek R (1997) Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour 134:749–774Google Scholar
  66. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  67. Stewart K, Harcourt A (1987) Gorillas: variation in female relationships. In: Smuts B, Cheney D, Seyfarth R, Wrangham W, Struhsaker T (eds) Primate societies. University of Chicago Press, Chicago, pp 155–164Google Scholar
  68. Stokes EJ (2004) Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol 64:233–246PubMedCrossRefGoogle Scholar
  69. Stokes EJ, Parnell RJ, Olejniczak C (2003) Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav Ecol Sociobiol 54:329–339CrossRefGoogle Scholar
  70. Takahata Y, Huffman MA, Suzuki S, Koyama N, Yamagiwa J (1999) Why dominants do not consistently attain high mating and reproductive success: a review of longitudinal Japanese macaque studies. Primates 40:143–158CrossRefGoogle Scholar
  71. van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130CrossRefGoogle Scholar
  72. 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, Oxford, pp 195–218Google Scholar
  73. van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proc R Soc Lond B Biol Sci 264:1687–1694CrossRefGoogle Scholar
  74. van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Infanticide by males, sex, and harassment in primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates, new and comparative perspectives. Cambridge University Press, Cambridge, pp 141–163Google Scholar
  75. Vogel ER (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344CrossRefGoogle Scholar
  76. Walters J, Seyfarth RM (1987) Conflict and cooperation. In: Smuts B, Cheney D, Seyfarth R, Wrangham W, Struhsaker T (eds) Primate societies. University of Chicago Press, Chicago, pp 306–317Google Scholar
  77. Wasser SK, Norton GW, Kleindorfer S, Rhine RJ (2004) Population trend alters the effects of maternal dominance rank on lifetime reproductive success in yellow baboons (Papio cynocephalus). Behav Ecol Sociobiol 56:338–345CrossRefGoogle Scholar
  78. Watts DP (1984) Composition and variability of mountain gorilla diets in the central Virungas. Am J Primatol 7:323–356CrossRefGoogle Scholar
  79. Watts DP (1985) Relations between group size and composition and feeding competition in mountain gorilla groups. Anim Behav 33:72–85CrossRefGoogle Scholar
  80. Watts DP (1987) Effects of mountain gorilla foraging activities on the productivity of their food plant species. Afr J Ecol 25:155–163Google Scholar
  81. Watts DP (1988) Environmental influences on mountain gorilla time budgets. Am J Primatol 15:195–211CrossRefGoogle Scholar
  82. Watts DP (1989) Infanticide in mountain gorillas—new cases and a reconsideration of the evidence. Ethology 81:1–18CrossRefGoogle Scholar
  83. Watts DP (1990a) Ecology of gorillas and its relation to female transfer in mountain gorillas. Int J Primatol 11:21–45CrossRefGoogle Scholar
  84. Watts DP (1990b) Mountain gorilla life histories, reproductive competition, and sociosexual behavior and some implications for captive husbandry. Zoo Biol 9:185–200CrossRefGoogle Scholar
  85. Watts DP (1991a) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225CrossRefGoogle Scholar
  86. Watts DP (1991b) Strategies of habitat use by mountain gorillas. Folia Primatol 56:1–16PubMedCrossRefGoogle Scholar
  87. Watts DP (1994) Agonistic relationships between female mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 34:347–358Google Scholar
  88. Watts DP (1996) Comparitive socioecology of gorillas. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. University of Cambridge, Cambridge, pp 16–28Google Scholar
  89. Watts DP (1998a) Long term habitat use by mountain gorillas (Gorilla gorilla beringei). 1. Consistency, variation, and home range size and stability. Int J Primatol 19:651–680CrossRefGoogle Scholar
  90. Watts DP (1998b) Long term habitat use by mountain gorillas (Gorilla gorilla beringei). 2. Reuse of foraging areas in relation to resource abundance, quality, and depletion. Int J Primatol 19:681–702CrossRefGoogle Scholar
  91. 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
  92. Watts DP (2001) Social relationships of female mountain gorillas. In: Robbins M, Sicotte P, Stewart K (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 215–240Google Scholar
  93. Williamson E, Gerald-Steklis N (2003) Composition of Gorilla gorilla beringei groups monitored by Karisoke Research Centre, 2001. Afr Primates 5:48–51Google Scholar
  94. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300Google Scholar
  95. Zuberbühler K, Jenny D (2002) Leopard predation and primate evolution. J Hum Evol 43:873–886PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Martha M. Robbins
    • 1
    Email author
  • Andrew M. Robbins
    • 1
  • Netzin Gerald-Steklis
    • 2
  • H. Dieter Steklis
    • 2
  1. 1.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany
  2. 2.Dian Fossey Gorilla Fund InternationalAtlantaUSA

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