Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life history perspective in baboons. Am J Human Biol 15:401–409

    Article  Google Scholar 

  • Altmann SA, Altmann J (1977) Analysis of rates of behaviour. Anim Behav 25:364–372

    Article  PubMed  CAS  Google Scholar 

  • Borries C, Sommer V, Srivastava A (1991) Dominance, age, and reproductive success in free ranging female Hanuman langurs (Presbytis entellus). Int J Primatol 12:231–257

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Chatterjee S, Price P (1991) Regression analysis by example, 2nd edn. Wiley-Interscience, New York

    Google Scholar 

  • 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 412–438

    Google Scholar 

  • 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 268:1367–1373

    Article  CAS  Google Scholar 

  • 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 75–98

    Google Scholar 

  • de Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843

    Article  PubMed  Google Scholar 

  • Dias LG, Strier KB (2003) Effects of group size on ranging patterns in Brachyteles arachnoides hypoxanthus. Int J Primatol 24:209–221

    Article  Google Scholar 

  • Ellis L (1995) Dominance and reproductive success among nonhuman animals—a cross-species comparison. Ethol and Sociobiol 16:257–333

    Article  Google Scholar 

  • Fossey D (1983) Gorillas in the mist. Houghton Mifflin, New York

    Google Scholar 

  • 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 217–236

    Google Scholar 

  • 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 58:277–288

    Article  Google Scholar 

  • Gerald CN (1995) Demography of the Virunga mountain gorilla (Gorilla gorilla beringei). MSc thesis, Princeton University, Princeton

  • Gerald-Steklis CN, Steklis HD (2001) Reproductive benefits for female mountain gorillas in multi-male groups. Am J Primatol 54:60–61

    Google Scholar 

  • 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 50:329–338

    Article  Google Scholar 

  • Gouzoules H, Gouzoules S, Fedigan L (1982) Behavioral dominance and reproductive success in female Japanese monkeys (Macaca fuscata). Anim Behav 30:1138–1150

    Article  Google Scholar 

  • Harcourt AH (1978) Strategies of emigration and transfer by primates, with particular reference to gorillas. Zeitschrift Fur Tierpsychologie 48:401–420

    PubMed  CAS  Google Scholar 

  • Harcourt AH (1987) Dominance and fertility among female primates. J Zool Lond 213:471–487

    Article  Google Scholar 

  • Harcourt AH, Greenberg J (2001) Do gorilla females join males to avoid infanticide? A quantitative model. Anim Behav 62:905–915

    Article  Google Scholar 

  • Harcourt AH, Fossey D, Sabaterpi J (1981) Demography of Gorilla gorilla. J Zool 195:215–233

    Article  Google Scholar 

  • Hausfater G, Altmann J, Altmann S (1982) Long-term consistency of dominance relations among female baboons (Papio cynocephalus). Science 217:752–755

    Article  PubMed  CAS  Google Scholar 

  • Hebblewhite M, Pletscher D (2002) Effects of elk group size on predation by wolves. Can J Zool-Revue Canadienne De Zoologie 80:800–809

    Article  Google Scholar 

  • Hill RA, Lee PC (1998) Predation risk as an influence on group size in cercopithecoid primates: implications for social structure. J Zool 245:447–456

    Article  Google Scholar 

  • Hill RA, Lycett JE, Dunbar RIM (2000) Ecological and social determinants of birth intervals in baboons. Behav Ecol 11:560–564

    Article  Google Scholar 

  • Holekamp KE, Smale L, Szykman M (1996) Rank and reproduction in the female spotted hyaena. J Reprod Fertil 108:229–237

    Article  PubMed  CAS  Google Scholar 

  • Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior in primates. Behav Ecol 2:143–155

    Article  Google Scholar 

  • Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202

    Article  Google Scholar 

  • 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 141:71–99

    Article  Google Scholar 

  • Janson CH (2000) Primate socio-ecology: the end of a golden age. Evol Anthropol 9:73–86

    Article  Google Scholar 

  • Janson CH, Goldsmith ML (1995) Predicting group size in primates—foraging costs and predation risks. Behav Ecol 6:326–336

    Article  Google Scholar 

  • Janson CH, van Schaik CP (1988) Recognizing the many faces of primate food competition—methods. Behaviour 105:165–186

    Google Scholar 

  • Koenig A (2000) Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109

    Article  Google Scholar 

  • Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783

    Article  Google Scholar 

  • 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 42:225–237

    Article  Google Scholar 

  • 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 64:351–357

    Article  PubMed  Google Scholar 

  • Leigh SR, Shea BT (1996) Ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43–65

    Article  PubMed  CAS  Google Scholar 

  • McNeilage A (1995) Mountain gorillas in the Virunga volcanoes: ecology and carrying capacity. PhD thesis, University of Bristol, Bristol

  • Mori A, Watanabe K, Yamaguchi N (1989) Longitudinal changes of dominance rank among the females of the Koshima group of Japanese monkeys. Primates 30:147–173

    Article  Google Scholar 

  • Packer C, Collins DA, Eberly LE (2000) Problems with primate sex ratios. Philos Trans R Soc Lond B Biol Sci 355:1627–1635

    Article  PubMed  CAS  Google Scholar 

  • 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 58:566–577

    Article  Google Scholar 

  • Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831

    Article  PubMed  CAS  Google Scholar 

  • Pusey AE, Oehlert GW, Williams JM, Goodall J (2005) Influence of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:3–31

    Article  Google Scholar 

  • 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 19:69–82

    Article  Google Scholar 

  • Robbins MM (1995) A demographic analysis of male life history and social structure of mountain gorillas. Behaviour 132:21–47

    Google Scholar 

  • 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 29–58

    Google Scholar 

  • Robbins MM, Robbins AM (2004) Simulation of the population dynamics and social structure of the Virunga mountain gorillas. Am J Primatol 63:201–223

    Article  PubMed  Google Scholar 

  • 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 142:779–809

    Article  Google Scholar 

  • Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD (2006) Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131:511–521

    Article  PubMed  Google Scholar 

  • Robinson JG (1988) Group size in wedge-capped capuchin monkeys, Cebus olivaceus, and the reproductive success of males and females. Behav Ecol Sociobiol 23:187–197

    Article  Google Scholar 

  • 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 85:723–730

    Article  Google Scholar 

  • Samuels A, Silk JB, Altmann J (1987) Continuity and change in dominance relations among female baboons. Anim Behav 35:785–793

    Article  Google Scholar 

  • Schaller GB (1963) The mountain gorilla: ecology and behavior. University of Chicago Press, Chicago

    Google Scholar 

  • 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 55:11–21

    Article  Google Scholar 

  • Setchell JM, Lee PC, Wickings EJ, Dixson AF (2002) Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). Int J Primatol 23:51–68

    Article  Google Scholar 

  • Sicotte P (1993) Intergroup encounters and female transfer in mountain gorillas—influence of group composition on male behavior. Am J Primatol 30:21–36

    Article  Google Scholar 

  • 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 59–88

    Google Scholar 

  • 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 26:337–355

    Article  Google Scholar 

  • Sokal R, Rohlf F (1995) Biometry, 3rd edn. Freeman, New York

    Google Scholar 

  • Srivastava A, Dunbar RIM (1996) The mating system of Hanuman langurs: a problem in optimal foraging. Behav Ecol Sociobiol 39:219–226

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sterck EHM (1997) Determinants of female dispersal in Thomas langurs. Am J Primatol 42:179–198

    Article  PubMed  CAS  Google Scholar 

  • Sterck EHM (1998) Female dispersal, social organization, and infanticide in langurs: are they linked to human disturbance? Am J Primatol 44:235–254

    Article  PubMed  CAS  Google Scholar 

  • Sterck EHM, Steenbeek R (1997) Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour 134:749–774

    Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • 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 155–164

    Google Scholar 

  • Stokes EJ (2004) Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol 64:233–246

    Article  PubMed  Google Scholar 

  • Stokes EJ, Parnell RJ, Olejniczak C (2003) Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav Ecol Sociobiol 54:329–339

    Article  Google Scholar 

  • 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 40:143–158

    Article  Google Scholar 

  • 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 40:105–130

    Article  Google Scholar 

  • 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 195–218

    Google Scholar 

  • van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proc R Soc Lond B Biol Sci 264:1687–1694

    Article  Google Scholar 

  • 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 141–163

    Google Scholar 

  • Vogel ER (2005) Rank differences in energy intake rates in white-faced capuchin monkeys, Cebus capucinus: the effects of contest competition. Behav Ecol Sociobiol 58:333–344

    Article  Google Scholar 

  • 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 306–317

    Google Scholar 

  • 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 56:338–345

    Article  Google Scholar 

  • Watts DP (1984) Composition and variability of mountain gorilla diets in the central Virungas. Am J Primatol 7:323–356

    Article  Google Scholar 

  • Watts DP (1985) Relations between group size and composition and feeding competition in mountain gorilla groups. Anim Behav 33:72–85

    Article  Google Scholar 

  • Watts DP (1987) Effects of mountain gorilla foraging activities on the productivity of their food plant species. Afr J Ecol 25:155–163

    Google Scholar 

  • Watts DP (1988) Environmental influences on mountain gorilla time budgets. Am J Primatol 15:195–211

    Article  Google Scholar 

  • Watts DP (1989) Infanticide in mountain gorillas—new cases and a reconsideration of the evidence. Ethology 81:1–18

    Article  Google Scholar 

  • Watts DP (1990a) Ecology of gorillas and its relation to female transfer in mountain gorillas. Int J Primatol 11:21–45

    Article  Google Scholar 

  • Watts DP (1990b) Mountain gorilla life histories, reproductive competition, and sociosexual behavior and some implications for captive husbandry. Zoo Biol 9:185–200

    Article  Google Scholar 

  • Watts DP (1991a) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–225

    Article  Google Scholar 

  • Watts DP (1991b) Strategies of habitat use by mountain gorillas. Folia Primatol 56:1–16

    Article  PubMed  CAS  Google Scholar 

  • Watts DP (1994) Agonistic relationships between female mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 34:347–358

    Google Scholar 

  • Watts DP (1996) Comparitive socioecology of gorillas. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. University of Cambridge, Cambridge, pp 16–28

    Google Scholar 

  • 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 19:651–680

    Article  Google Scholar 

  • 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 19:681–702

    Article  Google Scholar 

  • 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 169–180

    Google Scholar 

  • 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 215–240

    Google Scholar 

  • Williamson E, Gerald-Steklis N (2003) Composition of Gorilla gorilla beringei groups monitored by Karisoke Research Centre, 2001. Afr Primates 5:48–51

    Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Google Scholar 

  • Zuberbühler K, Jenny D (2002) Leopard predation and primate evolution. J Hum Evol 43:873–886

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

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.

Author information

Authors and Affiliations

  1. Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    Martha M. Robbins & Andrew M. Robbins

  2. Dian Fossey Gorilla Fund International, 800 Cherokee Avenue SE, Atlanta, GA, 30315-1440, USA

    Netzin Gerald-Steklis & H. Dieter Steklis

Authors
  1. Martha M. Robbins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew M. Robbins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Netzin Gerald-Steklis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Dieter Steklis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martha M. Robbins.

Additional information

Communicated by D. Watts

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robbins, M.M., Robbins, A.M., Gerald-Steklis, N. et al. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav Ecol Sociobiol 61, 919–931 (2007). https://doi.org/10.1007/s00265-006-0321-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0321-y

Keywords

Search

Navigation