Advertisement

Primates

, Volume 57, Issue 1, pp 17–28 | Cite as

Group structure predicts variation in proximity relationships between male–female and male–infant pairs of mountain gorillas (Gorilla beringei beringei)

  • S. RosenbaumEmail author
  • A. A. Maldonado-Chaparro
  • T. S. Stoinski
Special Feature: Original Article Understanding the Variability of Gorilla Social Structure

Abstract

Relationships between conspecifics are influenced by both ecological factors and the social organization they live in. Systematic variation of both—consistent with predictions derived from socioecology models—is well documented, but there is considerable variation within species and populations that is poorly understood. The mountain gorilla (Gorilla beringei) is unusual because, despite possessing morphology associated with male contest competition (e.g., extreme sexual dimorphism), they are regularly observed in both single-male and multimale groups. Both male–female and male–infant bonds are strong because males provide protection against infanticide and/or predation. Risk of these threats varies with social structure, which may influence the strength of social relationships among group members (including females and offspring, if females with lower infant mortality risk are less protective of infants). Here, we investigate the relationship between group structure and the strength of proximity relationships between males and females, males and infants, and females and offspring. Data come from 10 social groups containing 1–7 adult males, monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center in Volcanoes National Park, Rwanda. After controlling for group size and infant age, association strength was similar for male–female pairs across group types with both dominant and nondominant males, but male–infant relationships were strongest in single-male groups where paternity certainty was high and animals had fewer social partners to choose from. The male:female and male:infant ratios better predicted both male–female and male–infant associations than the absolute number of males, females, or infants did. The fewer the number of males per female or infant, the more both pair types associated. Dominant males in groups containing fewer males had higher eigenvector centrality (a measure of importance in a social network) than dominant males in groups with more males. Results indicate that nondominant males are an important influence on relationships between dominant males and females/infants despite their peripheral social positions, and that relationships between males and infants must be considered an important foundation of gorilla social structure.

Keywords

Social plasticity Group structure Network centrality Variable group composition Association strength Multimale groups 

Notes

Acknowledgments

The authors wish to thank M. Robbins, J. Silk, an anonymous reviewer, and members of the Lincoln Park Zoo’s Lester E. Fisher Center and Davee Center for their helpful comments on the data and manuscript. The Karisoke Research Center is a project of the Dian Fossey Gorilla Fund International (DFGFI). The authors and DFGFI thank the Rwandan government and national park authorities for their long-term commitment to gorilla conservation and their support of the Karisoke Research Center. DFGFI is greatly indebted to the many Karisoke field assistants and researchers for their work collecting demographic and behavioral data over the last 48 years. We wish to acknowledge the many staff members who have shown extraordinary commitment under dangerous conditions, in some cases giving their lives while protecting and studying the gorillas. This work was funded by the Wenner-Gren Foundation, the LSB Leakey Foundation, the National Science Foundation (doctoral dissertation improvement grant #1122321), and the donors who support DFGFI.

Compliance with ethical standards

Conflict of interest and statement on the welfare of animals

The authors declare that they have no conflict of interest. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Altmann J (1980) Baboon mothers and infants. Harvard University Press, CambridgeGoogle Scholar
  2. Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. J Wildlife Manage 66:912–918Google Scholar
  3. Anderson DR, Link WA, Johnson DH, Burnham KP (2001) Suggestions for presenting the results of data analyses. J Wildlife Manage 65:373–378Google Scholar
  4. Boinski S (1999) The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol Anthropol 8:101–112CrossRefGoogle Scholar
  5. Bonacich P (1987) Power and centrality: a family of measures. Am J Sociol 92(5):1170–1182Google Scholar
  6. Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102:9418–9423Google Scholar
  7. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425(6954):179–181PubMedCrossRefGoogle Scholar
  8. Butts CT (2014) SNA: tools for social network analysis. R package version 2.3-2. http://CRAN.R-project.org/package=sna
  9. Caillaud D, Ndagijimana F, Giarrusso AJ, Vecellio V, Stoinski TS (2014) Mountain gorilla ranging patterns: influence of group size and group dynamics. Am J Primatol 76:730–746PubMedCrossRefGoogle Scholar
  10. Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469CrossRefGoogle Scholar
  11. Chapman CA, Rothman JM (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12–22PubMedCrossRefGoogle Scholar
  12. Clutton-Brock T, Janson C (2012) Primate socioecology at the crossroads: past, present, and future. Evol Anthropol 21(4):136–150Google Scholar
  13. Doran DM, McNeilage A (2001) Subspecific variation in gorilla behavior: the influence of ecological and social factors. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 123–150Google Scholar
  14. Elgar MA (1986) The establishment of foraging flocks in house sparrows: risk of predation and daily temperature. Behav Ecol Sociobiol 19:433–438CrossRefGoogle Scholar
  15. Emlen ST (1994) Benefits, constraints and the evolution of the family. Trends Ecol Evol 9:282–285Google Scholar
  16. Fay JM, Carroll R, Kerbis Peterhans JC, Harris D (1995) Leopard attack on and consumption of gorillas in the Central African Republic. J Hum Evol 29:93–99Google Scholar
  17. Fletcher A (1994) The social development of immature mountain gorillas (Gorilla gorilla beringei). PhD thesis. University of Bristol, BristolGoogle Scholar
  18. Fletcher A (2001) Development of infant independence from the mother in wild mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 153–182CrossRefGoogle Scholar
  19. Fossey D (1979) Development of the mountain gorilla: the first thirty-six months. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin Cummings, Menlo Park, pp 139–186Google Scholar
  20. Fossey D (1983) Gorillas in the mist. Houghton Mifflin Co., New YorkGoogle Scholar
  21. Fossey D (1984) Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. In: Hausfater G, Hrdy SB (eds) Infanticide : comparative and evolutionary perspectives. Aldine, New York, pp 217–236Google Scholar
  22. Gray M, McNeilage A, Fawcett K, Robbins MM, Ssebide B, Mbula D, Uwingeli P (2010) Censusing the mountain gorillas in the Virunga volcanoes: complete sweep method versus monitoring. African J Ecol 48:588–599Google Scholar
  23. Gray M, Roy J, Vigilant L, Fawcett K, Basabose A, Cranfield M, Uwengeli 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
  24. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:17–52PubMedCrossRefGoogle Scholar
  25. Harcourt AH (1979a) Social relationships among adult female mountain gorillas. Anim Behav 27:251–264CrossRefGoogle Scholar
  26. Harcourt AH (1979b) Social relationships between adult male and female mountain gorillas in the wild. Anim Behav 27:325–342CrossRefGoogle Scholar
  27. Harcourt AH, Greenberg J (2001) Do gorilla females join males to avoid infanticide? A quantitative model. Anim Behav 62:905–915CrossRefGoogle Scholar
  28. Harcourt AH, Stewart KJ (2007) Gorilla society: conflict, compromise, and cooperation between the sexes. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  29. Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature 293(5827):55–57PubMedCrossRefGoogle Scholar
  30. Harvey PH, Kavanagh M, Clutton-Brock TH (1978) Sexual dimorphism in primate teeth. J Zool 186:475–485CrossRefGoogle Scholar
  31. Hemelrijk CK (1999) An individual–orientated model of the emergence of despotic and egalitarian societies. Proc R Soc B 266(1417):361–369PubMedCentralCrossRefGoogle Scholar
  32. Hinde RA (1976) On describing relationships. J Child Psychol Psychiatry 17:1–19PubMedCrossRefGoogle Scholar
  33. Janson CH (1986) The mating system as a determinant of social evolution in capuchin monkeys (Cebus). In: Else JG, Lee PC (eds) Primate ecology and conservation, vol II. Cambridge University Press, Cambridge, pp 169–179Google Scholar
  34. Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740CrossRefGoogle Scholar
  35. Kappeler PM, Barrett L, Blumstein DT, Clutton-Brock TH (2013) Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Phil Trans R Soc B 368(1618):20120337PubMedPubMedCentralCrossRefGoogle Scholar
  36. Koenig A, Scarry CJ, Wheeler BC, Borries C (2013) Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain. Phil Trans R Soc B 368(1618):20120348PubMedPubMedCentralCrossRefGoogle Scholar
  37. Langos D, Kulik L, Mundry R, Widdig A (2013) The impact of paternity on male–infant association in a primate with low paternity certainty. Molecular Ecol 22:3638–3651CrossRefGoogle Scholar
  38. Leutenegger W, Kelly JT (1977) Relationship of sexual dimorphism in canine size and body size to social, behavioral, and ecological correlates in anthropoid primates. Primates 18:117–136Google Scholar
  39. Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, CambridgeGoogle Scholar
  40. Mallavarapu S, Stoinski TS, Bloomsmith MA, Maple TL (2006) Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla). Am J Primatol 68:789–801PubMedCrossRefGoogle Scholar
  41. McElreath R, Bell AV, Efferson C, Lubell M, Richerson PJ, Waring T (2008) Beyond existence and aiming outside the laboratory: estimating frequency-dependent and pay-off-biased social learning strategies. Phil Trans R Soc B 363(1509):3515–3528PubMedPubMedCentralCrossRefGoogle Scholar
  42. Møller AP (1988) Ejaculate quality, testes size and sperm competition in primates. J Hum Evol 17:479–488CrossRefGoogle Scholar
  43. Nakamichi M, Kato E (2001) Long-term proximity relationships in a captive social group of western lowland gorillas (Gorilla gorilla gorilla). Zoo Biol 20:197–209CrossRefGoogle Scholar
  44. Nunn CL (1999) The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13CrossRefGoogle Scholar
  45. Ranhau B (2000) Eigenvector-centrality—a node centrality? Soc Netw 22:357–365CrossRefGoogle Scholar
  46. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  47. Robbins MM (1996) Male–male interactions in heterosexual and all-male wild mountain gorilla groups. Ethology 102:942–965Google Scholar
  48. Robbins MM (2001) The mountain gorilla social system: the male perspective. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge, pp 29–58CrossRefGoogle Scholar
  49. 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
  50. Robbins MM, Bermejo M, Cipolletta C, Magliocca F, Parnell RJ, Stokes E (2004) Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla). Am J Primatol 64:145–159PubMedCrossRefGoogle Scholar
  51. Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD (2006) Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131:511–521PubMedCrossRefGoogle Scholar
  52. 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
  53. Robbins MM, Gray M, Kagoda E, Robbins AM (2009) Population dynamics of the Bwindi mountain gorillas. Biol Conserv 142:2886–2895CrossRefGoogle Scholar
  54. 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:e78256PubMedPubMedCentralCrossRefGoogle Scholar
  55. Robbins AM, Gray M, Uwingeli P, Mburanumwe I, Kagoda E, Robbins MM (2014) Variance in the reproductive success of dominant male mountain gorillas. Primates 55:489–499PubMedCrossRefGoogle Scholar
  56. 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
  57. Rosenbaum S, Hirwa JP, Silk JB, Vigilant L, Stoinski TS (2015) Male rank, not paternity, predicts male-immature relationships in mountain gorillas, Gorilla beringei beringei. Anim Behav 104:13–24CrossRefGoogle Scholar
  58. Schaller GE (1963) The mountain gorilla: ecology and behavior. University of Chicago Press, OxfordGoogle Scholar
  59. Schradin C, Pillay N (2005) Intraspecific variation in the spatial and social organization of the African striped mouse. J Mammal 86:99–107CrossRefGoogle Scholar
  60. Schultz AH (1969) The life of primates. Weidenfeld and Nicolson, LondonGoogle Scholar
  61. Sicotte P (1994) Effect of male competition on male-female relationships in bi-male groups of mountain gorillas. Ethology 97:47–64CrossRefGoogle Scholar
  62. Sterck EHM (1999) Variation in langur social organization in relation to the socioecological model, human habitat alteration, and phylogenetic constraints. Primates 40:199–213PubMedCrossRefGoogle Scholar
  63. Stewart KJ (2001) Social relationships of immature gorillas and silverbacks. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, Cambridge UK, pp 184–213Google Scholar
  64. Stoinski TS, Hoff MP, Tl Maple (2003) Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the 6 months after parturition. Am J Primatol 61:61–72PubMedCrossRefGoogle Scholar
  65. Stoinski TS, Rosenbaum S, Ngaboyamahina T, Vecellio V, Ndagijimana F, Fawcett K (2009a) Patterns of male reproductive behaviour in multi-male groups of mountain gorillas: examining theories of reproductive skew. Behaviour 146:1193–1215CrossRefGoogle Scholar
  66. Stoinski TS, Vecellio V, Ngaboyamahina T, Ndagijimana F, Rosenbaum S, Fawcett KA (2009b) Proximate factors influencing dispersal decisions in male mountain gorillas, Gorilla beringei beringei. Anim Behav 77:1155–1164CrossRefGoogle Scholar
  67. Trivers R (1972) Parental investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man. Aldine de Gruyter, Chicago, pp 136–179Google Scholar
  68. van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87(1/2):120–144CrossRefGoogle Scholar
  69. van Schaik CP (1996) Social evolution in primates: the role of ecological factors and male behaviour. Proc Brit Acad vol 88. Oxford University Press, Oxford, pp 9–31)Google Scholar
  70. Viblanc VA, Arnaud CM, Dobson FS, Murie JO (2010) Kin selection in Columbian ground squirrels (Urocitellus columbianus): littermate kin provide individual fitness benefits. Proc R Soc Lond B 277:989–994CrossRefGoogle Scholar
  71. Vigilant L, Roy J, Bradley BJ, Stoneking CJ, Robbins MM, Stoinski TS (2015) Reproductive competition and inbreeding avoidance in a primate species with habitual female dispersal. Behav Ecol Sociobiol 69:1163–1172Google Scholar
  72. Warren Y, Williamson EA (2001) Carriage of infants by a silverback mountain gorilla. Folia Primatol 72:245–247PubMedCrossRefGoogle Scholar
  73. Watts DP (1989) Infanticide in mountain gorillas: new cases and a reconsideration of the evidence. Ethology 81:1–18CrossRefGoogle Scholar
  74. Watts DP (1992) Social relationships of immigrant and resident female mountain gorillas. I. Male–female relationships. Am J Primatol 28:159–181Google Scholar
  75. Watts DP (1994) Social relationships of immigrant and resident female mountain gorillas, II: relatedness, residence, and relationships between females. Am J Primatol 32:13–30CrossRefGoogle Scholar
  76. Watts D, Pusey A (1993) Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks L (eds) Juvenile primates: life history, development and behavior. University of Chicago Press, Chicago, pp 148–167Google Scholar
  77. Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344CrossRefGoogle Scholar
  78. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  79. Wolf JB, Trillmich F (2008) Kin in space: social viscosity in a spatially and genetically substructured network. Proc R Soc Lond B 275:2063–2069CrossRefGoogle Scholar
  80. Yamagiwa J (1983) Diachronic changes in two eastern lowland gorilla groups (Gorilla gorilla graueri) in the Mt. Kahuzi region, Zaire. Primates 24:174–183CrossRefGoogle Scholar
  81. Yamagiwa J (1987) Intra- and inter-group interactions of an all-male group of Virunga mountain gorillas. Primates 28:1–30CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2015

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of California—Los AngelesLos AngelesUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of California—Los AngelesLos AngelesUSA
  3. 3.The Dian Fossey Gorilla Fund InternationalAtlantaUSA
  4. 4.Institute for Mind and BiologyUniversity of ChicagoChicagoUSA

Personalised recommendations