Advertisement

Behavioral Ecology and Sociobiology

, Volume 68, Issue 11, pp 1785–1797 | Cite as

Proximate mechanisms of contest competition among female Bwindi mountain gorillas (Gorilla beringei beringei)

  • Edward Wright
  • Martha M. Robbins
Original Paper

Abstract

Socioecological models provide a framework for predicting how animals respond competitively to the abundance and distribution of food resources. Testing predictions of socioecological models requires analysis of relationships among food resource characteristics, competitive behaviors, and measures of rank-related skew in energy balance or reproductive success. A positive relationship between dominance rank and energy balance has been observed among female mountain gorillas in Bwindi Impenetrable National Park, Uganda. This study examines the proximate mechanisms underlying feeding competition among those females. To assess the contestability of food resources, we measured the time a female spent feeding at a food site (food site residence time). We also examined the relationship between dominance rank and the access to resources, as well as the rate, context, and direction of aggression, and the number of neighbors in close proximity. As predicted, females had longer food site residence times and higher aggression rates with fruit and decaying wood than with herbaceous vegetation, suggesting that those resources may be contestable. Aggression was predominantly directed down the dominance hierarchy, although against expectation, rank was not significantly correlated with aggression rates or the time spent feeding on contestable foods. Higher-ranking females had significantly fewer neighbors, suggesting that lower-ranking females avoid higher-ranking ones. This study provides additional support for the claim that there is variability in how primates respond to the quality and distribution of food resources and that avoidance as a strategy to cope with feeding competition may result in similar skew in energy balance as rank-related aggression.

Keywords

Aggression Contest competition Socioecological model Bwindi mountain gorillas 

Notes

Acknowledgments

We thank the Uganda Wildlife Authority and the Ugandan National Council for Science and Technology for permission to work in Bwindi Impenetrable National Park. We are grateful to the Institute of Tropical Forest Conservation for logistical support. A special thanks goes to all members of the gorilla research team, including Dennis Musinguzi, Beda Turyananuka, Tibenda Emmanuel, Caleb Ngamganeza, Gervasio Byaruhanga, and Edson Nzabarinda. We are extremely grateful to Roger Mundry, Colleen Stephens, and Andrew M. Robbins for statistical support. We thank Christophe Boesch and particularly Andrew M. Robbins for helpful discussion and constructive criticism on earlier versions of this manuscript. This project was funded by the Max Planck Society.

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical standards

This study complied with all Uganda Wildlife Authority regulations.

Supplementary material

265_2014_1788_MOESM1_ESM.doc (222 kb)
ESM 1 (DOC 222 kb)

References

  1. Adams DC, Anthony CD (1996) Using randomization techniques to analyse behavioural data. Anim Behav 51:733–738CrossRefGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedCrossRefGoogle Scholar
  3. Baayen RH (2008) Analyzing linguistic data: a practical introduction to statistics using R, 1st edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  4. Barr DJ, Levy R, Scheepers C, Tily HJ (2013) Random effects structure for confirmatory hypothesis testing: keep it maximal. J Mem Lang 68:255–278CrossRefGoogle Scholar
  5. Barton RA (1993) Sociospatial mechanisms of feeding competition in female olive baboons, Papio anubis. Anim Behav 46:791–802CrossRefGoogle Scholar
  6. Barton RA, Whiten A (1993) Feeding competition among female olive baboons, Papio anubis. Anim Behav 46:777–789CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4, http://CRAN.R-project.org/package=lme4
  8. Chancellor RL, Isbell LA (2008) Punishment and competition over food in captive rhesus macaques, Macaca mulatta. Anim Behav 75:1939–1947CrossRefGoogle Scholar
  9. Chancellor RL, Isbell LA (2009) Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behav Ecol Sociobiol 63:1447–1458PubMedCrossRefPubMedCentralGoogle Scholar
  10. Chapman CA, Rothman JM, Lambert JE (2012) Food as a selective force in primates. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University Of Chicago Press, Chicago, pp 149–168Google Scholar
  11. Chaves OM, Stoner KE, Ángeles-Campos S, Arroyo-Rodríguez V (2011) Wood consumption by Geoffroy’s spider monkeys and its role in mineral supplementation. PLoS ONE 6:e25070PubMedCrossRefPubMedCentralGoogle Scholar
  12. Clutton-Brock T, Huchard E (2013) Social competition and its consequences in female mammals. J Zool 289:151–171CrossRefGoogle Scholar
  13. Clutton-Brock T, Janson C (2012) Primate socioecology at the crossroads: past, present, and future. Evol Anthropol 21:136–150PubMedCrossRefGoogle Scholar
  14. R Core Team (2013) A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria, http://www.R-project.org/
  15. Côté SD (2000) Dominance hierarchies in female mountain goats: stability, aggressiveness and determinants of rank. Behaviour 1541–1566Google Scholar
  16. Dobson AJ, Barnett AG (2001) An introduction to generalized linear models, 2nd edn. Chapman and Hall/CRC, FloridaCrossRefGoogle Scholar
  17. Field AP (2005) Discovering statistics using SPSS. SAGE Publications, LondonGoogle Scholar
  18. Foerster S, Cords M, Monfort SL (2011) Social behavior, foraging strategies, and fecal glucocorticoids in female blue monkeys (Cercopithecus mitis): potential fitness benefits of high rank in a forest guenon. Am J Primatol 73:870–882PubMedCrossRefGoogle Scholar
  19. Fournier F, Festa-Bianchet M (1995) Social dominance in adult female mountain goats. Anim Behav 49:1449–1459CrossRefGoogle Scholar
  20. Fox J, Weisberg S (2011) An {R} companion to applied regression. Sage, Thousand OaksGoogle Scholar
  21. Fürtbauer I, Mundry R, Heistermann M et al (2011) You mate, I mate: macaque females synchronize sex not cycles. PLoS ONE 6:e26144PubMedCrossRefPubMedCentralGoogle Scholar
  22. Ganas J, Robbins MM, Nkurunungi J et al (2004) Dietary variability of mountain gorillas in Bwindi impenetrable National Park, Uganda. Int J Primatol 25:1043–1072CrossRefGoogle Scholar
  23. Ganas J, Ortmann S, Robbins MM (2009) Food choices of the mountain gorilla in Bwindi Impenetrable National Park, Uganda: the influence of nutrients, phenolics and availability. J Trop Ecol 25:123CrossRefGoogle Scholar
  24. Gemmill A, Gould L (2008) Microhabitat variation and its effects on dietary composition and intragroup feeding interactions between adult female lemur catta during the dry season at Beza Mahafaly Special Reserve, Southwestern Madagascar. Int J Primatol 29:1511–1533CrossRefGoogle Scholar
  25. Grant JWA, Guha RT (1993) Spatial clumping of food increases its monopolization and defense by convict cichlids, Cichlasoma nigrofasciatum. Behav Ecol 4:293–296CrossRefGoogle Scholar
  26. Hall CL, Fedigan LM (1997) Spatial benefits afforded by high rank in white-faced capuchins. Anim Behav 53:1069–1082CrossRefGoogle Scholar
  27. Harcourt AH (1979) Social relationships among adult female mountain gorillas. Anim Behav 27:251–264CrossRefGoogle Scholar
  28. Harcourt AH, Stewart KJ (1989) Functions of alliances in contests within wild gorilla groups. Behaviour 109:176–190CrossRefGoogle Scholar
  29. Harris TR (2006) Between-group contest competition for food in a highly folivorous population of black and white colobus monkeys (Colobus guereza). Behav Ecol Sociobiol 61:317–329CrossRefGoogle Scholar
  30. Hirsch BT (2011) Within-group spatial position in ring-tailed coatis: balancing predation, feeding competition, and social competition. Behav Ecol Sociobiol 65:391–399CrossRefGoogle Scholar
  31. Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155CrossRefGoogle Scholar
  32. 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
  33. Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123–133CrossRefGoogle Scholar
  34. Janson C (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 18:125–138CrossRefGoogle Scholar
  35. Janson CH (1990) Ecological consequences of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus apella. Anim Behav 40:922–934CrossRefGoogle Scholar
  36. Koenig A (2000) Competitive regimes in forest-dwelling Hanuman langur females (Semnopithecus entellus). Behav Ecol Sociobiol 48:93–109CrossRefGoogle Scholar
  37. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783CrossRefGoogle Scholar
  38. Koenig A, Borries C (2006) The predictive power of socioecological models: a reconsideration of resource characteristics, agonism, and dominance heirarchies. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates: ecology physiology and behavioral aspects. Cambridge University Press, pp 263 –284Google Scholar
  39. Koenig A, Borries C (2009) The lost dream of ecological determinism: time to say goodbye? … Or a White Queen’s proposal? Evol Anthropol 18:166–174CrossRefGoogle Scholar
  40. 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
  41. 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. Philos T Roy Soc B 368:20120348CrossRefGoogle Scholar
  42. Korstjens AH, Bergmann K, Deffernez C et al (2007) How small-scale differences in good competition lead to different social systems in three closely related sympatric colobines. In: McGraw S, Zuberbühler K, Noë R (eds) Monkeys in the Taï forest: an African primate community. Cambridge University Press, UK, pp 72–108Google Scholar
  43. Krause J (1994) Differential fitness returns in relation to spatial position in groups. Biol Rev 69:187–206PubMedCrossRefGoogle Scholar
  44. Manly BFJ (1997) Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall, New YorkGoogle Scholar
  45. Mathy JW, Isbell LA (2001) The relative importance of size of food and interfood distance in eliciting aggression in captive rhesus macaques (Macaca mulatta). Folia Primatol 72:268–277PubMedCrossRefGoogle Scholar
  46. McCullagh P, Nelder JA (2008) Generalized linear models. Chapman & Hall, LondonGoogle Scholar
  47. Nkurunungi JB, Ganas J, Robbins MM, Stanford CB (2004) A comparison of two mountain gorilla habitats in Bwindi Impenetrable National Park, Uganda. Afr J Ecol 42:289–297CrossRefGoogle Scholar
  48. Nsubuga AM, Robbins MM, Boesch C, Vigilant L (2008) Patterns of paternity and group fission in wild multimale mountain gorilla groups. Am J Phys Anthropol 135:263–274PubMedCrossRefGoogle Scholar
  49. Packer C, Pusey AE, Eberly LE (2001) Egalitarianism in female African lions. Science 293:690–693PubMedCrossRefGoogle Scholar
  50. Polansky L, Robbins MM (2013) Generalized additive mixed models for disentangling long-term trends, local anomalies, and seasonality in fruit tree phenology. Ecol Evol 3:3141–3151PubMedCrossRefPubMedCentralGoogle Scholar
  51. Post DG, Hausfater G, McCuskey SA (1980) Feeding behavior of yellow baboons (Papio cynocephalus): relationship to age, gender and dominance rank. Folia Primatol 34:170–195PubMedCrossRefGoogle Scholar
  52. Pruetz JD, Isbell LA (2000) Correlations of food distribution and patch size with agonistic interactions in female vervets (Chlorocebus aethiops) and patas monkeys (Erythrocebus patas) living in simple habitats. Behav Ecol Sociobiol 49:38–47CrossRefGoogle Scholar
  53. Reynolds V, Lloyd AW, Babweteera F, English CJ (2009) Decaying Raphia farinifera palm trees provide a source of sodium for wild chimpanzees in the Budongo Forest, Uganda. PLoS ONE 4:e6194PubMedCrossRefPubMedCentralGoogle Scholar
  54. Robbins MM (2008) Feeding competition and agonistic relationships among Bwindi Gorilla beringei. Int J Primatol 29:999–1018CrossRefGoogle Scholar
  55. Robbins MM (2011) Gorillas: diversity in ecology and behavior. In: Campbell CJ, Fuentes A, MacKinnon K, Bearder SK, Stumpf RM (eds) Primates perspect. Oxford University Press, New York, pp 326–339Google Scholar
  56. 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
  57. 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
  58. Robbins MM, Gray M, Kagoda E, Robbins AM (2009) Population dynamics of the Bwindi mountain gorillas. Biol Conserv 142:2886–2895CrossRefGoogle Scholar
  59. Robbins AM, Stoinski T, Fawcett K, Robbins MM (2011) Lifetime reproductive success of female mountain gorillas. Am J Phys Anthropol 146:582–593PubMedCrossRefGoogle Scholar
  60. Roberts S-J, Cords M (2013) Group size but not dominance rank predicts the probability of conception in a frugivorous primate. Behav Ecol Sociobiol 67:1995–2009CrossRefGoogle Scholar
  61. Ron T, Henzi SP, Motro U (1996) Do female chacma baboons compete for a safe spatial position in a southern woodland habitat? Behaviour 133:475–490CrossRefGoogle Scholar
  62. Rothman JM, van Soest PJ, Pell AN (2006) Decaying wood is a sodium source for mountain gorillas. Biol Lett 2:321–324PubMedCrossRefPubMedCentralGoogle Scholar
  63. Saito C (1996) Dominance and feeding success in female Japanese macaques, (Macaca fuscata) effects of food patch size and inter-patch distance. Anim Behav 51:967–980CrossRefGoogle Scholar
  64. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  65. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420PubMedCrossRefPubMedCentralGoogle Scholar
  66. Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. University of Chicago Press, Chicago, pp 197–218Google Scholar
  67. Snaith TV, Chapman CA (2007) Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol 16:94–106CrossRefGoogle Scholar
  68. Sterck EHM, Steenbeek R (1997) Female dominance relationships and food competition in the sympatric thomas langur and long-tailed macaque. Behaviour 134:749–774CrossRefGoogle Scholar
  69. Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309CrossRefGoogle Scholar
  70. Stewart KJ, Harcourt AH (1987) Gorillas: variation in female relationships. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 155–164Google Scholar
  71. Thouless CR (1990) Feeding competition between grazing red deer hinds. Anim Behav 40:105–111CrossRefGoogle Scholar
  72. van Noordwijk MA, van Schaik CP (1987) Competition among female long-tailed macaques (Macaca fascicularis). Anim Behav 35:577–589CrossRefGoogle Scholar
  73. van Schaik C (1989) The ecology of social relationships among female primates. In: Standen V, Foley R (eds) Comparative socioecology, the behavioral ecology of humans and other mammals. Blackwells, Oxford, pp 195–218Google Scholar
  74. 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
  75. Vogel ER, Janson CH (2007) Predicting the frequency of food‐related agonism in white‐faced capuchin monkeys (Cebus capucinus), using a novel focal‐tree method. Am J Primatol 69:533–550. doi: 10.1002/ajp.20368 PubMedCrossRefGoogle Scholar
  76. Vogel ER, Janson CH (2011) Quantifying primate food distribution and abundance for socioecological studies: an objective consumer-centered method. Int J Primatol 32:737–754CrossRefGoogle Scholar
  77. Watts DP (1984) Composition and variability of mountain gorilla diets in the Central Virungas. Am J Primatol 7:323–356CrossRefGoogle Scholar
  78. Watts DP (1985) Relations between group size and composition and feeding competition in mountain gorilla groups. Anim Behav 33:72–85CrossRefGoogle Scholar
  79. Watts DP (1994) Agonistic relationships between female mountain gorillas (Gorilla gorilla beringei). Behav Ecol Sociobiol 34:347–358CrossRefGoogle Scholar
  80. Watts DP (1997) Agonistic interventions in wild mountain gorilla groups. Behaviour 134:23–57CrossRefGoogle Scholar
  81. Wheeler BC, Scarry CJ, Koenig A (2013) Rates of agonism among female primates: a cross-taxon perspective. Behav Ecol 24:1369–1380PubMedCrossRefPubMedCentralGoogle Scholar
  82. Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5:139–159CrossRefGoogle Scholar
  83. Wikberg EC, Teichroeb JA, Bădescu I, Sicotte P (2013) Individualistic female dominance hierarchies with varying strength in a highly folivorous population of black-and-white colobus. Behaviour 150:295–320Google Scholar
  84. Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300CrossRefGoogle Scholar
  85. Wright E, Robbins AM, Robbins MM (2014) Dominance rank differences in the energy intake and expenditure of female Bwindi mountain gorillas. Behav Ecol Sociobiol 68:957–970CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany

Personalised recommendations