Time Constraints Limit Group Sizes and Distribution in Red and Black-and-White Colobus

  • Amanda H. Korstjens
  • R. I. M. Dunbar
Special Issue: Behavior, Ecology, and Conservation of Colobine Monkeys


Researchers have shown that, in frugivorous primates, a major constraint on group size is intra group feeding competition. The relationship is less obvious in folivorous primates. We investigated whether colobine group sizes are constrained by time limitations as a result of their low energy diet and ruminant-like digestive system. We used climate as an easy to obtain proxy for the productivity of a habitat. Using the relationships between climate, group size, and time budget components for populations of Colobus and Piliocolobus at different research sites, we created 2 taxon-specific models. In both genera, feeding time increased with group size or biomass. The models for Colobus and Piliocolobus correctly predicted the presence or absence of the genera at, respectively, 86% of 148 and 84% of 156 African primate sites. Median predicted group sizes where the respective genera were present are 19 for Colobus and 53 for Piliocolobus. We show that the differences between the 2 genera are due mainly to intrinsic differences in the way each taxon’s digestive physiology interacts with climatic variables to influence resting time requirements. The models may help us explore their responses to climatic change in both the past and the future.


Colobinae costs and benefits of group living geographical distribution socioecology systems model 



We thank Peter Fashing for inviting us to the special symposium on colobines at the IPS in Torino for which this paper was prepared. A. H. Korstjens is funded by a grant from the Leverhulme Trust; R. I. M. Dunbar is funded by a British Academy Research Professorship. A. Korstjens’ visit to the conference was made possible by financial support from the Royal Society. We thank Sarah Elton, Russell Hill, Erik Willems, and Julia Lehmann for their constructive comments on the analyses and their input in constructing the databases. We thank 2 anonymous reviewers and the editor for their useful comments on earlier versions of the manuscript.


  1. Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics, 5, 325–383.CrossRefGoogle Scholar
  2. Bocian, C. M. (1997). Niche Separation of Black-and-White Colobus monkeys (Colobus angolensis and C. guereza) in the Ituri Forest. Ph.D. Dissertation, City University of New York, New York.Google Scholar
  3. Boesch, C., & Boesch, H. (1989). Hunting behaviour of wild chimpanzees in the Taï National Park. American Journal of Physical Anthropology, 78, 547–573.PubMedCrossRefGoogle Scholar
  4. Bronikowski, A. M., & Altmann, J. (1996). Foraging in a variable environment, weather patterns and the behavioral ecology of baboons. Behavioral Ecology and Sociobiology, 39, 11–25.CrossRefGoogle Scholar
  5. Caraco, T. (1979). Time budgeting and group-size: Theory. Ecology, 60, 611–617.CrossRefGoogle Scholar
  6. Chapman, C. A., & Chapman, L. J. (2000). Constraints on group size in red colobus and red-tailed guenons, examining the generality of the ecological constraints model. International Journal of Primatology, 21, 565–585.CrossRefGoogle Scholar
  7. Chapman, C. A., & Chapman, L. J. (2002). Foraging challenges of red colobus monkeys, influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology, 133, 861–875.PubMedGoogle Scholar
  8. Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002a). Application of protein-to-fibre ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.CrossRefGoogle Scholar
  9. Chapman, C. A., Chapman, L. J., & Gillespie, T. R. (2002b). Scale issues in the study of primate foraging, red colobus of Kibale National Park. American Journal of Physical Anthropology, 117, 349–363.CrossRefGoogle Scholar
  10. Chivers, D. J. (1994). Functional anatomy of the gastrointestinal tract. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys (pp. 205–227). Cambridge University Press.Google Scholar
  11. Clutton-Brock, T. H. (1975). Feeding behaviour of red colobus and black and white colobus in East Africa. Folia Primatologica, 23, 165–207.Google Scholar
  12. Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology (London), 183, 1–39.CrossRefGoogle Scholar
  13. Cowlishaw, G., & Dunbar, R. I. M. (2000). Primative conservation biology. University of Chicago, Chicago.Google Scholar
  14. Dasilva, G. L. (1989). The ecology of the western black and white colobus (Colobus polykomos polykomos Zimmerman 1780) on a riverine island in southeastern Sierra Leone. Ph.D. Dissertation, University of Oxford, Oxford, England.Google Scholar
  15. Davies, A. G., Oates, J. F., & Dasilva, G. L. (1999). Patterns of frugivory in three West African colobine monkeys. International Journal of Primatology, 20, 327–357.CrossRefGoogle Scholar
  16. Decker, B. S. (1994). Effects of habitat disturbance on the behavioral ecology and demographics of the Tana river red colobus (Colobus badius ruformitratus). International Journal of Primatology, 15, 703–737.Google Scholar
  17. Dinesen, L., Lehmberg, T., Rahner, M. C., & Fjeldsa, J. (2001). Conservation priorities for the forests of the Udzungwa Mountains, Tanzania, based on primates, duikers and birds. Biological Conservation, 99, 223–236.CrossRefGoogle Scholar
  18. Dittus, W. (1977). The evolution of behavior regulating density and age-specific sex ratios in a primate population. Behaviour, 69, 265–302.Google Scholar
  19. Dunbar, R. I. M. (1987). Habitat quality, population dynamics, and group composition in colobus monkeys (Colobus guereza). International Journal of Primatology, 8, 299–329.Google Scholar
  20. Dunbar, R. I. M. (1988). Primate social systems. Croom Helm, London.Google Scholar
  21. Dunbar, R. I. M. (1991). Functional significance of social grooming in primates. Folia Primatologica, 57, 121–131.Google Scholar
  22. Dunbar, R. I. M. (1992a). A model of the gelada socioecological system. Primates, 33, 69–83.CrossRefGoogle Scholar
  23. Dunbar, R. I. M. (1992b). Time, a hidden constraint on the behavioural ecology of baboons. Behavioral Ecology and Sociobiology, 31, 35–49.CrossRefGoogle Scholar
  24. Dunbar, R. I. M. (1996). Determinants of group size in primates, a general model. Proceedings of the British Academy, 88, 33–57.Google Scholar
  25. Dunbar, R. I. M., & Dunbar, E. P. (1974). Ecology and population dynamics of Colobus guereza in Ethiopia. Folia Primatologica, 21, 188–208.Google Scholar
  26. Dunbar, R. I. M., & Dunbar, P. (1988). Maternal time budgets of Gelada baboons. Animal Behaviour, 36, 970–980.CrossRefGoogle Scholar
  27. Dunbar, R. I. M., & Sharman, M. (1984). Is social grooming altruistic? Zeitschrift Fur Tierpsychologie-Journal of Comparative Ethology, 64, 163–173.Google Scholar
  28. Fashing, P. J. (2001a). Activity and ranging patterns of guerezas in the Kakamega Forest, intergroup variation and implications for intragroup feeding competition. International Journal of Primatology, 22, 549–577.CrossRefGoogle Scholar
  29. Fashing, P. J. (2001b). Feeding ecology of guerezas in the Kakamega forest, Kenya, the importance of Moraceae fruit in their diet. International Journal of Primatology, 22, 579–609.CrossRefGoogle Scholar
  30. Fimbel, C., Vedder, A., Dierenfeld, E., & Mulindahabi, F. (2001). An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. African Journal of Ecology, 39, 83–92.CrossRefGoogle Scholar
  31. Fleury, M.-C., & Gautier-Hion, A. (1999). Seminomadic ranging in a population of black colobus (Colobus satanas) in Gabon and its ecological correlates. International Journal of Primatology, 20, 491–509.CrossRefGoogle Scholar
  32. Gatinot, B. L. (1978). Characteristics of the diet of West African red colobus. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology, vol. 1: Behaviour (pp. 253–255). New York: Academic Press.Google Scholar
  33. Gillespie, T. R., & Chapman, C. A. (2001). Determinants of group size in the red colobus monkey (Procolobus badius), an evaluation of the generality of the ecological-constraints model. Behavioral Ecology and Sociobiology, 50, 329–338.CrossRefGoogle Scholar
  34. Harvey, P. H., & Clutton-Brock, T. H. (1981). Primate home-range size and metabolic needs. Behavioral Ecology and Sociobiology, 8, 151–155.CrossRefGoogle Scholar
  35. Hill, R. A., & Dunbar, R. I. M. (2002). Climatic determinants of diet and foraging behaviour in baboons. Evolutionary Ecology, 16, 579–593.CrossRefGoogle Scholar
  36. Isbell, L. A. (1983). Daily ranging behaviour of red colobus (Colobus badius tephrosceles) in Kibale Forest, Uganda. Folia Primatologica, 41, 34–48.Google Scholar
  37. Isbell, L. A. (1991). Contest and scramble competition, Patterns of female aggression and ranging behaviour among primates. Behavioral Ecology, 2, 143–155.CrossRefGoogle Scholar
  38. Janson, C. H. (1988). Food competition in brown capuchin monkeys (Cebus apella), Quantitive effects of group size and tree productivity. Behaviour, 105, 53–76.Google Scholar
  39. Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates, foraging costs and predation risks. Behavioral Ecology, 6, 326–336.CrossRefGoogle Scholar
  40. Janson, C. H., & van Schaik, C. P. (1988). Recognizing the many faces of primate food competition, methods. Behaviour, 105, 165–186.Google Scholar
  41. Koenig, A. (2000). Competitive regimes in forest–dwelling Hanuman langur females (Semnopithecus entellus). Behavioral Ecology and Sociobiology, 48, 93–109.CrossRefGoogle Scholar
  42. Koenig, A., Beise, J., Chalise, M. K., & Ganzhorn, J. U. (1998). When females should contest for food-testing hypotheses about resource density, distribution, size, and quality with Hanuman langurs (Presbytis entellus). Behavioral Ecology and Sociobiology, 42, 225–237.CrossRefGoogle Scholar
  43. Korstjens, A. H. (2001). The mob, the secret sorority, and the phantoms. An analysis of the socio-ecological strategies of the three Colobines of Taï. Ph.D. Dissertation, Utrecht University, Utrecht.Google Scholar
  44. Korstjens, A. H., Nijssen, E. C., & Noë, R. (2005). Inter-group relationships in western black-and-white colobus, Colobus polykomos polykomos. International Journal of Primatology, 26, 1267–1289.CrossRefGoogle Scholar
  45. Korstjens, A. H., Sterck, E. H. M., & Noë, R. (2002). How adaptive or phylogenetically inert is primate social behaviour? A test with two sympatric colobines. Behaviour, 139, 203–225.CrossRefGoogle Scholar
  46. Korstjens, A., Verhoeckx, I., & Dunbar, R. (2006). Time as a constraint on group size in spider monkeys. Behavioral Ecology and Sociobiology, 60, 683–694. DOI  1.1007/s00265-006-0212-2.CrossRefGoogle Scholar
  47. Le Houérou, H. N. (1984). Rain use efficiency, a unifying concept in arid land ecology. Journal of Arid Environments, 7, 213–247.Google Scholar
  48. Legates, D. R., & Willmott, C. J. (1990a). Mean seasonal and spatial variability in gauge-corrected global precipitation. International Journal of Climatology, 10, 111–127.CrossRefGoogle Scholar
  49. Legates, D. R., & Willmott, C. J. (1990b). Mean seasonal and spatial variability in global surface air temperature. Theoretical and Applied Climatology, 41, 11–21.CrossRefGoogle Scholar
  50. Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2007a). Fission-fusion social systems as a strategy for coping with ecological constraints, a primate case. Evolutionary Ecology, DOI 10.1007/s10682-006-9141-9.
  51. Lehmann, J., Korstjens, A. H., Dunbar, R. I. M. (2007b). Group-size, grooming and social cohesion in animal primates. Animal Behaviour, in press.Google Scholar
  52. Lewis, S., Sherratt, T. N., Hamer, K. C., & Wanless, S. (2001). Evidence of intra-specific competition for food in a pelagic seabird. Nature, 412, 816–819.PubMedCrossRefGoogle Scholar
  53. Maisels, F., Gauthierhion, A., & Gautier, J. P. (1994). Diets of 2 sympatric colobines in Zaire, more evidence on seed-eating in forests on poor soils. International Journal of Primatology, 15, 681–701.Google Scholar
  54. McGraw, W. S. (1998). Posture and support use of old world monkeys (Cercopithecidae), the influence of foraging strategies, activity patterns, and the spatial distribution of preferred food items. American Journal of Primatology, 46, 229–250.PubMedCrossRefGoogle Scholar
  55. McKey, D. B., Gartlan, J. S., Waterman, P. G., & Choo, G. M. (1981). Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry. Biological Journal of the Linnean Society, 16, 115–146.Google Scholar
  56. McKey, D., & Waterman, P. G. (1982). Ranging behaviour of a group of black colobus (Colobus satanas) in the Douala-Edea Reserve, Cameroon. Folia Primatologica, 39, 264–304.CrossRefGoogle Scholar
  57. Oates, J. F. (1977a). The guereza and its food. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys and apes (pp. 275–321). London: Academic Press.Google Scholar
  58. Oates, J. F. (1977b). The social life of a black-and-white colobus monkey, Colobus guereza. Zeitshrift für Tierpschychologie, 45, 1–6.Google Scholar
  59. Oates, J. F. (1994). The natural history of African colobines. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys (pp. 75–128). Cambridge: Cambridge University Press.Google Scholar
  60. Oates, J. F., & Korstjens, A. H. (in press). The olive colobus, Procolobus verus. In J. Kingdon, D. C. D. Happold & T. M. Butynski (Eds.), Mammals of Africa (pp. 75–128). Oxford: Oxford University Press.Google Scholar
  61. Oates, J. F., Whitesides, G. H., Davies, A. G., Waterman, P. G., Green, S. M., Dasilva, G. L., et al. (1990). Determinants of variation in tropical forest primate biomass, new evidence from West Africa. Ecology, 71, 328–343.CrossRefGoogle Scholar
  62. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation, the primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.CrossRefGoogle Scholar
  63. Rode, K. D., Chapman, C. A., Chapman, L. J., & McDowell, L. R. (2003). Mineral resource availability and consumption by Colobus in Kibale National Park, Uganda. International Journal of Primatology, 24, 541–573.CrossRefGoogle Scholar
  64. Rose, M. D. (1978). Feeding and associated positional behavior of black and white colobus monkeys (Colobus guereza). In G. G. Montgomery (Ed.), The ecology of arboreal folivores (pp. 253–262). Washington DC: Smithsonian Institution Press.Google Scholar
  65. Siex, K. S., & Struhsaker, T. T. (1999). Ecology of the Zanzibar red colobus monkey, demographic variability and habitat stability. International Journal of Primatology, 20, 163–192.CrossRefGoogle Scholar
  66. Snaith, T. V., & Chapman, C. A. (2005). Towards an ecological solution to the folivore paradox, patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles). Behavioral Ecology and Sociobiology, 59, 185.CrossRefGoogle Scholar
  67. Stanford, C. B. (1995). The influence of chimpanzee predation on group size and anti-predator behaviour in red colobus monkeys. Animal Behavior, 49, 577–587.Google Scholar
  68. Stanford, C. B. (1998). Chimpanzee and red colobus: The ecology of predator and prey. Cambridge: Harvard University Press, pp. 296.Google Scholar
  69. Starin, E. D. (1991). Socioecology of the red colobus monkey in the gambia with particular reference to female-male differences and transfer patterns. PhD Dissertation, City University of New York, New York.Google Scholar
  70. Steenbeek, R., & van Schaik, C. P. (2001). Competition and group size in Thomas's langurs, the folivore paradox revisited. Behavioral Ecology and Sociobiology, 49, 100–110.CrossRefGoogle Scholar
  71. Sterck, E. H. M., & Steenbeek, R. (1997). Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour, 139, 9–10.Google Scholar
  72. Struhsaker, T. T. (1978). Food habits of five monkey species in the Kibale Forest, Uganda. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology, vol. 1: Behaviour (pp. 225–248). New York: Academic Press.Google Scholar
  73. Struhsaker, T. T., & Leland, L. (1987). Colobines, Infanticide by adult males. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 83–97). Chicago: University of Chicago Press.Google Scholar
  74. Teichroeb, J. A., Saj, T. L., Paterson, J. D., & Sicotte, P. (2003). Effect of group size on activity budgets of Colobus vellerosus in Ghana. International Journal of Primatology, 24, 743–758.CrossRefGoogle Scholar
  75. Terborgh, J., & Janson, C. H. (1986). The socioecology of primate groups. Annual Review of Ecological Systematics, 17, 111–135.CrossRefGoogle Scholar
  76. Treves, A., & Chapman, C. A. (1996). Conspecific threat, predation avoidance, and resource defense, implications for grouping in langurs. Behavioral Ecology and Sociobiology, 39, 43–53.CrossRefGoogle Scholar
  77. Tuhkanen, S. (1980). Climate parameters and indices in plant geography. Acta Phytogeographica Sueca, 67, 9–11.Google Scholar
  78. Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (1997). The primate community of the Lope Reserve, Gabon, diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 1–24.PubMedCrossRefGoogle Scholar
  79. van Schaik, C. P., & van Noordwijk, M. A. (1988). Scramble and contest in feeding competition among female long-tailed macaques (Macaca fascicularis). Behaviour, 105, 77–98.Google Scholar
  80. van Schaik, C. P., van Noordwijk, M. A., de Boer, R. J., & den Tonkelaar, I. (1983). The effects of group size on time budgets and social behaviour in wild long-tailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology, 13, 173–181.CrossRefGoogle Scholar
  81. Waterman, P. G., & Kool, K. M. (1994). Colobine food selection and plant chemistry. In A. G. Davies & J. F. Oates (Eds.), Colobine monkeys (pp. 251–284). Cambridge, UK: Cambridge University Press.Google Scholar
  82. Waterman, P. G., Ross, J. A. M., Bennett, E. L., & Davies, A. G. (1988). A comparison of the floristics and leaf chemistry of the tree flora in 2 Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old-World. Biological Journal of Linnean Society, 34, 1–32.Google Scholar
  83. Watts, D. P. (1985). Relations between group size and composition and feeding competition in mountain gorilla groups. Animal Behavior, 33, 72–85.CrossRefGoogle Scholar
  84. Whitesides, G. H. (1989). Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa, Biological significance or chance? Animal Behavior, 37, 760–776.CrossRefGoogle Scholar
  85. Whitten, P. L. (1983). Diet and dominance among female vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 5, 139–159.CrossRefGoogle Scholar
  86. Williamson, D. K., & Dunbar, R. (1999). Energetics, time budgets and group size. In P. Lee (Ed.), Primate socioecology (pp. 321–338). Cambridge, UK: Cambridge University Press.Google Scholar
  87. Willmott, C. J., & Feddema, J. J. (1992). A more rational climatic moisture index. Professional Geographer, 44, 84–88.CrossRefGoogle Scholar
  88. Willmott, C. J., & Matsuura, K. (2001). Terrestrial air temperature and precipitation, monthly and annual climatologies (Version 3.02).
  89. Wrangham, R. W., Gittleman, J. L., & Chapman, C. A. (1993). Constraints on group size in primates and carnivores, population density and day-range as assays of exploitation competition. Behavioral Ecology and Sociobiology, 32, 199–209.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.School of Conservation SciencesBournemouth University, Christchurch HousePooleUK
  2. 2.British Academy Centenary Research Project, School of Biological SciencesUniversity of LiverpoolLiverpoolUK

Personalised recommendations