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Mixed-species primate groups in the kibale forest: Ecological constraints on association

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Abstract

Five species of diurnal primates in the Kibale Forest of western Uganda— red colobus (Colobus badius),black- and- white colobus (Colobus guereza),redtail monkeys (Cercopithecus ascanius),blue monkeys (Cercopithecus mitis),mangabeys (Cercocebus albigena)-often associate in mixed- species groups that vary in size and composition from day to day. Across this range of species, we found no consistent effect of association on feeding rate. In addition, there is no systematic difference between the species- specific individual feeding rates when animals were in mixed- species groups feeding in a specific tree on one day and when individuals of one of the same species were feeding in the same individual tree on a subsequent day. If associating in a mixed- species group lowers the risk of predation, one might expect that the number of vigilant events would decrease in mixed- species groups. However, the only species to exhibit a consistent decrease in vigilant behavior when in association was the red colobus. Redtail monkeys were more vigilant when in association. We predicted that the density and distribution of food resources would both constrain the frequency of association and the size of mixed- species groups. Based on 22 months of data on food resources and bimonthly censuses, we found no relationship between the frequency of association (except mangabeys) or mean mixed- species group size and the density and distribution of food resources for all species. Finally, we examined the behavior of the monkeys in and out of association before and after the playback of a crowned hawk eagle call (Spizaetus coronatus),a known predator. When more species were in association, the amount of time they spent being vigilant following the playback was greater and the response more intense than when fewer species were in association or when the group was alone. The results of this study illustrate that the nature of the costs and benefits of polyspecific associations for these different monkey species are complex and vary from species to species.

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References

  • Alexander, R. D. (1974). The evolution of social behaviour.Annu. Rev. EcoL Sociobiol. 5: 325–384.

    Article  Google Scholar 

  • Altmann, S. (1974). Baboons, space, time, and energy.Am. Zool. 14: 221–248.

    Google Scholar 

  • Beauchamp, J. J., and Olson, J. S. (1973). Corrections for bias in regression estimates after logarithmic transformations.Ecology 54: 1403–1407.

    Article  Google Scholar 

  • Boinski, S. (1989). Why don'tSaimiri oerstedii andCebus capucinus form mixed-species groups?Int J. Primatol. 10: 103–114.

    Google Scholar 

  • Bradbury, J. W., and Vebrencamp, S. L. (1977). Social organization and foraging in emballonurid bats. II. A model for the determination of group size.Behav. EcoL Sociobiol 1: 383–404.

    Article  Google Scholar 

  • Brown, L., Urban, E. K., and Newman, K. (1982).The Birds of Africa, Academic Press, New York.

    Google Scholar 

  • Butynski, T. M. (1990). Comparative ecology of blue monkeys(Cercopithecus mitis) in high- and low-density subpopulations.EcoL Monogr. 60: 1–26.

    Article  Google Scholar 

  • Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates.Folia Primatol. 29: 90–105.

    Google Scholar 

  • Chapman, C. A. (1990a). Association patterns of spider monkeys: The influence of ecology and sex on social organization.Behav. Ecol. Sociobiol. 26: 409–414.

    Article  Google Scholar 

  • Chapman, C. A. (1990b). Ecological constraints on group size in three species of neotropical primates.Folia Primatol. 55: 1–9.

    PubMed  CAS  Google Scholar 

  • Chapman, C. A., and Lefebvre, L. (1990). Manipulating foraging group size: Spider monkeys food calls at fruiting trees.Anim. Behav. 39: 891–896.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Wrangham, R. W., Hunt, K. Gebo, D., and Gardner, L. (1992). Estimators of fruit abundance of tropical trees.Biotropica 24: 527–531.

    Article  Google Scholar 

  • Chapman, C. A., White, F. J., and Wrangham, R. W. (1993). Defining subgroup size in fission-fusion societies.Folia Primatol. 61: 31–34.

    PubMed  CAS  Google Scholar 

  • Chapman, C. A., Wrangham, R. W., and Chapman, L. J. (1995). Ecological constraints on group size: An analysis of spider monkey and chimpanzee subgroups.Behav. Ecol. Sociobiol. 36: 59–70.

    Article  Google Scholar 

  • Cody, M. L. (1971). Finch flocks in the Mojave desert.Theor. Pop. Biol. 2: 141–158.

    Article  Google Scholar 

  • Cords, M. (1986). Interspecific and intraspecific variation in diet of two forest guenons,Cercopithecus ascanius andC. mitis. J. Anim Ecol. 55: 811–827.

    Article  Google Scholar 

  • Cords, M. (1987). Mixed-species association ofCercopithecus monkeys in the Kakamega Forest, Kenya.Univ. Calif. Publ. 117.

  • Cords, M. (1990). Vigilance and mixed-species associations of some east African forest monkeys.Behav. EcoL Sociobiol. 26: 297–300.

    Article  Google Scholar 

  • Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop ofSaguinus mystax andSaguinus fuscicollis in Amazonian Peru.Behaviour 105: 18–34.

    Google Scholar 

  • Gartlan, J. S., and Struhsaker, T. T. (1972). Polyspecific associations and niche separation of rain-forest anthropoids in Cameroon, West Africa.J. Zool. 168: 221–226.

    Article  Google Scholar 

  • Gautier-Hion, A. (1988). Polyspecific associations among forest guenons: Ecological, behavioral and evolutionary aspects. In Gautier-Hion, A., Bouliere, F., Gautier, J.-P., and Kingdon, J. (eds.),A Primate Radiation, Cambridge University Press, Cambridge, pp. 454–476.

    Google Scholar 

  • Gautier-Hion, A., and Tutin, C. E. G. (1988). Simultaneous attack by adult males of a polyspecific troop of monkeys against a crowned hawk eagle.Folia Primatol. 51: 149–151.

    PubMed  CAS  Google Scholar 

  • Gautier-Hion, A., Quris, R., and Gautier, J.-P. (1983). Monospecific vs polyspecific life: A comparative study of foraging and antipredatory tactics in a community ofCercopithecus monkeys.Behav. Ecol. Sociobiol. 12: 325–335.

    Article  Google Scholar 

  • Gebo, D. L., and Chapman, C. A.(1995). Positional behavior in five sympatric old world monkeys.Am. J. Phys. Anthropol. 97: 49–76.

    Article  PubMed  CAS  Google Scholar 

  • Giraldeau, L. (1988). The stable group and the determinants of foraging group size. In Slobodchikoff, C. N. (ed.),The Ecology of Social Behavior, Academic Press, New York, pp. 33–53.

    Google Scholar 

  • Goodall, J. (1986).The Chimpanzees of Gombe, Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Hamilton, W. D. (1971). Geometry of the selfish herd.J. Theor. Biol. 31: 295–311.

    Article  PubMed  CAS  Google Scholar 

  • Holmes, R. T., and Pitelka, F. A. (1968). Food overlap among coexisting sandpipers on northern Alaskan tundra.Syst. Zool. 17: 305–318.

    Article  Google Scholar 

  • Isbell, L. A. (1984). Daily ranging behavior of red colobus(Colobus badius) in Kibale Forest, Uganda.Folia Primatol. 41: 34–48.

    Google Scholar 

  • Isbell, L. A. (1991). Contest and scramble competition: Patterns of female aggression and ranging behavior among primates.Behav. Ecol. 2: 143–155.

    Article  Google Scholar 

  • Klein, L. L., and Klein, D. J. (1973). Observations on two types of neotropical primate intertaxa associations.Am. J. Phys. Anthropol. 38: 649–654.

    Article  PubMed  CAS  Google Scholar 

  • Klein, L. L., and Klein, D. J. (1977). Feeding behavior of the Columbian spider monkey.Ateles belzebuth. In Clutton-Brock, T. T. (ed.),Primate Ecology, Academic Press, London, pp. 153–181.

    Google Scholar 

  • Leighton, M., and Leighton, D. R. (1982). The relationship between size of feeding aggregate to size of food patch: Howler monkeys(Alouatta palliata) feeding inTrichilia cipo fruiting trees on Barro Colorado Island.Biotropica 14: 81–90.

    Article  Google Scholar 

  • Millar, D. M. (1984). Reducing transformation bias in curve fitting.Am. Stat. 38: 124–126.

    Article  Google Scholar 

  • Milton, K. (1984). Habitat, diet, and activity patterns of free-ranging woolly spider monkeys(Brachyteles arachnoides E. Geoffroyi 1906).Int. J. Primatol. 5: 491–514.

    Article  Google Scholar 

  • Milton, K., and May, M. L. (1976). Body weight, diet and home range area in primates.Nature 259: 459–462.

    Article  PubMed  CAS  Google Scholar 

  • Morse, D. H. (1977). Feeding behaviour and predator avoidance in heterospecific groups.Bioscience 27: 332–339.

    Article  Google Scholar 

  • Munn, C. A., and Terborgh, J. (1979). Multispecies territoriality in neotropical foraging flocks.Condor 81: 338–347.

    Article  Google Scholar 

  • Nishida, T. (1968). The social group of wild chimpanzees in the Mahale Mountains.Primates 9: 167–224.

    Article  Google Scholar 

  • Norconk, M.A. (1986).Interactions Between Primate Species in a Neotropical Forest: Mixed-Species Troops of Saguinus mystaxand S. fuscicollis(Callithrichidae), Ph.D. dissertation, University of California, Los Angeles.

    Google Scholar 

  • Norconk, M. A. (1990a). Introductory remarks: Ecological and behavioral correlates of polyspecific primate troops.Am. J. Primatol. 21: 81–85.

    Article  Google Scholar 

  • Norconk, M.A. (1990b). Mechanisms promoting stability in mixedSaguinus mystax andS. fuscicollis troops.Am. J. Primatol. 21: 159–170.

    Article  Google Scholar 

  • Oates, J. F. (1977). The guereza and its food. In Clutton-Brock, T. T. (ed.),Primate Ecology Academic Press, London, pp. 276–322.

    Google Scholar 

  • Oates, J. F., and Whitesides, G. H. (1990). Association between olive colobus(Procolobus verus), diana guenons(Cercopithecus diana), and other forest monkeys in Sierra Leone.Am. J. Primatol. 21: 129–146.

    Article  Google Scholar 

  • Peters, R., Cloutier, S., Dube, D., Evans, A, Hastings, P., Kohn, D., and Sawer-Foner, B. (1988). The ecology of the weight of fruit on trees and shrubs in Barbados.Oecologia 74: 612–616.

    Article  Google Scholar 

  • Podolsky, R. D. (1990). Effects of mixed-species associations on resource use bySaimiri sciureus andCebus apella.Am. J. Primatol. 21: 147–158.

    Article  Google Scholar 

  • Rodman, P. S. (1973). Synecology of Bornean primates. I. A test for interspecific interactions in spatial distribution of five species.Am. J. Phys. Anthropol. 38: 655–660.

    Article  PubMed  CAS  Google Scholar 

  • Rudran, R. (1978). Socioecology of the blue monkey(Cercopithecus mitis stuhlmanni) of the Kibale Forest, Uganda.Smithsonian Contrib. Zool. 249: 1–88.

    Google Scholar 

  • Schaller, G. (1972).The Serengeti Lion, University of Chicago Press, Chicago.

    Google Scholar 

  • Seyfarth, R., and Cheney, D. (1990). The assessment by vervet monkeys of their own and another species' alarm calls.Anim. Behav. 40: 754–764.

    Article  Google Scholar 

  • Skorupa, J. P. (1988).The Effect of Selective Timber Harvesting on Rainforest Primates in Kibale Forest, Uganda, Ph.D. dissertation, University of California, Davis.

    Google Scholar 

  • Skorupa, J. P. (1989). Crowned eaglesStephanoaetus coronatus in rainforest: Observations on breeding chronology and diet at a nest in Uganda.Ibis 131: 294–298.

    Google Scholar 

  • Sokal, R., and Rohlf, F. (1981).Biometry, W. H. Freeman, San Francisco.

    Google Scholar 

  • Struhsaker, T. T. (1975).The Red Colobus Monkey, University of Chicago Press, Chicago.

    Google Scholar 

  • Struhsaker, T. T. (1981). Polyspecific associations among tropical rain-forest primates.Z. Tierpsychol. 57: 268–304.

    Google Scholar 

  • Struhsaker, T. T., and Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys in the Kibale Forest, Uganda.Behav. Ecol. Sociobiol. 26: 435–443.

    Article  Google Scholar 

  • Struhsaker, T. T., and Leland, L. (1979). Socioecology of five sympatric monkey species in the Kibale Forest, Uganda.Adv. Study Behav. 9: 159–227.

    Article  Google Scholar 

  • Terborgh, J. (1983).Five New World Primates: A Study in Comparative Ecology, Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Terborgh, J. (1990). Mixed flock and polyspecific associations: Costs and benefits of mixed groups to birds and monkeys.Am. J. Primatol. 21: 87–100.

    Article  Google Scholar 

  • Terborgh, J., and Janson, C. H. (1986). The socioecology of primate groups.Ann. Rev. Ecol. Syst. 17: 111–135.

    Article  Google Scholar 

  • van Schaik, C. P. (1983). Why are diurnal primates living in groups?Behaviour 87: 120–144.

    Google Scholar 

  • Vickery, W. L., Giraldeau, L., Templeton, J. J., Kramer, D. L., and Chapman, C. A. (1991). Producers, scroungers, and group foraging.Am. Nat. 137: 847–863.

    Article  Google Scholar 

  • Waser, P. M. (1977). Feeding, ranging and group size in the mangabeyCercocebus albigena. In Clutton-Brock, T. T. (ed.),Primate Ecology, Academic Press, London, pp. 183–222.

    Google Scholar 

  • Waser, P. M. (1980). Polyspecific associations ofCercocebus albigena: Geographic variation and ecological correlates.Folia Primatol 33: 57–76.

    Article  PubMed  CAS  Google Scholar 

  • Waser, P. M. (1982). Primate polyspecific associations: Do they occur by chance?Anim. Behav. 30: 1–8.

    Article  Google Scholar 

  • Waser, P. M. (1984). “Chance” and mixed-species associations.Behav. Ecol. Sociobiol. 15: 197–202.

    Article  Google Scholar 

  • Waser, P. M. (1987). Interactions among primate species. In Smuts, B. B.,et al. (eds.),Primate Societies, University of Chicago Press, Chicago, pp. 210–226.

    Google Scholar 

  • Whitesides, G. H. (1989). Interspecific associations of Diana monkeys,Cercopithecus diana, in Sierra Leone, West Africa: Biological significance or chance?Anim. Behav. 37: 760–776.

    Article  Google Scholar 

  • Wolf, N. G. (1985). Odd fish abandon mixed-species groups when threatened.Behav. Ecol. Sociobiol. 17: 47–52.

    Article  Google Scholar 

  • Wrangham, R. W., Gittleman, J., and Chapman, C. A. (1993). Constraints on group size in primates and carnivores: Population density and day-range as assays of exploitation competition.Behav. EcoL Sociobiol. 32: 199–210.

    Article  Google Scholar 

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  1. Department of Zoology, University of Florida, 32611, Gainesville, Florida

    Colin A. Chapman & Lauren J. Chapman

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Chapman, C.A., Chapman, L.J. Mixed-species primate groups in the kibale forest: Ecological constraints on association. International Journal of Primatology 17, 31–50 (1996). https://doi.org/10.1007/BF02696157

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