Abstract
Diet data have been used to address a number of theoretical issues. We often calculate the proportion of time spent eating different foods (e.g., fruits, leaves) to place species into dietary categories and contrast morphological or behavioral traits among categories. Yet we have little understanding of how flexible species can be in terms of the plant parts and species consumed. To address this issue, we analyzed data on the diets of red colobus monkeys (Procolobus badius) from Kibale National Park, Uganda, to evaluate temporal and spatial variability in the plant parts and species eaten. After considering observer differences and sampling issues, we evaluated how different a group's diet could be if samples were taken in different years. We found that the diet of the same groups showed significant, consistent changes over a 4‐year period. For example, the time spent feeding on leaves increased from 56% in 1994 to 76% in 1998. The plant parts and species eaten by eight groups inhabiting different types of forest (e.g., pristine, logged, riverine) varied among groups. The largest interdemic difference was seen in the use of young leaves (38%). Dietary differences were also found between groups with overlapping home ranges (41–49% overlap). Different subspecies of Procolobus badius also varied in diet; however, this variation was often not of the magnitude documented within Kibale for the same population. The fact that diet can vary considerably over small spatial and short temporal scales within the same species raises the intriguing question as to what level of interspecific difference is biologically significant for addressing particular questions. We conclude that behavioral flexibility blurs our traditional stereotypic assessment of primates; a study of one group that occupies a specific habitat at one point in time may not adequately represent the species. Am J Phys Anthropol 117:349–363, 2002. © 2002 Wiley‐Liss, Inc.
Keywords: Procolobus badius; diet, methodology; scale; dietary overlap; competition; conservation
LITERATURE CITED
- Altmann SA. 1998. Foraging for survival: yearling baboons in Africa. Chicago: University of Chicago Press. [Google Scholar]
- Anapol F, Lee S. 1994. Morphological adaptation to diet in anthropoid primates. Am J Phys Anthropol 94: 239–261. [DOI] [PubMed] [Google Scholar]
- Barrett L. 1995. Foraging strategies, ranging behaviour and territoriality among grey‐cheeked mangabeys in Kibale Forest, Western Uganda. Ph.D. dissertation, University College London. [Google Scholar]
- Bocian CM. 1997. Niche separation of black‐and‐white colobus (Colobus angolensis and C. guereza) in the Ituri forest. Ph.D. thesis, City University of New York. [Google Scholar]
- Butynski TM. 1990. Comparative ecology of blue monkeys (Cercopithecus mitis) in high‐ and low‐density subpopulations. Ecol Monogr 60: 1–26. [Google Scholar]
- Chalmers N. 1979. Social behavior in primates. London: Edward Arnold Press. [Google Scholar]
- Chapman CA. 1987. Flexibility in diets of three species of Costa Rican Primates. Folia Primatol (Basel) 49: 90–105. [Google Scholar]
- Chapman CA. 1989. Ecological constraints on group size in three species of neotropical primates. Folia Primatol (Basel) 73: 1–9. [DOI] [PubMed] [Google Scholar]
- Chapman CA, Chapman LJ. 1990. Dietary variability in primate populations. Primates 31: 121–128. [Google Scholar]
- Chapman CA, Chapman LJ. 1997. Forest regeneration in logged and unlogged forests of Kibale National Park, Uganda. Biotropica 29: 396–412. [Google Scholar]
- Chapman CA, Chapman LJ. 1999. Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40: 215–232. [DOI] [PubMed] [Google Scholar]
- Chapman CA, Chapman LJ. 2000. Constraints on group size in redtail monkeys and red colobus: testing the generality of the ecological constraints model. Int J Primatol 21: 565–585. [Google Scholar]
- Chapman CA, Lambert JE. 2000. Habitat alteration and the conservation of African Primates: a case study of Kibale National Park, Uganda. Am J Primatol 50: 169–186. [DOI] [PubMed] [Google Scholar]
- Chapman CA, Onderdonk DA. 1998. Forests without primates: primate/plant codependency. Am J Primatol 45: 127–141. [DOI] [PubMed] [Google Scholar]
- Chapman CA, Chapman LJ, Glander KE. 1989. Primate populations in northwestern Costa Rica: potential for recovery. Primate Conserv 10: 37–44. [Google Scholar]
- Chapman CA, Chapman LJ, Wrangham R, Isabirye‐Basuta G, Ben‐David K. 1997. Spatial and temporal variability in the structure of a tropical forest. Afr J Ecol 35: 287–302. [Google Scholar]
- Chapman CA, Wrangham RW, Chapman LJ, Kennard DK, Zanne AE. 1999. Fruit and flower phenology at two sites in Kibale National Park, Uganda. J Trop Ecol 15: 189–211. [Google Scholar]
- Chivers DJ, Hladik CM. 1980. Morphology of the gastrointestinal tract in primates: comparison with other mammals in relation to diet. J Morphol 116: 337–386. [DOI] [PubMed] [Google Scholar]
- Clutton‐Brock TH. 1975. Feeding behaviour of red colobus and black and white colobus in East Africa. Folia Primatol (Basel) 23: 165–207. [DOI] [PubMed] [Google Scholar]
- Clutton‐Brock TH. 1977. Some aspects of intraspecific variation in feeding and ranging behaviour in primates In: Clutton‐Brock TH, editor. Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys, and apes. London: Academic Press; p 539–556. [Google Scholar]
- Clutton‐Brock TH, Harvey PH. 1977. Primate ecology and social organization. J Zool Lond 183: 1–39. [Google Scholar]
- Curtin SH. 1980. Dusky and banded leaf monkeys In: Chivers DJ, editor. Malayan forest primates. New York: Plenum Press; p 107–145. [Google Scholar]
- Curtin SH, Chivers DJ. 1978. Leaf‐eating primates of peninsular Malaysia: the siamang and the dusky leaf‐monkey In: Montgomery GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press; p 441–464. [Google Scholar]
- Dasilva GL. 1992. The western black‐and‐white colobus as a low‐energy strategist: activity budgets, energy expenditure, and energy intake. J Anim Ecol 61: 79–91. [Google Scholar]
- Dasilva GL. 1994. Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. Int J Primatol 15: 1–26. [Google Scholar]
- Davies AG. 1991. Seed‐eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern Borneo. Int J Primatol 12: 119–144. [Google Scholar]
- Davies AG. 1994. Colobine populations In: Davies AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press; p 285–310. [Google Scholar]
- Davies AG, Bennett EL, Waterman PG. 1988. Food selection by two south‐east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biol J Linn Soc 34: 33–56. [Google Scholar]
- Davies AG, Oates JF, Dasilva GA. 1999. Patterns of frugivory in three West African colobine monkeys. Int J Primatol 20: 327–357. [Google Scholar]
- Fashing PJ. 1999. The behavioural ecology of an African colobine monkey: diet, range use, and patterns of intergroup aggression in eastern black and white colobus monkeys (Colobus guereza) Ph.D. thesis, Columbia University. [Google Scholar]
- Fleagle JG. 1977. Locomotor behavior and muscular anatomy of sympatric Malaysian leaf‐monkeys (Presbytis obscura and Presbytis melalophus). Am J Phys Anthropol 46: 297–308. [DOI] [PubMed] [Google Scholar]
- Fleagle JG. 1978. Locomotion, posture, and habitat utilization in two sympatric Malaysian leaf monkeys (Presbytis obscura and Presbytis melalophos) In: Montgomery GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press; p 243–251. [Google Scholar]
- Fleagle JG, Mittermeier RA. 1980. Locomotor behavior, body size and comparative ecology of seven Surinam monkeys. Am J Phys Anthropol 52: 301–314. [Google Scholar]
- Freeland WJ. 1977. Dynamics of primate parasites. Ph.D. dissertation, University of Michigan, Ann Arbor. [Google Scholar]
- Gatinot BL. 1977. Le régime alimentaire du colobe bai au Sénegal. Mammalia 41: 373–402. [Google Scholar]
- Gebo DL. 1992. Locomotor and postural behavior in Alouatta palliata and Cebus capucinus . Am J Primatol 26: 277–290. [DOI] [PubMed] [Google Scholar]
- Gebo DL, Chapman CA. 1995a. Positional behavior in five sympatric old world monkeys. Am J Phys Anthropol 97: 49–76. [DOI] [PubMed] [Google Scholar]
- Gebo DL, Chapman CA. 1995b. Habitat, annual, and seasonal effects on positional behavior in red colobus monkeys. Am J Phys Anthropol 96: 73–82. [DOI] [PubMed] [Google Scholar]
- Grant J, Chapman CA, Richardson K. 1992. Defended versus undefended home range size of mammals. Behav Ecol Sociobiol 31: 149–161. [Google Scholar]
- Harrison MJS, Hladik CM. 1986. Un primate granivore: le colobe noir dans la forêt du Gabon, potentialité d'évolution du comportement alimentaire. Rev Ecol 41: 281–298. [Google Scholar]
- Harvey PH, Martin RD, Clutton‐Brock TH 1987. Life history in comparative perspective In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: Chicago University Press; p 181–196. [Google Scholar]
- Hill WCO. 1964. The maintenance of langurs (Colobinae) in captivity: experiences and some suggestions. Folia Primatol (Basel) 2: 222–231. [Google Scholar]
- Holmes RT, Pitelka FA. 1968. Food overlap among coexisting sandpipers on northern Alaskan tundra. Syst Zool 17: 305–318. [Google Scholar]
- Howard PC. 1991. Nature conservation in Uganda's tropical forest reserves. Gland, Switzerland: IUCN. [Google Scholar]
- Isbell LA. 1991. Contest and scramble competition: patterns of female aggression and ranging behaviour among primates. Behav Ecol 2: 143–155. [Google Scholar]
- Johns AD, Skorupa JP. 1987. Responses of rain‐forest primates to habitat disturbance: a review. Int J Primatol 8: 157–191. [Google Scholar]
- Kay RF. 1984. On the use of anatomical features to infer foraging behavior of extinct primates In: Rodman PS, Cant JGH, editors. Adaptations of foraging in nonhuman primates. New York: Columbia University Press; p 21–53. [Google Scholar]
- Kingston B. 1967. Working plan for Kibale and Itwara Central Forest Reserves. Entebbe, Uganda: Uganda Forest Department. [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: 2225–237. [Google Scholar]
- Maisels F, Gautier‐Hion A, Gautier J‐P. 1994. Diets of two sympatric colobines in Zaire: more evidence on seed‐eating in forests on poor soils. Int J Primatol 15: 681–701. [Google Scholar]
- Marsh CW. 1981. Ranging behaviour and its relation to diet selection in Tana River red colobus (Colobus badius rufomitratus). J Zool London 195: 473–492. [Google Scholar]
- McKey DB. 1978. Soils, vegetation, and seed‐eating by black colobus monkeys In: Montgomery GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press; p 423–437 [Google Scholar]
- McKey DB, Waterman PG. 1982. Ranging behavior of a group of black colobus (Colobus satanas) in the Douala‐Edea Reserve, Cameroon. Folia Primatol (Basel) 39: 264–304. [DOI] [PubMed] [Google Scholar]
- McKey DB, Gartlan JS, Waterman PG, Choo CM. 1981. Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry. Biol J Linn Soc 16: 115–146. [Google Scholar]
- Milton K, May ML. 1976. Body weight, diet, and home range area in primates. Nature 259: 459–462. [DOI] [PubMed] [Google Scholar]
- Moreno‐Black GS, Maples WR. 1977. Differential habitat utilization of four Cercopithecidae in a Kenyan forest. Folia Primatol (Basel) 27: 85–107. [DOI] [PubMed] [Google Scholar]
- Mturi FA. 1993. Ecology of the Zanzibar red colobus monkey, Colobus badius kirkii (Gray, 1968), in comparison with other red colobines In: Lovett JC, Wasser SK, editors. Biogeography and ecology of the rain forest of eastern Africa. Cambridge: Cambridge University Press; p 243–266. [Google Scholar]
- Napier JR. 1970. Paleoecology and catarrhine evolution In: Napier JR, Napier PH, editors. Old World monkeys: evolution, systematics, and behavior. New York: Academic Press; p 53–95. [Google Scholar]
- Naughton‐Treves L, Treves A, Chapman CA, Wrangham R. 1998. Temporal patterns of crop raiding by primates: linking food availability in croplands and adjacent forest. J Appl Ecol 35: 596–606. [Google Scholar]
- Oates JF. 1977. The guereza and its food In: Clutton‐Brock TH, editor. Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys, and apes. New York: Academic Press; p 275–321. [Google Scholar]
- Olupot W. 1998. Long‐term variation in mangabey (Cercocebus albigena johnstoni Lydekker) feeding in Kibale National Park, Uganda. Afr J Ecol 36: 96–101. [Google Scholar]
- Olupot W. 1999. Mangabey dispersal and conservation in Kibale National Park, Uganda. Ph.D. thesis, Purdue University. [Google Scholar]
- Olupot W, Chapman CA, Brown CH, Waser PM. 1994. Mangabey (Cercocebus albigena) population density, group size, and ranging: a twenty‐year comparison. Am J Primatol 32: 197–205. [DOI] [PubMed] [Google Scholar]
- Onderdonk DA, Chapman CA. 2000. Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21: 587–611. [Google Scholar]
- Osmaston HA. 1959. Working plan for the Kibale and Itwara Forests. Entebbe: Uganda Forest Department; 60 p [Google Scholar]
- Richards A. 1974. Intra‐specific variation in the social organization and ecology of Propithecus verreauxi . Folia Primatol (Basel) 22: 178–207. [DOI] [PubMed] [Google Scholar]
- Richards A. 1985. Primates in Nature. New York: W.H. Freeman and Co. [Google Scholar]
- Rudran R. 1978a. Socioecology of the blue monkey (Cercopithecus mitis stuhlmannii) of the Kibale Forest, Uganda. Smithson Contrib Zool; 249. [Google Scholar]
- Rudran R. 1978b. Intergroup dietary comparisons and folivorous tendencies of two groups of blue monkeys (Cercopithecus mitis stuhlmanni) In: Montgomery GG, editor. The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press; p 483–503. [Google Scholar]
- Skorupa JP. 1988. The effect of selective timber harvesting on rain‐forest primates in Kibale Forest, Uganda. Ph.D. dissertation, University of California at Davis. [Google Scholar]
- Sokal RR, Rohlf FJ. 1981. Biometry. San Francisco: Freeman. [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. [Google Scholar]
- Strier KB. 1994. Myth of the typical primate. Yrbk Phys Anthropol 37: 233–271. [Google Scholar]
- Struhsaker TT. 1975. The red colobus monkey. Cambridge: University of Chicago Press. [Google Scholar]
- Struhsaker TT. 1978. Food habits of five monkey species in the Kibale Forest, Uganda In: Chivers DJ, Herbert J, editors. Recent advances in primatology Volume 1 Behaviour. New York: Academic Press; p 225–248. [Google Scholar]
- Struhsaker TT. 1980. Comparison of the behaviour and ecology of red colobus and red‐tail monkeys in the Kibale Forest, Uganda. Afr J Ecol 18: 33–51. [Google Scholar]
- Struhsaker TT. 1997. Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. Gainesville, FL: University Press of Florida. [Google Scholar]
- Struhsaker TT, Leland L. 1979. Socioecology of five sympatric monkey species in the Kibale Forest, Uganda In: Rosenblatt J, Hinde RA, Beer C, Busnel MC, editors. Advances in the study of behavior Volume 9 New York: Academic Press; p 158–228. [Google Scholar]
- Struhsaker TT, Oates JF. 1975. Comparison of the behavior and ecology of red colobus and black‐and‐white colobus monkeys in Uganda: a summary In: Tuttle RH, editor. Socioecology and psychology of primates. The Hague: Mouton Publishers; p 103–124. [Google Scholar]
- Sussman RW. 1987. Species‐specific dietary patterns in primates and human dietary adaptations In: Kinzey WG, editor. The evolution of human behavior: primate models. Albany: State University of New York Press; p 151–179. [Google Scholar]
- Teleen S. 1994. Group size and group structure of guereza, Colobus guereza occidentalis (Rochebrune 1886), in the Kibale Forest, Uganda. Diploma, Technischen Universitat Braunschweig. [Google Scholar]
- Terborgh J. 1983. Five New World primates. Princeton: Princeton University Press. [Google Scholar]
- Tutin CEG. 1999. Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 40: 249–265. [DOI] [PubMed] [Google Scholar]
- van Schaik CP. 1989. The ecology of social relationships amongst female primates In: Standen V, Foley RA, editors. Comparative socioecology. Cambridge: Blackwell Press; p 195–218. [Google Scholar]
- Wallis SJ. 1978. The sociology of Cercocebus albigena johnstoni (Lyddeker): an arboreal, rain forest monkey. Dissertation, University of London. [Google Scholar]
- Waser PM. 1974. Inter‐group interactions in a forest monkey the mangabey Cercocebus albigena. Ph.D. dissertation, Rockefeller University, New York. [Google Scholar]
- Waser PM. 1975. Monthly variation in feeding and activity patterns of the mangabey, Cercocebus albigena (Lydekker). E Afr Wildl J 13: 249–263. [Google Scholar]
- Waser PM. 1987. Interactions among primate species In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker T, editors. Primate societies. Chicago: Chicago University Press; p 210–226. [Google Scholar]
- Waser PM, Floody O. 1974. Ranging patterns of the mangabey, Cercocebus albigena, in the Kibale Forest, Uganda. Z Tierpsychol 35: 85–101. [Google Scholar]
- Yeager CP. 1989. Feeding ecology of the proboscis monkey (Narvalis larvatus). Int J Primatol 10: 497–530. [Google Scholar]