Skip to main content
Log in

The role of phytochemistry in dietary choices of Tana River red colobus monkeys(Procolobus badius rufomitratus)

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

We conducted a phytochemical survey of tree species growing within the riverine forests of the Tana River National Primate Reserve in Kenya to understand better the feeding ecology of an endangered resident primate, the Tana River red colobus monkey (Procolobus badius rufomitratus).Young leaves, which make up a large percentage of this monkey's diet, are significantly higher in nitrogen and lower in acid detergent fiber than more abundant mature leaves are. Phenolic chemistry had little inhibitory effect on feeding by P. b. rufomitratus.Choice among tree species by P. b. rufomitratusappears to be influenced largely by leaf availability,once an acceptable threshold of nitrogen and fiber is reached When mature leaves are eaten, they selected species that are high in nitrogen and low in fiber. A significantly higher nitrogen content was found for the mature leaves of all leguminous versus nonleguminous tree species. Consequently, the availability of certain types of mature leaf species during periods of preferred food scarcity may prove critical to groups of Tana River red colobus monkeys.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bate-Smith, E. C. (1972). Detection and determination of ellagitannins.Phytochemistry 11: 1153–1156.

    Article  CAS  Google Scholar 

  • Bate-Smith, E. C. (1975). Phytochemistry of proanthocyanidins.Phytochemistry 14: 1107–1113.

    Article  CAS  Google Scholar 

  • Bate-Smith, E. C. (1977). Astringent tanninsof Acer species.Phytochemistry 16: 1421–1426.

    Article  CAS  Google Scholar 

  • Bate-Smith, E. C. (1981). Astringent tannins of the leaves ofGeranium species.Phytochemistry 20: 211.

    Article  CAS  Google Scholar 

  • Bauchop, T. (1978). Digestion of leaves in vertebrate arboreal folivores. In Montgomery, G. G. (ed.),The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington, DC, pp. 193–204.

    Google Scholar 

  • Bauchop, T., and Martucci, R. W. (1968). Ruminant-like digestion of the langur monkey.Science 161: 698–699.

    Article  PubMed  CAS  Google Scholar 

  • Bryant, J. P., Chapin, F. S., and Klein, D. R. (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Oikos 40: 357–368.

    Article  CAS  Google Scholar 

  • Butynski, T. M, and Mwangi, G. (1994). Conservation status and distribution of the Tana River red colobus and crested mangabey. Report for Zoo Atlanta, Kenya Wildlife Service, National Museums of Kenya, Institute of Primate Research and East African Wildlife Society.

  • Chivers, D. J. (1994). Functional anatomy of the gastrointestinal tract. In Davies, A. G., and Oates, J. F. (eds.),Colobine Monkeys: Their Evolutionary Ecology, Cambridge University Press, Cambridge, pp. 205–227.

    Google Scholar 

  • Olivers, D. J., and Hladik, C. M. (1980). Morphology of GI tract in primates: Comparisons with other mammals in relation to diet.J. Morphol. 166: 337–386.

    Article  Google Scholar 

  • Choo, G. M., Waterman, P. G., McKey, D. B., and Gartlan, J. S. (1981). A simple enzyme assay for dry matter digestibility and its value in studying food selection by generalist herbivores.Oecologia 49: 170–178.

    Article  Google Scholar 

  • Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol. Monogr. 53(2): 209–233.

    Article  Google Scholar 

  • Coley, P. D., and Aide, T. M. (1991). Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In Price, P. W., Lewinsohn, T. M., Fernandes, G. W., and Benson, W. W. (eds.),Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, John Wiley and Sons, New York, pp. 25–49.

    Google Scholar 

  • Coley, P. D., Bryant, J. P., and Chapin, F. S., III (1985). Resource availability and plant antiherbivore defense.Science 230: 895–899.

    Article  PubMed  Google Scholar 

  • Davies, A. G., Bennet, E. L., and Waterman, P. G. (1988). Food selection by two south-east Asian colobine monkeys(Presbytis rubicunda andPresbytis melaphos) in relation to plant chemistry.Biol. J. Linn. Soc. 34: 33–56.

    Google Scholar 

  • Decker, B. S. (1989).Effects of Habitat Disturbance on the Behavioral Ecology and Demographics of the Tana River Red Colobus (Colobus badius rufomitratus), Ph.D. thesis, Emory University, Atlanta, GA.

    Google Scholar 

  • Decker, B. S. (1994). Effects of habitat disturbance on the behavioral ecology and demographics of the Tana River red colobus(Colobus badius rufomitratus).Int. J. Primatol. 15(5): 703–737.

    Google Scholar 

  • Dudt, J. F., and Shure, D. J. (1994). The influence of light and nutrients on foliar phenolics and insect herbivory inCornus florida andLinodendron tulipifera.Ecology 75: 86–98.

    Article  Google Scholar 

  • Emlen, J. M. (1966). The role of time and energy in food choice.Am. Nat. 100: 611–617.

    Article  Google Scholar 

  • Farnsworth, N. R. (1966). Biological and phytochemical screening of plants.J. Pharm. Sci. 55(3): 225–276.

    Article  PubMed  CAS  Google Scholar 

  • Feeny, P. P. (1970). Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51: 565–581.

    Article  Google Scholar 

  • Feeny, P. P. (1976). Plant apparency and chemical defense. In Wallace, J., and Mansell, R. L. (eds.),Biochemical Interactions Between Plants and Insects, Recent Advances in Phytochemistry 10, Plenum Press, New York, pp. 1–40.

    Google Scholar 

  • Fox, L. R., and Macauley, B. J. (1977). Insect grazing onEucalyptus in response to variation in leaf tannins and nitrogen.Oecologia 29: 145–162.

    Google Scholar 

  • Fraenkel, G. (1959). The raison d'etre of secondary plant substances.Science 121: 1466–1470.

    Article  Google Scholar 

  • Freeland, W. J., and Janzen, D. H. (1974). Strategies in herbivory by mammals: The role of plant secondary compounds.Am. Nat. 108: 269–289.

    Article  CAS  Google Scholar 

  • Gartlan, J. S., McKey, D. B., Waterman, P. G., Mbi, G. N., and Struhsaker, T. T. (1980). A comparative study of the phytochemistry of two African ram forests.Biochem. Syst. Ecol. 8: 401–422.

    Article  Google Scholar 

  • Glander, K. E. (1982). The impact of secondary compounds on primate feeding behavior.Yrbk. Phys. Anthropol. 25: 1–18.

    Article  Google Scholar 

  • Hagerman, A. E., and Butler, L. G. (1991). Tannins and lignins. In Rosenthal, G. A., and Berenbaum, M. R. (eds.),Herbivores: Their Interaction with Secondary Plant Metabolites, Vol I, 2nd ed., Academic Press, New York, pp. 355–388.

    Google Scholar 

  • Harborne, J. B. (1982).Introduction to Ecological Biochemistry, 2nd ed., Academic Press, New York.

    Google Scholar 

  • Harper, J. L. (1989). The value of a leaf.Oecologia 80: 53–58.

    Article  Google Scholar 

  • Hoberg, P. (1986). Soil nutrient availability, root symbioses amd tree species composition in tropical Africa: A review.J. Trop. Ecol. 2: 359–372.

    Article  Google Scholar 

  • Hughes, F. M. R. (1988). The ecology of African floodplain forests: A review.J. Biogeogr. 15: 127–140.

    Article  Google Scholar 

  • Kay, R. N. B., and Davies, A. G. (1994). Digestive physiology. In Davies, A. G., and Oates, J. F. (eds.),Colobine Monkeys: Their Evolutionary Ecology, Cambridge University Press, Cambridge, pp. 229–249.

    Google Scholar 

  • Kinnaird, M. F. (1992). Phenology of flowering and fruiting of an East African riverine forest ecosystem.Biotropica 24(2a): 187–194.

    Article  Google Scholar 

  • Krebs, J. R., and Kacelnik, A. (1991). Decision-making. In Krebs, J. R., and Davies, N. B. (eds.),Behavioural Ecology: An Evolutionary Approach, 3rd ed., Blackwell Scientific, Cambridge, pp. 105–136.

    Google Scholar 

  • Lee, P. C., Thornback, J., and Bennett, E. (1988).Threatened Primates of Africa. IUCN Red Data Book, IUCN, Cambridge.

    Google Scholar 

  • MacArthur, R. H., and Pianka, E. R. (1966). On the optimal use of a patchy environment.Am. Nat. 100: 603–609.

    Article  Google Scholar 

  • Macauley, B. J., and Fox, L. R. (1980). Variation in total phenols and condensed tannins inEucalyptus: Leaf phenology and insect grazing.Austral J. Ecol. 5: 31–35.

    Article  Google Scholar 

  • Maiseis, F., and Gautier-Hion, A. (1994). Why are Caesalpinioideae so important for monkeys in hydromorphic rainforests of the Zaire basin? In Sprent, J. I., and McKey, D. (eds.),Advances in Legume Systematics 5: The Nitrogen Factor, Royal Botanic Gardens, Kew, pp. 189–204.

    Google Scholar 

  • Maiseis, F., Gautier-Hion, A., and 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(5): 681–701.

    Google Scholar 

  • Marks, D. L., Swain, T., Goldstein, S., Richard, A., and Leighton, M. (1988). Chemical correlates of rhesus monkey food choice: The influence of hydrolyzable tannins.J. Chem. Ecol. 14(1): 213–235.

    Article  CAS  Google Scholar 

  • Marsh, C. W. (1978a).Ecology and Social Organization of the Tana River Red Colobus (Colobus badius rufomitratus), Ph.D. dissertation, University of Bristol, Bristol, UK.

    Google Scholar 

  • Marsh, C. W. (1978b). Tree phenology in a gallery forest on the Tana River, Kenya.East Afr. Agr. Forest. J. 43(4): 305–316.

    Google Scholar 

  • Marsh, C. W. (1981a). Diet choice among red colobus(Colobus badius rufomitratus) on the Tana River, Kenya.Folia Primatol 35: 147–178.

    PubMed  CAS  Google Scholar 

  • Marsh, C. W. (1981b). Ranging behavior and its relation to diet selection in Tana River red colobus(Colobus badius rufomitratus).J. Zool. Lond. 195: 473–492.

    Article  Google Scholar 

  • Marsh, C. W. (1986). A resurvey of Tana River primates and their habitat.Primate Conserv. 7: 72–82.

    Google Scholar 

  • Martin, J. S., Martin, M. M., and Bernays, E. A. (1987). Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: Implications for theories of plant defense.J. Chem. Ecol. 13(3): 605–621.

    Article  CAS  Google Scholar 

  • Maynard, A. B., and Loosli, J. K. (1969).Animal Nutrition, McGraw-Hill, New York.

    Google Scholar 

  • McKey, D. (1978). Soils, vegetation and seed-eating by black colobus monkeys. In Montgomery, G. G. (ed.),The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington, DC, pp. 423–437.

    Google Scholar 

  • McKey, D. (1979). The distribution of secondary compounds within plants. In Rosenthal, G. A., and Janzen, D. H. (eds.),Herbivores: Their Interaction with Secondary Plant Metabolites, Academic Press, New York, pp. 56–133.

    Google Scholar 

  • McKey, D., Gartlan, S. G., Waterman, P. G., and Choo, G. N. (1981). Food selection by black colobus monkeys(Colobus satanas) in relation to plant chemistry.Biol. J. Linnean Soc. 16: 115–146.

    Google Scholar 

  • Medley, K. E. (1990).Forest Ecology and Conservation in the TRNPR, Kenya, Ph.D. dissertation. Michigan State University, East Lansing.

    Google Scholar 

  • Medley, K. E. (1992). Patterns of forest diversity along the Tana River, Kenya.J. Trop. Ecol. 8: 353–371.

    Google Scholar 

  • Milton, K. (1979). Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food choice by generalist herbivores.Am. Nat. 114: 362–378.

    Article  CAS  Google Scholar 

  • Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species.Am. Nat. 117: 495–505.

    Article  Google Scholar 

  • Moir, R. J. (1968). Ruminant digestion and evolution.Handbk. Physiol. (Sect. 6) 5: 2673–2694.

    Google Scholar 

  • Mole, S., and Waterman, P. G. (1987). Tannins as antifeedants to mammalian herbivores-still an open question? In Waller, G. R. (ed.),Allelochemicals: Role in Agriculture and Forestry, American Chemical Society Symposium Series, American Chemical Society Press, Washington, DC, pp. 572–587.

    Google Scholar 

  • Nagy, K. A., and Milton, K. (1979). Aspects of dietary quality, nutrient assimilation and water balance in wild howler monkeys(Alouatta palliata).Oecologia 39: 249–258.

    Article  Google Scholar 

  • Oates, J. F. (1977). The guereza and its food. In Clutton-Brock, T. H. (ed.),Primate Ecology, Academic Press, London, pp. 276–321.

    Google Scholar 

  • Oates, J. F., Swain, T., and Zantovska, J. (1977). Secondary compounds and food selection by colobus monkeys.Biochem. Syst. Ecol. 5: 317–321.

    Article  CAS  Google Scholar 

  • Oates, J. F., Waterman, P. G., and Choo, G. M. (1980). Food selection by a South Indian leaf-monkey,Presbytis johnii, in relation to leaf chemistry.Oecologia 45: 45–56.

    Article  Google Scholar 

  • Oates, J. F., Gartlan, J. S., and Struhsaker, T. T. (1987). A framework for African rain forest primate conservation. In Marsh, C. W., and Mittermeier, R. A. (eds.),Primate Conser- vation in the Tropical Rain Forest, Alan R. Liss, New York, pp. 321–327.

    Google Scholar 

  • Oates, J. F., Whitesides, G. H., Davies, A. G., Waterman, P. G., Green, S. M., Dasilva, G. L., and Mole, S. (1990). Determinants of variation in tropical forest primate biomass: New evidence from West Africa.Ecology 71(1): 328–343.

    Article  Google Scholar 

  • Parra, R. (1978). Comparison of foregut and hindgut fermentation in herbivores. In Montgomery, G. G. (ed.),The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC, pp. 205–229.

    Google Scholar 

  • Post, D. G. (1984). Is optimization the optimal approach to primate foraging? In Rodman, P. S., and Cant, J. G.(eds.),Adaptations for Foraging in Nonhuman Primates, Columbia University Press, New York, pp. 280–303.

    Google Scholar 

  • Rhoades, D. F., and Cates, R. G. (1976). Toward a general theory of plant antiherbivore chemistry. In Wallace, J., and Mansell, R. L. (eds.),Biochemical Interactions Between Plants and Insects, Recent Advances in Phytochemistry 10, Plenum Press, New York, pp. 168–213.

    Google Scholar 

  • Richard, A. F. (1985).Primates in Nature, W. H. Freeman, New York.

    Google Scholar 

  • Rosner, B. (1990).Fundamentals of Biostatistics, 3rd ed., PWS-Kent, Boston.

    Google Scholar 

  • Schoener, T. W. (1971). Theory of feeding strategies.Annu. Rev. Ecol. Syst. 2: 369–403.

    Article  Google Scholar 

  • Seal, U. S., Lacy, R. C., Medley, K., Seal, R., and Foose, T. J. (1991).Tana River Primate Reserve Conservation Assessment Workshop Report, CBSG/SSC/IUCN, Kenya Wildlife Service and World Bank, Apple Valley, MN.

    Google Scholar 

  • Shure, D. J., and Wilson, L. A. (1993). Patch size effects on plant chemical defenses in successional openings of the Southern Appalachians.Ecology 74(1): 55–67.

    Article  CAS  Google Scholar 

  • Stephens, D. W., and Krebs, J. R. (1986).Foraging Theory, Princeton University Press, Princeton, NJ.

    Google Scholar 

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

    Google Scholar 

  • Struhsaker, T. T. (1981). Forest and primate conservation in East Africa.Afr. J. Ecol. 19: 99–114.

    Google Scholar 

  • Swain, T., and Hillis, W. E. (1959). The phenolic constituents ofPrunus domestica. I. The quantitative analysis of phenolic constituents.J. Agr. Food Sci. 10: 63–68.

    Article  CAS  Google Scholar 

  • Waterman, P. G. (1984). Food acquisistion and processing as a function of plant chemistry. In Chivers, D. J., Wood, B. A., and Bilsborough, A. (eds.),Food Acquisition and Processing in Primates, Plenum Press, New York, pp. 177–211.

    Google Scholar 

  • Waterman, P. G. (1986). A phytochemist in the rain forest.Phytochemistry 25(1): 3–17.

    Article  CAS  Google Scholar 

  • Waterman, P. G., and Choo, G. M. (1981). The effects of digestibility reducing compounds in leaves on food selection by some Colobinae.Malays. Appl. Biol. 10: 147–162.

    Google Scholar 

  • Waterman, P. G., and Kool, K. M. (1994). Colobine food selection and plant chemistry. In Davies, A. G., and Oates, J. F. (eds.),Colobine Monkeys: Their Evolutionary Ecology, Cambridge University Press, Cambridge, pp. 251–284.

    Google Scholar 

  • Waterman, P. G., Mbi, C. N., McKey, D. B., and Gartlan, J. S. (1980). African rainforest vegetation and rumen microbes: phenolic compounds and nutrients as correlates of digestability.Oecologia 47: 22–33.

    Article  Google Scholar 

  • Waterman, P. G., Ross, J. A. M., Bennett, E. L., and Davies, A. G. (1988). A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World.Biol. J. Linn. Soc. 34: 1–32.

    Google Scholar 

  • Westoby, M. (1974). An analysis of diet selection by large generalist herbivores. Am. Nat. 108: 290–304.

    Article  Google Scholar 

  • White, F. (1983).The Vegetation of Africa, UNESCO, Paris.

    Google Scholar 

  • Wrangham, R., and Waterman, P. G. (1981). Feeding behaviour of vervet monkeys onAcacia products.J. Anim. Ecol. 50: 715–731.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mowry, C.B., Decker, B.S. & Shure, D.J. The role of phytochemistry in dietary choices of Tana River red colobus monkeys(Procolobus badius rufomitratus) . International Journal of Primatology 17, 63–84 (1996). https://doi.org/10.1007/BF02696159

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02696159

Key words

Navigation