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

  • Christopher B. Mowry
  • Barbara S. Decker
  • Donald J. Shure
Article

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.

Key words

phytochemistry Procolobus badius rufomitratus riverine forest leguminous trees 

References

  1. Bate-Smith, E. C. (1972). Detection and determination of ellagitannins.Phytochemistry 11: 1153–1156.CrossRefGoogle Scholar
  2. Bate-Smith, E. C. (1975). Phytochemistry of proanthocyanidins.Phytochemistry 14: 1107–1113.CrossRefGoogle Scholar
  3. Bate-Smith, E. C. (1977). Astringent tanninsof Acer species.Phytochemistry 16: 1421–1426.CrossRefGoogle Scholar
  4. Bate-Smith, E. C. (1981). Astringent tannins of the leaves ofGeranium species.Phytochemistry 20: 211.CrossRefGoogle Scholar
  5. 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
  6. Bauchop, T., and Martucci, R. W. (1968). Ruminant-like digestion of the langur monkey.Science 161: 698–699.PubMedCrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.Google Scholar
  9. 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
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Coley, P. D. (1983). Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol. Monogr. 53(2): 209–233.CrossRefGoogle Scholar
  13. 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
  14. Coley, P. D., Bryant, J. P., and Chapin, F. S., III (1985). Resource availability and plant antiherbivore defense.Science 230: 895–899.CrossRefPubMedGoogle Scholar
  15. 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
  16. 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
  17. 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
  18. 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.CrossRefGoogle Scholar
  19. Emlen, J. M. (1966). The role of time and energy in food choice.Am. Nat. 100: 611–617.CrossRefGoogle Scholar
  20. Farnsworth, N. R. (1966). Biological and phytochemical screening of plants.J. Pharm. Sci. 55(3): 225–276.PubMedCrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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
  23. 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
  24. Fraenkel, G. (1959). The raison d'etre of secondary plant substances.Science 121: 1466–1470.CrossRefGoogle Scholar
  25. Freeland, W. J., and Janzen, D. H. (1974). Strategies in herbivory by mammals: The role of plant secondary compounds.Am. Nat. 108: 269–289.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Glander, K. E. (1982). The impact of secondary compounds on primate feeding behavior.Yrbk. Phys. Anthropol. 25: 1–18.CrossRefGoogle Scholar
  28. 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
  29. Harborne, J. B. (1982).Introduction to Ecological Biochemistry, 2nd ed., Academic Press, New York.Google Scholar
  30. Harper, J. L. (1989). The value of a leaf.Oecologia 80: 53–58.CrossRefGoogle Scholar
  31. Hoberg, P. (1986). Soil nutrient availability, root symbioses amd tree species composition in tropical Africa: A review.J. Trop. Ecol. 2: 359–372.CrossRefGoogle Scholar
  32. Hughes, F. M. R. (1988). The ecology of African floodplain forests: A review.J. Biogeogr. 15: 127–140.CrossRefGoogle Scholar
  33. 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
  34. Kinnaird, M. F. (1992). Phenology of flowering and fruiting of an East African riverine forest ecosystem.Biotropica 24(2a): 187–194.CrossRefGoogle Scholar
  35. 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
  36. Lee, P. C., Thornback, J., and Bennett, E. (1988).Threatened Primates of Africa. IUCN Red Data Book, IUCN, Cambridge.Google Scholar
  37. MacArthur, R. H., and Pianka, E. R. (1966). On the optimal use of a patchy environment.Am. Nat. 100: 603–609.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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
  40. 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
  41. 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.CrossRefGoogle Scholar
  42. 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
  43. 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
  44. Marsh, C. W. (1981a). Diet choice among red colobus(Colobus badius rufomitratus) on the Tana River, Kenya.Folia Primatol 35: 147–178.PubMedGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Marsh, C. W. (1986). A resurvey of Tana River primates and their habitat.Primate Conserv. 7: 72–82.Google Scholar
  47. 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.CrossRefGoogle Scholar
  48. Maynard, A. B., and Loosli, J. K. (1969).Animal Nutrition, McGraw-Hill, New York.Google Scholar
  49. 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
  50. 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
  51. 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
  52. Medley, K. E. (1990).Forest Ecology and Conservation in the TRNPR, Kenya, Ph.D. dissertation. Michigan State University, East Lansing.Google Scholar
  53. Medley, K. E. (1992). Patterns of forest diversity along the Tana River, Kenya.J. Trop. Ecol. 8: 353–371.Google Scholar
  54. 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.CrossRefGoogle Scholar
  55. Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species.Am. Nat. 117: 495–505.CrossRefGoogle Scholar
  56. Moir, R. J. (1968). Ruminant digestion and evolution.Handbk. Physiol. (Sect. 6) 5: 2673–2694.Google Scholar
  57. 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
  58. 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.CrossRefGoogle Scholar
  59. 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
  60. Oates, J. F., Swain, T., and Zantovska, J. (1977). Secondary compounds and food selection by colobus monkeys.Biochem. Syst. Ecol. 5: 317–321.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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
  63. 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.CrossRefGoogle Scholar
  64. 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
  65. 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
  66. 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
  67. Richard, A. F. (1985).Primates in Nature, W. H. Freeman, New York.Google Scholar
  68. Rosner, B. (1990).Fundamentals of Biostatistics, 3rd ed., PWS-Kent, Boston.Google Scholar
  69. Schoener, T. W. (1971). Theory of feeding strategies.Annu. Rev. Ecol. Syst. 2: 369–403.CrossRefGoogle Scholar
  70. 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
  71. 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.CrossRefGoogle Scholar
  72. Stephens, D. W., and Krebs, J. R. (1986).Foraging Theory, Princeton University Press, Princeton, NJ.Google Scholar
  73. Struhsaker, T. T. (1975).The Red Colobus Monkey, University of Chicago Press, Chicago.Google Scholar
  74. Struhsaker, T. T. (1981). Forest and primate conservation in East Africa.Afr. J. Ecol. 19: 99–114.Google Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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
  77. Waterman, P. G. (1986). A phytochemist in the rain forest.Phytochemistry 25(1): 3–17.CrossRefGoogle Scholar
  78. 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
  79. 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
  80. 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.CrossRefGoogle Scholar
  81. 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
  82. Westoby, M. (1974). An analysis of diet selection by large generalist herbivores. Am. Nat. 108: 290–304.CrossRefGoogle Scholar
  83. White, F. (1983).The Vegetation of Africa, UNESCO, Paris.Google Scholar
  84. Wrangham, R., and Waterman, P. G. (1981). Feeding behaviour of vervet monkeys onAcacia products.J. Anim. Ecol. 50: 715–731.CrossRefGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • Christopher B. Mowry
    • 1
  • Barbara S. Decker
    • 2
  • Donald J. Shure
    • 1
  1. 1.Department of BiologyEmory UniversityAtlanta
  2. 2.National Museums of KenyaNairobiKenya
  3. 3.Big Canoe
  4. 4.Berry College Department of BiologyMt. BerryGeorgia

Personalised recommendations