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International Journal of Primatology

, Volume 24, Issue 3, pp 541–573 | Cite as

Mineral Resource Availability and Consumption by Colobus in Kibale National Park, Uganda

  • Karyn D. Rode
  • Colin A. Chapman
  • Lauren J. Chapman
  • Lee R. McDowell
Article

Abstract

Very little information exists on mineral nutrition of tropical, forest-dwelling species, yet minerals are critical to growth, reproduction, and survival. We examined the mineral resources available to and consumed by colobus in Kibale National Park, Uganda. We combined behavioral data on black-and-white (Colobus guereza) and red colobus (Piliocolobus tephrosceles) in a section of unlogged forest, a heavily logged area, and a forest fragment with mineral analysis of their foods to estimate the proportion of the diet containing specific minerals (mineral content). We compared mineral content of colobus foods (natural and crops) across plant parts and among plant species. Additionally, we estimated mineral intake of frugivorous primates in Kibale from published dietary data and our estimates of mineral content of foods. Dietary mineral content for all colobus groups and frugivorous species is similar despite significant differences in the mineral content of foods. Ripe and unripe fruits are lower in mineral content than most foods. Foods rarely consumed, such as bark, petioles, and caterpillars have high levels of some minerals. The mineral content of crops is low in comparison to that ofnatural foods. For all colobus groups of both species, sodium content of foods was extremely low and iron content was generally low, suggesting that intake isbelow suggested requirements, though current suggested iron requirements may overestimate physiological needs. Copper content was marginal and deficient seasonally for most colobus groups. Despite a sodium-limiting environment, only one of 8 colobus groups appeared to select sodium; however, this may be due to a lack of variation in sodium content among plant species and a positive correlation between high plant sodium content and secondary compounds. Despite the lack of selection for sodium by colobines, some behaviors point to a potential sodium deficiency, including urine drinking, consumption of high-sodium swamp plants, and use of mud-puddles.

colobines minerals nutrition herbivory crop raiding foraging sodium population regulation 

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References

  1. Altmann, S. A. (1998). Foraging for Survival: Yearling Baboons in Africa, University of Chicago Press, Chicago.Google Scholar
  2. Baranga, D. (1983). Changes in chemical composition of food parts in the diet of colobus monkeys. Ecology 64: 668-673.Google Scholar
  3. Barker, D., Fitzpatrick, M. P., and Dierenfeld, E. S. (1998). Nutrient composition of selected whole invertebrates. Zoo Biol. 17: 123-134.Google Scholar
  4. Beck, J., Muhlenberg, E., and Fiedlerm K. (1999). Mud-puddling behavior in tropical butterflies: In search of proteins or minerals. Oecologia 119: 140-148.Google Scholar
  5. Bell, F. R. (1995). Perception of sodium appetite in farm animals. In Phillips, C. J. C., and Chiy, P.C. (Eds.), Sodium in Agriculture, Cantebury, UK, pp. 82-90.Google Scholar
  6. Belovsky, G. E. (1981). A possible population response of moose to sodium availability. J. Mammal. 62: 631-633.Google Scholar
  7. Blair-West, J. R., Coghlan, J. P., Denton, D. A., Nelson, J. F., Orchard, E., Scoggins, B. A., Wright, R. D., Myers, K., and Jungueira, C. L. (1968). Physiological, morphological, and behavioral adaptations to a sodium deficient environment by wild native Australian and introduced species of animals. Nature 217: 922-928.Google Scholar
  8. Buss, D. H., and Cooper, R. W. (1970). Composition of milk from talapoin monkeys. Folia Primatol. 13: 196-206.Google Scholar
  9. Chapman, C. A., and Chapman, L. J. (1997). Forest regeneration in logged and unlogged forests of Kibale National Park, Uganda. Biotropica 29: 396-412.Google Scholar
  10. Chapman, C. A., and Chapman, L. J. (1999). Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primate 40: 215-232.Google Scholar
  11. Chapman, C. A., and Chapman, L. J. (2002). Foraging challenges of red colobus monkeys: Influence of nutrients and secondary compounds. Comp. Biochem. Physiol. 133: 861-875.Google Scholar
  12. Chapman, C. A., Chapman, L. J., Bjorndal, K. A., and Onderdonk, D. A. (2002). Application of protein to fiber ratios to predict colobine abundance on different spatial scales. Int. J. Primatol. 23: 283-310.Google Scholar
  13. Chapman, C. A., Chapman, L. J., Cords, M., Gathua, M. J., Gautier-Hion, A., Lambert, J. E., Rode, K. D., Tutin, C. E. G., and White, L. J. T. (2002). Variation in the diets of Cercopithecus species: Differences within forests, among forests, and across species. In Glenn, M., and Cords, M. (eds), The Guenons: Diversity and Adaptation in African Monkeys, Plenum Press, New York, pp. 325-350.Google Scholar
  14. Chapman, L. J., Chapman, C. A., Crisman, T. L., and Nordlie, F. G. (1998). Dissolved oxygen and thermal regimes of a Ugandan crater lake. Hydrobiologia 385: 201-211.Google Scholar
  15. Chapman, C. A., and Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: A case study of Kibale National Park, Uganda. Am. J. Primatol. 50: 169-186.Google Scholar
  16. Chapman, C. A., Lawes, M. J., Naughton-Treves, L., Gillespie, T. R. (2003). Primate survival in community-owned forest fragments: Are metapopulation models useful amidst intensive use. In Marsh, L. K. (ed.), Primates in Fragments: Ecology and Conservation, Kluwer Academic/Plenum, New York, pp. 63-78.Google Scholar
  17. Chiy, P. C., and Phillips, C. J. C. (1995). Sodium in ruminant nutrition, production, reproduction, and health. In Phillips, C. J. C., and Chiy, P. C. (Eds.), Sodium in Agriculture, Cantebury, UK, pp. 107-144.Google Scholar
  18. Conover, M. R. (1998). Perceptions of American agricultural producers about wildlife on their farms and ranches. Wildl. Soc. Bull. 26: 597-604.Google Scholar
  19. Crissey, S. D., and Pribyl, L. S. (1997). Utilizing wild foraging ecology information to provide captive primates with an appropriate diet. Proc. Nutr. Soc. 56: 1083-1094.Google Scholar
  20. Cunningham-Rundles, S., and Ho Lin, D. (1998). Nutrition and the immune system of the gut. Nutrition 14: 573-579.Google Scholar
  21. Delgiudice, G. D., Singer, F. J., Seal, U. S., and Bowser G. (1994). Physiological responses of Yellowstone bison to winter nutritional deprivation. J. Wildl. Manage. 58: 24-34.Google Scholar
  22. Dierenfeld, E. S., and McCann, C. M. (1999). Nutrient composition of selected species consumed by semi free-ranging lion-tailed macaques (Macaca silenus) and ring-tailed lemurs (Lemur catta) on St. Catherines Island, Georgia, U.S.A. Zoo Biol. 18: 481-494.Google Scholar
  23. Dorrestein, G. M., de Sa, L., Ratiarison, S., and Mete, A. (2000). Iron in the liver of animals in the zoo: A pathologist's point of view. In Nijboer, J., Hatt, J.-M., Kaumanns, W., Beijnen, A., and Ganslosser, U. (Eds.), Zoo Animal Nutrition, Filander Verlag, Furth, The Netherlands, pp. 291-299.Google Scholar
  24. Faber, W. E., Pehrson, A., and Jordan, P. A. (1993). Seasonal use of salt blocks by mountain hares in Sweden. J. Wildl. Manage 57: 842-846.Google Scholar
  25. Fox, L. M., Krausman, P. R., Morrison, M. L., and Noon, T. H. (2000). Mineral content of Sonoran pronghorn forage. Calif. Fish Game 86: 159-174.Google Scholar
  26. Fraser, D. (1979). Aquatic feeding by the woodchuck. Can. Field Nat. 93: 309-310.Google Scholar
  27. Fraser, D., Chavez, E. R., and Paloheimo, J. E. (1984). Aquatic feeding by moose: Selection of plant species and feeding areas in relation to plant chemical composition and characteristics of lakes. Can. J. Zool. 62: 80-87.Google Scholar
  28. Hailey, A., and Coulson, I. M. (1996). Differential scaling of home range to daily movement in two African tortoises. Can. J. Zool. 74: 97-102.Google Scholar
  29. Hambidge, M. (2000). Human zinc deficiency. J. Nutr. 130: 1344-1349.Google Scholar
  30. Hellgren, E. C., and Pitts, W. J. (1997). Sodium economy in white-tailed deer (Odocoileus virginianus). Phys. Zool. 70: 547-555.Google Scholar
  31. Hladik, C. M. (1978). Adaptive strategies of primates in relation to leaf-eating. In Montgomery, G. C. (ed.), The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington, DC, pp. 373-395.Google Scholar
  32. Holdo, R. M., Dudley, J. P., and McDowell, L. R. (2002). Environmental sodium availability and mineral lick use in the African elephant. J. Mammal. 83: 652-664.Google Scholar
  33. Hotz, C., and Brown, K. H. (2001). Identifying populations at risk of zinc deficiency: The uses of supplementation trials. Nutr. Res. 59: 80-89.Google Scholar
  34. Jackson, J. L., Lesho, E., and Peterson, C. (2000). Zinc and the common cold: A meta-analysis revisited. J. Nutr. 130: 1512-1515.Google Scholar
  35. Janson, C. H., and Chapman, C. A. (2000). Primate resources and the determination of primate community structure. In Fleagle, J. G., Janson, C. H., and Reed, K. (Eds.), Primate Communities, Cambridge University Press, Cambridge, England, pp. 237-267.Google Scholar
  36. Kaumanns, W., Hampe, K., Schwitzer, C., and Stahl, D. (2000). Primate nutrition: towards an integrated approach. In Nijboer, J., Hatt, J.-M., Kaumanns, W., Beijnen, A., and Ganslosser, U. (Eds.), Zoo Animal Nutrition, Filander Verlag, Furth, The Netherlands, pp. 91-106.Google Scholar
  37. Krishnamani, R., and Mahaney, W. C. (2000). Geophagy among primates: Adaptive significance and ecological consequences. Anim. Beh. 59: 899-915.Google Scholar
  38. Lambert, J. E. (2000). Urine drinking in wild Cercopithecus ascanius: Evidence of nitrogen balancing? Afr. J. Ecol. 38: 360-362.Google Scholar
  39. Laska, M., Salazar, L. T. H., and Luna, E. R. (2000). Food preferences and nutrient composition in captive spider monkeys, Ateles geoffroyi. Int. J. Primatol. 21: 671-683.Google Scholar
  40. MacCracken, J. G., Vanballenberghe, V., and Peek, J. M. (1993). Use of aquatic plants by moose—Sodium hunger or foraging efficiency. Can. J. Zool. 71: 2345-2351.Google Scholar
  41. Marriott, B. M., Smith, J. C., Jacobs, R. M., Jones, A. O. L., and Altmann, J. D. (1996). Copper, iron, manganese, and zinc content of hair from two populations of rhesus monkeys. Biol. Trace Element Res. 53: 167-183.Google Scholar
  42. Masters, D. G., Norman, N. C., and Dynes, R. A. (2001). Opportunities and limitations for animal production from saline land. Asian-Australasian. J. Anim. Sci. 14: 199-211.Google Scholar
  43. Mattfield, G. F., Wiley, J. E., III, and Behrend, D. F. (1972). Salt versus browse-seasonal baits for deer trapping. J. Wildl. Manage. 36: 996-998.Google Scholar
  44. McDowell, L. R. (1985). Nutrition of Grazing Ruminants in Warm Climates, Academic Press, New York.Google Scholar
  45. McDowell, L. R. (1992). Minerals in Animal and Human Nutrition, Academic Press, New York.Google Scholar
  46. McDowell, L. R. (1997). Minerals for Grazing Ruminants in Tropical Regions, University of Florida, Gainesville.Google Scholar
  47. McNaughton, S. J. (1988). Mineral nutrition and spatial concentrations of African ungulates. Nature 334: 343-345.Google Scholar
  48. Melack, J. M. (1978). Morphometric, physical and chemical features of the volcanic crater lakes of western Uganda. Arch. HydroBiol. 84: 430-453.Google Scholar
  49. Miles, P. H., Wilkinson, N. S., and McDowell, L. R. (2001). Analysis of Minerals for Animal Nutrition Research, Department of Animal Sciences, University of Florida, Gainesville.Google Scholar
  50. Milewski, A. (2000). Iodine as a possible controlling nutrient for elephant populations. Pachyderm 28: 78-90.Google Scholar
  51. Miller, B. K., and Litvaitis, J. A. (1992). Use of roadside saltlicks by moose, Alces alces, in Northern New Hampshire. Can. Field-Nat. 106: 112-117.Google Scholar
  52. Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. J. Zool. 239: 39-63.Google Scholar
  53. Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest living relative have lessons for us? Nutrition 15: 488-498.Google Scholar
  54. Milton, K. (2000). Back to basics: Why foods of wild primates have relevance for modern human health. Nutrition 16: 480-483.Google Scholar
  55. Minatel, L., and Carfagnini, J. C. (2000). Copper deficiency and immune response in ruminants. Nutr. Res. 20: 1519-1529.Google Scholar
  56. 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.Google Scholar
  57. National Bureau of Standards (1982). U.S. Dept of Commerce. Standard Ref. Material 1572: Citrus Leaves, Washington, DC.Google Scholar
  58. National Research Council (1978). Nutrient Requirements of Non-Human Primates, National Academy Press, Washington, DC.Google Scholar
  59. National Research Council (1984). Nutrient Requirements of Domestic Animals, Nutrient Requirements of Beef Cattle, 6th edn., National Academy of Sciences, Washington, DC.Google Scholar
  60. Naughton-Treves, L. (1998). Predicting patterns of crop raiding by wildlife around Kibale National Park, Uganda. Con. Biol. 12: 151-168.Google Scholar
  61. NIST (1998). Standard Reference Material Catalog. NIST Publications 260, Gaithersburg, MD.Google Scholar
  62. Nicolosi, R. J., and Hunt, R. D. (1979). Dietary allowances for nutrients in nonhuman primates. In Hayes, K. C. (ed.), Primates in Nutritional Research, Academic Press, New York.Google Scholar
  63. Oates, J. F. (1978). Water-plant and soil consumption by guereza monkeys (Colobus guereza): A relationship with minerals and toxins in the diet? Biotropica 10: 241-253.Google Scholar
  64. 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: 328-343.Google Scholar
  65. Oftedal, O. T. (1991). The nutritional consequences of foraging in primates: The relationship of nutrient intakes to nutrient requirements. Phil. Trans. R. Soc. London 334: 161-170.Google Scholar
  66. Pletscher, D. H. (1987). Nutrient budgets for white-tailed deer in New England with special reference to sodium. J. Mammal. 68: 330-336.Google Scholar
  67. Power, M. L., Tardif, S. D., Layne, D. G., and Schulkin, J. (1999). Ingestion of calcium solutions by common marmosets (Callithrix jacchus). Am. J. Primatol. 47: 255-261.Google Scholar
  68. Ramirez, R. G., Haenlein, G. F. W., Trevino, A., and Reyna, J. (1996). Nutrient and mineral profile of white-tailed deer (Odocoileus virginianus, texanus) diets in northeastern Mexico. Small Ruminant Res. 23: 7-16.Google Scholar
  69. Robbins, C. T. (1993). Wildlife Feeding and Nutrition, Academic Press, New York.Google Scholar
  70. Ruel, M. T., and Bouis, H. E. (1998). Plant breeding: A long-term strategy for the control of zinc deficiency in vulnerable populations. Am. J. Clin. Nutr. 68: 488-494.Google Scholar
  71. Sandstead, H. H., and Lofgren, P. A. (2000). Symposium: Dietary zinc and iron—Recent perspectives regarding growth and development. J. Nutr. 130: 345-346.Google Scholar
  72. Schwitzer, C., and Kaumanns, W. (2000). Feeding behaviour in two captive groups of black and white ruffed lemurs (Varecia v. variegata), Kerr 1792. In Nijboer, J., Hatt, J.-M., Kaumanns, W., Beijnen, A., and Ganslosser, U. (Eds.), Zoo Animal Nutrition, Filander Verlag, Furth, The Netherlands, pp. 119-130.Google Scholar
  73. Silver, S. C., Ostro, L. E. T., Yeager, C. P., and Dierenfeld, E. S. (2000). Phytochemical and mineral components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize. Zoo Biol. 19: 95-109.Google Scholar
  74. Skorupa, J. (1988). The Effect of Selective Timber Harvesting on Rain-forest Primates in Kibale Forest, Uganda. PhD Dissertation, University of California, Davis.Google Scholar
  75. Smith, W. H. (1976). Character and significance of forest tree root exudates. Ecology 57: 324-331.Google Scholar
  76. Spelman, L. H., Osborn, K. G., and Anderson, M. P. (1989). Pathogenesis of hemosiderosis in lemurs: Role of dietary iron, tannin, and ascorbic acid. Zoo Biol. 8: 239-251.Google Scholar
  77. Struhsaker, T. T. (1997). Ecology of an African Rain Forest: Logging in Kibale and the Conflict Between Conservation and Exploitation, University Presses of Florida, Gainesville.Google Scholar
  78. Sukumar, R. (1990). Ecology of the Asian elephant in southern India. II: Raiding habits and crop raiding patterns. J. Trop. Ecol. 6: 33-53.Google Scholar
  79. Sukumar, R., and Gadgil, M. (1988). Male-female differences in foraging on crops by Asian elephants. Anim. Behav. 36: 1233-1235.Google Scholar
  80. Sun, C., Moermond, T. C., and Givnish, T. J. (1997). Nutritional determinants of diet in three turacos in a tropical montane forest. Auk 114: 200-211.Google Scholar
  81. Weeks, H. P., Jr., and Kirkpatrick, C. M. (1978). Salt preferences and sodium drive phenology in fox squirrels and woodchucks. J. Mammal. 59: 531-542.Google Scholar
  82. Weir, J. S. (1972). Spatial distribution of elephants in an African national park in relation to environmental sodium. Oikos 23: 1-13.Google Scholar
  83. Wrangham, R. W., Conklin-Brittain, N. L., and Hunt, K. D. (1998). Dietary responses of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I: Antifeedants. Int. J. Primatol. 19: 949-970.Google Scholar
  84. Yeager, C. P., Silver, S. C., and Dierenfeld, E. S. (1997). Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). Am. J. Primatol. 41: 117-128.Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Karyn D. Rode
    • 1
  • Colin A. Chapman
    • 1
    • 2
  • Lauren J. Chapman
    • 1
    • 2
  • Lee R. McDowell
    • 3
  1. 1.Department of ZoologyUniversity of FloridaGainesville
  2. 2.Wildlife Conservation SocietyBronx
  3. 3.Animal Sciences DepartmentUniversity of FloridaGainesville

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