A 12-Year Phenological Record of Fruiting: Implications for Frugivore Populations and Indicators of Climate Change

  • Colin A. Chapman
  • Lauren J. Chapman
  • Amy E. Zanne
  • John R. Poulsen
  • Connie J. Clark


Answering the fundamental ecological question of what determines animal abundance has become critical with the accelerating need for informed management plans for endangered species. A major difficulty in testing general hypotheses to account for variation in abundance is that periods of food scarcity, which may be responsible for limiting population size, occur on a superannual basis. Research on folivorous primates suggests that periods of food scarcity are critical in determining regional biomass; however, studies of frugivores have found no single fallback food generally used by all species. In this study we quantify fruit availability during a 12-year period in Kibale National Park, Uganda to determine patterns of fruit scarcity. Over these 12 years, temporal variability in fruit availability was high; the proportion of trees per month with ripe fruit varied from 0.14 to 15.93%. In addition, there was dramatic interannual variation in fruit availability: in 1990, on average only 1.09% of trees bore ripe fruit each month, while in 1999 an average of 6.67% of trees bore fruit each month. Over the past 12 years, fruit has become more available, fruit-scarce months have declined in frequency, and the duration of periods of fruit scarcity has decreased. If figs (Ficus spp.) served as a fallback food resource over these 12 years, they would have had to be available during months when few trees were fruiting. Over this 149-month period, there were 34 months when less than 1% of monitored trees fruited. Figs were not fruiting in 17 of these months, and, in only 11 of the 34 months were more than 1% of the fig trees fruiting. Rainfall data collected since 1903 indicates that the region is becoming moister, and droughts are less frequent. There has also been a significant increase in the maximum mean monthly temperature and a decrease in the minimum mean monthly temperature since we started recording these data in 1990.

Key words

Bottlenecks conservation fruit frugivore global climate change keystone species phenology Uganda 


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  1. Andrewartha, H. G., and L. C. Birch. 1954. The distribution and abundance of animals. University of Chicago Press, Chicago.Google Scholar
  2. Borges, R. M. 1993. Figs, Malabar giant squirrels, and fruit shortages within two tropical Indian forests. Biotropica 25, 183–190.Google Scholar
  3. Boutin, S. 1990. Food supplementation experiments with terrestrial vertebrates: Patterns, problems, and the future. Canadian Journal of Zoology 68, 203–220.Google Scholar
  4. Bush, M. B. 2000. Ecology of a changing planet. Prentice Hall, Upper Saddle River, New Jersey.Google Scholar
  5. Butynski, T. M. 1988. Guenon birth seasons and correlates with rainfall and food. In A. Gautier-Hion, F. Bourliere, J-P. Gautier, and J. Kingdon (Eds.). A primate radiation: evolutionary biology of African guenons, pp. 284–322. Cambridge University Press, Cambridge, England.Google Scholar
  6. Chapman, C. A. 1987. Flexibility in diets of three species of Costa Rican primates. Folia Primatologica 49, 90–105.CrossRefGoogle Scholar
  7. 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
  8. Chapman, C. A. and Chapman, L. J. 1990. Dietary variability in primate populations. Primates 31, 121–128.Google Scholar
  9. Chapman, C. A., Chapman, L.J., Bjorndal, K. A., and Onderdonk, D.A. 2002a. Application of protein to fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology 23, 283–310.CrossRefGoogle Scholar
  10. Chapman, C. A., Chapman, L. J., Cords, M., Gauthua, M., Gautier-Hion, A., Lambert, J. E., Rode, K. D., Tutin, C. E. G., and White, L. J. T. 2002b. Variation in the diets of Cercopithecus Species: Differences within forests, among forests, and across species. In M. Glenn and M. Cords (Eds.). The guenons: Diversity and adaptation in African monkeys, pp. 319–344. Plenum Press, New York, New York.Google Scholar
  11. Chapman, C. A., Chapman, L.J., and Gillespie, T. R. 2002c. Scale issues in the study of primate foraging: Red colobus of Kibale National Park. American Journal of Physical Anthropology 117, 349–363.PubMedCrossRefGoogle Scholar
  12. Chapman, C. A., Chapman, L.J., Wrangham, R., Isabirye-Basuta, G., and Ben-David, K. 1997. Spatial and temporal variability in the structure of a tropical forest. African Journal of Ecology 35, 287–302.CrossRefGoogle Scholar
  13. Chapman, C. A., Chapman, L.J., Naughton-Treves, L., Lawes, M. J., and McDowell, L. R.. Predicting folivorous primate abundance: Validation of a nutrition model. Conservation Biology (Submitted).Google Scholar
  14. Chapman C. A. and Lambert, J. E. 2000. Habitat alteration and the conservation of African primates: A case study of Kibale National Park, Uganda. American Journal of Primatology 50, 169–186.PubMedCrossRefGoogle Scholar
  15. Chapman, C. A. and Peres, C. 2001. Primate conservation in the new millennium: The role of scientists. Evolutionary Anthropology 10, 16–33.CrossRefGoogle Scholar
  16. Chapman, L. J., Chapman, C. A., Brazeau, D., McGlaughlin, B., Jordan, M. 1999a. Papyrus swamps and faunal diversification: Geographical variation among populations of the African cyprinid Barbus neumayeri. Journal of Fish Biology 54, 310–327.Google Scholar
  17. Chapman C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K., and Zanne, A. E. 1999b. Fruit and flower phenology at two sites in Kibale National Park, Uganda. Journal of Tropical Ecology 15, 189–211.CrossRefGoogle Scholar
  18. Conklin, N. L. and Wrangham. R. W. 1994. The value of figs to hind-gut fermenting frugivores-A nutritional analysis. Biochemical Systematic Ecology 22, 137–151.Google Scholar
  19. Cords, M. 1987. Forest guenons and patas monkeys: Male-male competition in one male group. In D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker (Eds.). Primate societies, pp. 98–111. University of Chicago Press, Chicago, Illinois.Google Scholar
  20. Davies A. G. 1994. Colobine populations. In A. G. Davies and J. F. Oates (Eds.). Colobine monkeys: Their ecology, behaviour and evolution, pp. 285–310. Cambridge University Press, Cambridge, England.Google Scholar
  21. Fitter, A. H. and R. S. R. Fitter. 2002. Rapid changes in flowering time in British plants. Science 296, 1689–1692.PubMedCrossRefGoogle Scholar
  22. Foster, R. B. 1982. The seasonal rhythm of fruit fall on Barro Colorado Island. In E. G. Leigh, A. S. Rand Jr, and D. M. Windsor (Eds.). Ecology of a tropical forest, pp 151–172. Smithsonian Institution Press, Washington, DC.Google Scholar
  23. Gautier-Hion, A. 1988. The diet and dietary habits of forest guenons. In A. Gautier-Hion, F. Bourliere, and J-P. Gautier (Eds.). A primate radiation: Evolutionary biology of the African guenons, pp. 257–283. Cambridge University Press, Cambridge, England.Google Scholar
  24. Gautier-Hion, A., Gautier, J-P. and Maisels, F. 1993. Seed dispersal versus seed predation: An inter-site comparison of two related African monkeys. Vegetatio 107/108, 237–244.Google Scholar
  25. Gautier-Hion, A. and Michaloud, G. 1989. Are figs always keystone resources for tropical frugivorous vertebrates? A test in Gabon. Ecology 70, 1826–1833.Google Scholar
  26. Goodman, S. M., Ganzhorn, J. U., and Wilme, L. 1997. Observations at a Ficus tree in a Malagasy humid forest. Biotropica 29, 480–488.Google Scholar
  27. Harrison, R. D. 2000. Repercussions of El Nino: Drought causes extinction and the breakdown of mutualisms in Borneo. Proceedings of the Royal Society of London B. Biological Sciences 267, 911–915.Google Scholar
  28. Hughes, L. 2000. Biological consequences of global warming: Is the signal already apparent? Trends in Ecology and Evolution 15, 56–61.PubMedGoogle Scholar
  29. Janzen, D. H. 1979. How to be a fig. Annual Review of Ecology and Systematics 10, 13–51.CrossRefGoogle Scholar
  30. Kannan, R. and James, D. A. 1999. Fruiting phenology and the conservation of the Great Pied Hornbill (Bucerus bicornis) in the Western Ghats of southern India. Biotropica 31, 167–177.Google Scholar
  31. Kingston B. 1967. Working plan for Kibale and Itwara Central Forest Reserves. Uganda Forest Department, Entebbe, Uganda.Google Scholar
  32. Krebs, C. J. 1978. A review of the Chitty hypothesis of population regulation. Canadian Journal of Zoology 56, 2463–2480.Google Scholar
  33. Lambert, F. R. and Marshall, A. G. 1991. Keystone characteristics of bird-dispersed Ficus in a Malaysian lowland rain forest. Journal of Ecology 79, 793–809.Google Scholar
  34. Lambert, J. E., Chapman, C. A., Wrangham, R. W., Conklin-Brittain, N. L. The hardness of cercopithecine foods: Implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology (Submitted).Google Scholar
  35. Lee, P. C. 1987. Nutrition, fertility and maternal investment in primates. Journal of Zoology (London) 213, 409–422.CrossRefGoogle Scholar
  36. Leighton, M. and Leighton, D. R. 1983. Vertebrate response to fruiting seasonality within a Bornean rain forest. In S. L. Sutton, T. C. Whitmore, and A. L. Chadwick (Eds). Tropical rain forest ecology and management (pp. 584–596). Blackwell, Oxford.Google Scholar
  37. McKey, D. B. 1978. Soils, vegetation, and seed-eating by black colobus monkeys. In G. G. Montgomery (Ed.). The ecology of arboreal folivores (pp. 423–437). Smithsonian Institution Press, Washington, DC.Google Scholar
  38. Melnick, D. J. and Pearl, M. C. 1987. Cercopithecines in multimale groups: Genetic diversity and population structure. In D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker (Eds.). Primate societies (pp. 121–134). University of Chicago Press, Chicago.Google Scholar
  39. Milton, K. 1979. Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. American Naturalist 114, 363–378.CrossRefGoogle Scholar
  40. Milton, K. 1982. Dietary quality and demographic regulation in a howler monkey population. In E. G. Leigh, A. S, Rand, and D. M. Windsor (Eds.). The ecology of a tropical forest (pp. 273–289). Smithsonian Institution Press, Washington, DC.Google Scholar
  41. Milton, K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler (Alouatta palliata) population in Panama. Journal of Zoology (London) 239, 39–63.CrossRefGoogle Scholar
  42. Milton, K. 1998. Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparison with the Colobinae. International Journal of Primatology 19, 513–547.CrossRefGoogle Scholar
  43. Milton, K., van Soest, P. J., and Robertson, J. B. 1980. Digestive efficiencies of wild howler monkeys. Physiological Zoology 53, 402–409.Google Scholar
  44. Milton, D., D. M. Windsor, D. W. Morrison, and M. Estribi. 1982. Fruiting phonologies of two Neotropical Ficus species. Ecology 62: 752–762.Google Scholar
  45. National Research Council. 1992. Conserving biodiversity: A research agenda for development agencies. National Academy Press, Washington, D.C.Google Scholar
  46. Nicholson, A. J., 1933. The balance of animal populations. Journal of Animal Ecology 2, 132–178.Google Scholar
  47. 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
  48. O’Brien, T. G., Kinnaird, M. F., Darenfeld, N. L., Conklin-Brittain, R. W., and Silver, S. C. 1998. What’s so special about figs? Nature 392, 668.Google Scholar
  49. Osmaston, H.A. 1959. Working plan for the Kibale and Itwara Forests. Uganda Forest Department, Entebbe.Google Scholar
  50. Ottersen, G. 2001. Ecological effects of the North Atlantic Oscillation. Oecologia 128, 1–14.CrossRefGoogle Scholar
  51. Peres, C. A. 2000. Identifying keystone plant resources in tropical forests: The case of gums from Parkia pods. Journal of Tropical Ecology 16, 1–31.CrossRefGoogle Scholar
  52. Poulsen, J. R., Clark, C. J., and Smith, T. B. 2001. Seasonal variation in the feeding ecology of the greycheeked mangabey (Lophocebus albigena) in Cameroon. American Journal of Primatology 54, 91–105.PubMedCrossRefGoogle Scholar
  53. Poulsen, J. R., Clark, C. J., Connor, E. F., and Smith, T. B. 2002. Differential resource use by hornbills and primates: implications for seed dispersal. Ecology 83, 228–240.CrossRefGoogle Scholar
  54. Power, M. E., Tilman, D., Esters, J. A., Menges, B. A., Bond, W. J., Mills, L. S., Daily, G., Castilla, J. C., Lubchenco, J., and Paine, R. T. 1996. Challenges in the quest of keystone. Bioscience 46, 609–620.Google Scholar
  55. Skorupa J. P. 1988. The effect of selective timber harvesting on rain-forest primates in Kibale Forest, Uganda. Ph.D. Dissertation, University of California, Davis, California.Google Scholar
  56. Sokal R. R. and Rohlf. F. J. 1981. Biometry. Freeman, San Francisco, California.Google Scholar
  57. Struhsaker, T. T. 1975. The red colobus monkey. University of Chicago Press, Chicago, Illinois.Google Scholar
  58. Struhsaker, T. T. 1978. Interrelations of red colobus monkeys and rain-forest trees in the Kibale Forest, Uganda. In G.G. Montgomery (Ed.). The ecology of arboreal folivores. (pp. 397–422). Smithsonian Institute Press, Washington, DC.Google Scholar
  59. Struhsaker, T. T. 1997. Ecology of an African rain forest: Logging in Kibale and the conflict between conservation and exploitation. The University Press of Florida, Gainesville, Florida.Google Scholar
  60. Terborgh, J. 1986. Keystone plant resources in the tropical forest. In M.E. Soule (Ed.). Conservation biology: The science of scarcity and diversity (pp. 330–344). Sinauer, Sunderland.Google Scholar
  61. Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J.-M., Hoegh-Guldber, O., and Bairlein, F. 2002. Ecological responses to recent climate change. Nature 416, 389–395.PubMedCrossRefGoogle Scholar
  62. 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. Biological Journal of the Linnaean Society 34, 1–32.Google Scholar
  63. Wrangham, R. W., Roders, M. E., and Basuta, G. I. 1993. Ape food density in the ground layer in Kibale Forest, Uganda. African Journal of Ecology 31, 49–57.Google Scholar
  64. Wuethrich, B. 2000. How climate change alters rhythms of the wild. Science 287, 793–795.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Colin A. Chapman
    • 1
    • 2
  • Lauren J. Chapman
    • 1
    • 2
  • Amy E. Zanne
    • 1
    • 2
  • John R. Poulsen
    • 1
    • 2
  • Connie J. Clark
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of FloridaGainesvilleUSA
  2. 2.Wildlife Conservation SocietyBronxUSA

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