Abstract
Ascertaining the full range of dietary constituents of a primate population allows the identification of habitats with important food resources and can assist efforts to conserve primates. For unhabituated populations, we can acquire otherwise unobtainable dietary information from macroscopic inspection of fecal samples. This method has made a significant contribution to understanding food intake in various primate species. Increasing knowledge of the omnivorous diet of our closest living relatives, the common chimpanzee (Pan troglodytes) and the bonobo (P. paniscus), which range and forage in various habitats to meet daily nutrient requirements, provides more scope to assess human omnivory and its evolution from our last common ancestor. However, macroscopic inspection may lead to bias toward undigested and therefore identifiable food items, e.g., fruit seeds, vs. pulverized components, e.g., leaves, that are unidentifiable at this level. This study seeks to validate findings from macroscopic inspection by comparing species identified in fecal samples from select individuals vs. data from direct observations of their feeding. We collected data from 10 adult chimpanzees of the Kanyawara community in Kibale National Park. We identified 86% of species from which fruit had been eaten vs. only 21% from which leaves had been eaten in fecal samples analyzed. This study provides empirical support for previous assumptions and confirms the limitations of macroscopic inspection of feces for identifying the nonfrugivorous dietary elements to species level. However, valuable insights into seasonality of diet can be gleaned from macroscopic inspection. Also, if we combine data on species identified in feces with direct observation of food intake, we can establish when food items were eaten, which enables estimations of gut passage rates for wild populations. Finally, analyzing fecal samples collected from various group members can provide insight into the dietary repertoire at the individual level.
Similar content being viewed by others
References
Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology, 58, 1–21.
Bogart, S. L., & Pruetz, J. D. (2011). Insectivory of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. American Journal of Physical Anthropology, 145, 11–20.
Chapman, C. A., White, F. J., & Wrangham, R. W. (2001). Party size in chimpanzees and bonobos: A re-evaluation of theory based on two similarly forested sites. In R. W. Wrangham, W. C. McGrew, F. B. M. de Waal, & P. G. Heltne (Eds.), Chimpanzee cultures (pp. 41–57). Cambridge: Harvard University Press.
Deblauwe, I. (2008). Comparison of insectivory by sympatric western lowland gorillas and chimpanzees in lowland rainforest, southeast Cameroon. Ph.D. thesis, University of Antwerp, Belgium.
Deblauwe, I., & Janssens, G. J. P. (2008). New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: The role of nutritional value. American Journal of Physical Anthropology, 135, 42–55.
Doran, D., McNeilage, A., Greer, D., Bocian, C., Mehlman, P., & Shah, N. (2002). Western lowland gorilla diet and resource availability: New evidence, cross-site comparisons, and reflections on indirect sampling methods. American Journal of Primatology, 58, 91–116.
Ghiglieri, M. P. (1984). The chimpanzees of Kibale Forest: A field study of ecology and social structure. New York: Columbia University Press.
Gross-Camp, N. D., Masozera, M., & Kaplin, B. A. (2009). Chimpanzee seed dispersal quantity in a tropical montane forest of Rwanda. American Journal of Primatology, 71, 1–11.
Hanya, G., Noma, N., & Agetsuma, N. (2003). Altitudinal and seasonal variations in the diet of Japanese macaques in Yakushima. Primates, 44, 51–59.
Head, J. S., Boesch, C., Makaga, L., & Robbins, M. M. (2011). Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: Dietary composition, seasonality and intersite comparisons. International Journal of Primatology, 32, 755–775.
Hohmann, G., & Fruth, B. (2008). New records on prey capture and meat eating by bonobos at LuiKotale, Salonga National Park, Democratic Republic of Congo. Folia Primatologica, 79, 103–110.
Huffman, M. A., & Wrangham, R. W. (1994). The diversity of medicinal plant use by chimpanzees in the wild. In R. W. Wrangham, W. C. McGrew, F. B. M. de Waal, & P. G. Heltne (Eds.), Chimpanzee cultures (pp. 129–148). Cambridge: Harvard University Press.
Julliot, C., & Sabatier, D. (1993). Diet of the red howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology, 14, 527–550.
Kibale Chimpanzee Project (2009). Resource document. Kibale Chimpanzee project. Retrieved from http://kibalechimpanzees.wordpress.com/. (Accessed September 19, 2012).
Lambert, J. E. (2002). Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). International Journal of Primatology, 23, 1169–1185.
Malenky, R. K., Kuroda, S., Vineburg, E. O., & Wrangham, R. W. (1994). The significance of terrestrial herbaceous foods for bonobos, chimpanzees and gorillas. In R. W. Wrangham, W. C. McGrew, F. B. M. de Waal, & P. G. Heltne (Eds.), Chimpanzee cultures (pp. 59–76). Cambridge: Harvard University Press.
Martin, P., & Bateson, P. (2007). Measuring behaviour: An introductory guide. Cambridge: Cambridge University Press.
McGrew, W. C. (1983). Animal foods in the diets of wild chimpanzees (Pan troglodytes): Why cross-cultural variation? Journal of Ethology, 1, 46–61.
McGrew, W. C., Baldwin, P. J., & Tutin, C. E. G. (1988). Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. American Journal of Primatology, 16, 213–226.
McGrew, W. C., Marchant, L. F., & Phillips, C. A. (2009). Standardised protocol for faecal analysis. Primates, 50, 363–366.
Milton, K., & Demment, M. W. (1988). Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. Journal of Nutrition, 118, 1082–1088.
Moreno-Black, G. (1978). The use of scat samples in primate diet analysis. Primates, 19, 215–221.
Morgan, D., & Sanz, C. (2006). Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goualougo Triangle, Republic of Congo. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 97–122). Cambridge: Cambridge University Press.
O’Driscoll Worman, C., & Chapman, C. (2004). Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology, 21, 689–697.
Ortmann, S., Bradley, B., Stolter, C., & Ganzhorn, A. (2006). Estimating the quality and composition of wild animal diets – a critical survey of methods. In M. M. Robbins & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioural aspects (pp. 397–419). Cambridge: Cambridge University Press.
Osborne, T. Z., Chapman, L. J., Chapman, C. A., Crisman, T. L., Prenger, J. P., Nyguen, S., & Stecker, E. (2001). Invertebrate community structure and oxygen availability in an intermittent stream/wetland/river system of the Ugandan highlands. Verhandlungen des Internationalen Verein Limnologie, 27, 3599–3603.
Phillips, C. A. (2011). Chimpanzee diet: Analyses at macroscopic, microscopic and molecular level. Ph.D. thesis, University of Cambridge, Cambridge.
Potts, K. B., Watts, D. P., & Wrangham, R. W. (2011). Comparative feeding ecology of two communities of chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. International Journal of Primatology, 32, 669–690.
Poulsen, J. P., Clark, C. J., & Smith, T. B. (2001). Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology, 17, 787–808.
Pruetz, J. D. (2006). Feeding ecology of savannah chimpanzees. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates: Ecological, physical and behavioural aspects (pp. 161–179). Cambridge: Cambridge University Press.
Rogers, M. E., Maisels, F., Williamson, E. A., Fernandez, M., & Turin, C. E. G. (1990). Gorilla diet in the Lopé Reserve, Gabon: A nutritional analysis. Oecologia, 84, 326–339.
Schöning, C., Ellis, D., Fowler, A., & Sommer, V. (2007). Army ant prey availability and consumption by chimpanzees (Pan troglodytes vellerosus) at Gashaka (Nigeria). Journal of Zoology, 271, 125–133.
Sekercioglu, C. H. (2002). Effects of forestry practices on vegetation structure and bird community of Kibale National Park, Uganda. Biological Conservation, 107, 229–240.
Stanford, C. B., & Nkurunungi, J. B. (2003). Behavioral ecology of sympatric chimpanzees and gorillas in Bwindi Impenetrable National Park, Uganda: Diet. International Journal of Primatology, 24, 901–919.
Surbeck, M., Fowler, A., Deimel, C., & Hohmann, G. (2009). Evidence for the consumption of arboreal, diurnal primates by bonobos (Pan paniscus). American Journal of Primatology, 71, 171–174.
Tutin, C. E. G., & Fernandez, M. (1992). Insect-eating by sympatric lowland gorillas (Gorilla g. gorilla) and chimpanzees (Pan t. troglodytes) in the Lopé Reserve, Gabon. American Journal of Primatology, 28, 29–40.
Tutin, C. E. G., & Fernandez, M. (1993a). Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé Reserve, Gabon. American Journal of Primatology, 30, 195–212.
Tutin, C. E. G., & Fernandez, M. (1993b). Faecal analysis as a method of describing diets of apes: Examples from sympatric gorillas and chimpanzees at Lopé, Gabon. Tropics, 2, 189–197.
Tutin, C. E. G., Fernandez, M., Rogers, E., Williamson, A., & McGrew, W. C. (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lopé Reserve, Gabon. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 334, 179–186.
Watts, D. P., Potts, K. P., Lwanga, J. S., & Mitani, J. C. (2012). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity. American Journal of Primatology, 74, 114–129.
Williamson, E. A., Tutin, C. E. G., Rogers, M. E., & Fernandez, M. (1990). Composition of the diet of lowland gorillas at Lopé in Gabon. American Journal of Primatology, 21, 265–277.
Wrangham, R. W. (1995). Relationship of chimpanzee leaf-swallowing to a tapeworm infection. American Journal of Primatology, 37, 297–303.
Wrangham, R. W., Conklin, N. L., Chapman, C. A., & Hunt, K. D. (1991). The significance of fibrous foods for Kibale Forest chimpanzees. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 334, 171–178.
Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.
Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., & Isabiirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. C. McGrew, L. P. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 45–57). Cambridge: Cambridge University Press.
Acknowledgments
We thank Murray Edwards College of Cambridge, Board of Graduate Studies of University of Cambridge, Ridgeway-Venn Travel Fund, and Sir Richard Stapely Education Trust (C. A. Phillips) and Leverhulme Trust and European Research Council (W. C. McGrew) for funding; Uganda Wildlife Authority, Uganda Council for Science and Technology, and Makarere University Biological Field Station for permission to live and work in Kibale National Park; Richard Wrangham and Martin Muller of the Kibale Chimpanzee Project for generous logistical support; all staff of the Kibale Chimpanzee Project for help in data collection and for identification of plant samples; Chris Rolfe and Steve Boreham, University of Cambridge, for supplying the Endecott soil test sieves for analyses. We thank NRF and DST (South Africa) for logistical support. We thank two anonymous reviewers for helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Phillips, C.A., McGrew, W.C. Identifying Species in Chimpanzee (Pan troglodytes) Feces: A Methodological Lost Cause?. Int J Primatol 34, 792–807 (2013). https://doi.org/10.1007/s10764-013-9696-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-013-9696-6