Abstract
Gorilla adaptation has been debated in recent years given the wide variation among diets of gorillas in different habitats. Gorillas are the largest of living primates, have large colons and should be capable of processing tough foods. Preliminary captive studies have suggested that they may well have long average gut retention times relative to smaller hominoids, which should facilitate digestive efficiency in their wild counterparts. Indeed, wild gorillas consume large amounts of fibrous foods as staples or fall-back foods across their range, in response to habitat-related or seasonal changes in fruit availability. Fluctuations in diet might be matched by changes in digesta passage and digestibility, with possible selective retention of harder to digest items. We further studied digestive processes via chemical cobalt and chromium markers to track liquid and solids, as they passed through the guts of gorillas at the San Francisco Zoo (SFZ). In addition, we examined the effects of variation in captive diets on intake, digesta passage, digestion and behavior. The SFZ gorillas exhibited high digestibility coefficients, and gut passage was long relative to those of smaller-bodied hominoids. The results permit us to understand more fully the relationships of digestive processes to adaptation and dietary flexibility in the wild and to inform the development of dietary recommendations to improve the well-being of captive gorillas.
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REFERENCES
Allen, M. S., and Mertens, D. B. (1988). Evaluating constraints on fiber digestion by rumen microbes. J. Nutr. 118: 261-270.
AOAC. (1996). Official Methods of Analysis of AOAC International16th edn., Association of Offical Analytical Chemists International, Gaithersburg, MD.
Calvert, J. J. (1985). Food selection by western gorillas (Gorilla gorilla gorilla) in relation to food chemistry. Oecologia 65: 236-246.
Campbell, J. L., Eisemann, J. H., Glander, K. E., and Crissey, S. D. (1999). Intake, digestibility and passage of a commercially designed diet by two Propithecus species. Am. J. Primatol. 48: 237-246.
Caton, J. M. (1999). A preliminary report on the digestive strategy of the western lowland gorilla. Australas. Primatol. 13(4): 2-7.
Caton, J. M., Hume, I. D., Hill, D. M., and Harper, P. (1999). Digesta Retention in the gastro-intestinal tract of the orangutan (Pongo pygmaeus). Primates 4(4): 551-558.
Chivers, D. J., and Hladik, C. M. (1980). Morphology of the gastrointestinal tract in primates: Comparisons with other mammals in relation to diet. J. Morphol. 166: 337-86.
Chivers, D. J., and Langer, P. (eds.) (1994). The Digestive System in Mammals: Food Form and Function, Cambridge University Press, Cambridge.
Collet, J., Bourreau, E., Cooper, R. W., Tutin, C. E. G., and Fernandez, M. (1984). Experimental demonstration of cellulose digestion by Troglodytella gorillae, an intestinal ciliate of lowland gorillas. Int. J. Primatol. 5: 328.
Conklin-Brittain, N. L., Knott, C., and Wrangham, R. W. (2000). The feeding ecology of apes. In Proceedings of the Apes Challenges for the 21 Century st, Brookfield Zoo, Chicago, IL, p. 31.
Conklin, N. L., Wrangham, R. W., and Hunt, K. D. (1998). Dietary responses of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. Int. J. Primatol. 19: 971-998.
Crissey, S. D., Slifka, K. A., Barr, J. E., Bowen, P. E., Stacewicz-Sapuntzakis, M., Langman, C., Ward, A., Meerdink, G., and Ange, K. (2000). Blood nutrition parameters in captive apes at four zoos. In Proceedings of the Apes Challenges for the 21 Century st, Brookfield Zoo, Chicago, IL, p. 32.
Demment, M. W., and Van Soest, P. J. (1985). A nutritional explanation of body-size patterns of ruminant and nonruminant herbivores. Am. Nat. 125: 641-672.
Dierenfeld, E. S., Koontz, F. W., and Goldstein, R. S. (1992). Feed intake, digestion and passage of the Proboscis monkey (Nasalis lavartus) in captivity. Primates 33: 399-405.
Doran, D., and McNeilage, A. (1998). Gorilla ecology and behavior. Evol. Anthropol. 6: 120-131.
Doran, D. M., McNeilage, A., Greer, D., Bocian, C., Mehlman, P., and Shah, N. (2002). Western lowland gorilla diet and resource availability: New evidence, cross-site comparisons, and reflections on indirect sampling methods. Am. J. Primatol. 58: 91-116.
Edwards, M.S., and Ullrey, D.E. (1999a). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. i. ruffed lemurs (Varecia variegata variegata and V.v. rubra). Zoo Biol. 18(6): p. 529-536.
Edwards, M. S., and Ullrey, D. E. (1999b). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. ii. hindgut-and foregut-fermenting folivores. Zoo Biol. 18: 537-549.
Ellis, W. C., Matis, J. H., and Lascano, C. (1979). Quantifying ruminal turnover. Fed. Proc. 38: 2702-2706.
Goldsmith, M. L. (1999). Gorilla socioecology. In Dolhinow, P., and Fuentes, A. (eds.), The Nonhuman Primates, Mayfield Publishing, Mountain View, CA, p. 58-63.
Goldsmith, M. L. (2003). Comparative behavioral ecology of a lowland and highland gorilla population: Where do Bwindi gorillas fit? In Taylor, A. B., and Goldsmith, M. L. (eds.), Gorilla Biology: A Multidisciplinary Perspective, Cambridge University Press, Cambridge, p. 358-384.
Gould, E., and Bres, M. (1986). Regurgitation and reingestion in captive gorillas: Description and intervention. Zoo Biol. 5: 241-250.
Gross, J., Want, Z., and Wunder, B. A. (1986). Adaptation to food quality and energy needs: Changes in gut morphology and capacity of Microtus orchrogaster. J. Mammal. 66: 661-669.
Hume, I. D. (1989). Optimal digestive strategies in mammalian herbivores. Physiol. Zool. 62: 1145-1163.
Kay, R. F., and Davies, A. G. (1994). Digestive physiology. In Davies, A. G., and Oates, J. F. (eds.), Colobine Monkeys, Their Ecology Behaviour and Evolution, Cambridge University Press, Cambridge, p. 229-250.
Kirkpatrick, R. C., Zou, R. J., Dierenfeld, E. S., and Zhou, H. W. (2001). Digestion of selected foods by Yunnan snub-nosed monkey Rhinopithecus bieti (Colobinae) Am. J. Phys. Anthropol. 114: 156-162.
Lambert, J. (1999). Primate digestion: Interactions among anatomy physiology, and feeding ecology. Evol. Anthropol. 7(1): 8-20.
Lambert, J. E. (2002). Digestive retention times in forest guenons with reference to chimpanzees. Int. J. Primatol. 23(6): 1169-1185.
Lee, W. B., and Houston, D. C. (1993). The effects of diet quality on gut anatomy in British voles. J. Comp. Physiol. (B) 163: 337-339.
Lukas, K. E. (1999). A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas (G.g.gorilla). Appl. Anim. Behav. Sci. 63: 237-249.
Lukas, K. E. (2000). An inter-institutional study of individual and nutritional factors associated with regurgitation and reingestion in captive gorillas. In Proceedings of the Apes Challenges for the 21st Century, Brookfield Zoo, Chicago, IL, p. 47.
Lukas, K. E., Hamor, G., Bloomsmith, M. A., Horton C. L., and Maple, T. L. (1999). Removing milk from captive gorilla diets: The impact on regurgitation and reingestion (R/R) and other behaviors. Zoo Biol. 18: 515-528.
Maisels, F. (1993). Gut passage rate in guenons and mangabeys: Another indicator of a flexible dietary niche? Folia Primatol. 61: 35-37.
Martin, R. D., Chivers, D. J., Maclarnon, A. M., and Hladik, C. M. (1985). Gastrointestinal allometry in primates and other mammals, In Jungers, W. L. (ed.), Size and Scaling in Nonhuman Primates, Plenum Press, New York, p. 61-89.
Milton, K. (1984). The role of food-processing factors in primate food choice. In Rodman, P. S., and Cant, J. G. H. (eds.), Adaptations for Foraging in Nonhuman Primates, Columbia University Press, New York, p. 249-279.
Milton, K. (1998). Physiological ecology of howlers (Alouatta): Energetic and digestive considerations and comparisons with the Colobinae. Int. J. Primatol. 19: 513-548.
Milton, K. (1999). A hypothesis to explain the role of meat-eating in human evolution. Evol. Anthropol. 1999. 8(1): 11-21.
Milton, K., and Demment, M. W. (1988). Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. J. Nutr. 118: 1082-1088.
National Research Council (NRC). (2003). Nutrient Requirements of Nonhuman Primates., 2nd rev. edn., Committee on Animal Nutrition, The National Academies Press, Washington, DC.
Norconk, M. A., Oftedal, O. T., Power, M. L., Jakubasz, M., and Savage, A. (2002). Digesta passage and fiber digestibility in captive White-Faced Sakis (Pithecia pithecia). Am. J. Primatol. 58: 23-34.
Parra, R. (1978). Comparison of foregut and hindgut fermentation in herbivores. In Montgomery, G. G. (ed.), The Ecology of Arboreal Folivores, Smithsonian Press, Washington, DC, p. 205-229.
Popovich, D. G., Jenkins, D. J. A., Kendall, C. W. C., Dierenfeld, E. S., Carroll, R. W., Tariq, N., and Vidgen, E. (1997). The western lowland gorilla diet has implications for the health of humans and other hominoids. J. Nutr. 127: 2000-2006.
Remis, M. J. (1997). Gorillas as seasonal frugivores: Use of variable resources. Am. J. Primatol. 43: 87-109.
Remis, M. J. (2000). Initial studies on the contributions of body size and gastrointestinal passage times to dietary flexibility among gorillas (Gorilla gorilla gorilla). Am. J. Phys. Anthropol. 112: 171-180.
Remis, M. J. (2002). Food preferences of captive gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). Int. J. Primatol. 23: 231-249.
Remis, M. J. (2003). Are gorillas vacuum cleaners of the forest floor? The roles of body size, habitat and food preferences on gorilla dietary flexibility and nutrition. In Taylor, A. B., and Goldsmith, M. L. (eds.), Gorilla Biology: A Multidisciplinary Perspective, Cambridge University Press, Cambridge, p. 395-404.
Remis, M. J., Dierenfeld, E. S., and Mowry, C. B. (2001). Nutritional aspects of the diet of western lowland gorillas (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic during fruit scarcity. Int. J. Primatol. 40: 106-136.
Reumpler, U. (1992). The Cologne Zoo diet for lowland gorillas to eliminate regurgitation and reingestion. Int. Zoo Yrbk 31: 225-229.
Robbins, M., and McNeilage, A. (2002). Home range and frugivory patterns of mountain gorillas in Bwindi Impenetrable National Park, Uganda. Int. J. Primatol. 24(3): 467-491.
Rogers, M. E, Abernathy, K., Bermejo, M., Chiopoletta, C., Doran, D. M., McFarland, K., Nishihara, T., Remis, M. J., and Tutin, C. (in press). Western gorilla diet: A synthesis from six sites. Am. J. Primatol.
Rogers, M. E., Williamson, E. A., Tutin, C. E. G., and Fernandez, M. (1990). Gorilla diet in the Lope Reserve, Gabon: A nutritional analysis. Oecologia 84: 326-339.
Schmidt, D. A., Kerley, M. S., Dempsey, J. L., and Porton, I. J. (2000). Fiber in ape diets: A Review. In Proceedings of the Apes Challenges for the 21 Century st, Brookfield Zoo, Chicago, Il., p. 59.
Stevens, C. E., Hume, I. D. (1995). Comparative Physiology of the Vertebrate Digestive System (2nd edn.), Cambridge University Press, Cambridge.
Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A., and McGrew, W. C. (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lope Reserve, Gabon. Philos. Trans. R. Soc. Lon. B 334: 179-186.
Tutin, C. E. G., Ham, R. M., White, L. J. T., and Harrison, M. J. S. (1997). The primate community of the Lope Reserve, Gabon: Diets, responses to fruit scarcity and effects on biomass. Am. J. Primatol. 42: 1-24.
Uden, P., Colucci P. E., and van Soest P. J. (1980). Investigation of chromium, cerium, and cobalt as markers in digesta: Rate of passage studies. J. Sci. Food Agric. 31: 625-632.
U.S. Department of Agriculture, Agricultural Research Service. (19761992). Composition of Foods. Raw, Processed and Prepared, Human Nutrition Information Service, Government Printing Office, Washington, DC.
van Soest, P. J. (1994). Nutritional Ecology of the Ruminant, 2nd edn., Cornell University Press, Ithaca, New York.
van Soest, P. J., Robertson, J. B., and Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74: 3583-3597.
Ward, A., and Lintzenich, B. (2000). Weight management strategies in Captive Apes. In: Proceedings of the Apes Challenges for the 21 Century st, Brookfield Zoo, Chicago, IL, p. 68.
Warner, A. C. (1981). Rate of passage of digesta through the gut of mammals and birds. Nutr. Abstr. Rev. Ser. B 51: 789-820.
Watts, D. P. (1996). Comparative socioecology of gorillas. In McGrew, W. C., Marchant, L. F., and Nishida, T. (eds.), Great Ape Societies, Cambridge University Press, Cambridge, p. 16-28.
WCS. (2001). Zootrition Software, Wildlife Conservation Society, New York.
Wrangham, R. W., Conklin-Brittain, N. L., and Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance 1. antifeedants. Int. J. Primatol 19(6): 949-970.
Wrick, K. L., Robertson, J. B., Van Soest, P. J., Lewis, B. A., Rivers, J. M., Roe, D. A., and Hackler, L. R. (1983). The influence of dietary fiber source on human intestinal transit and stool output. J. Nutr. 113: 1464-1479.
Yamagiwa, J., Basabose, K., Kaleme, K., and Yumoto, T. (2003). Within-group feeding competition and socioecological factors influencing social organization of gorillas in the Kahuzi-Biega National Park, Democratic Republic of Congo. In Taylor, A. B., and Goldsmith, M. L. (eds.), Gorilla Biology: A Multidisciplinary Perspective, Cambridge University Press, Cambridge, p. 328-357.
Yamagiwa, J., Maruhashi, T., Yumoto, T., and Mwanza, N. (1996). Dietary and ranging overlap in sympatric gorillas and chimpanzees in Kahuzi-Biega National Park, Zaire. In McGrew, W. C., Marchant, L., and Nishida, T. (eds.), Great Ape Societies, Cambridge University Press, Cambridge, p. 82-98.
Yamagiwa, J., Mwanza, N., Yumoto, T., and Maruhashi, T. (1994). Seasonal changes in the composition of the diet of eastern lowland gorillas. Primates 35: 1-14.
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Remis, M.J., Dierenfeld, E.S. Digesta Passage, Digestibility and Behavior in Captive Gorillas Under Two Dietary Regimens. International Journal of Primatology 25, 825–845 (2004). https://doi.org/10.1023/B:IJOP.0000029124.04610.c7
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DOI: https://doi.org/10.1023/B:IJOP.0000029124.04610.c7