Abstract
The aim of this study was to investigate the dietary and physiological effects of condensed tannin ingestion on foregut fermenters, using Thallomys nigricauda, a folivorous rodent, as a model. We initially investigated the variability in physiological parameters, such as daily body mass (DMb), daily feed intake, daily fecal energy loss (FE), daily energy intake (DEI), daily urine pH, and daily urinary ammonia and urea concentrations, in response to different diets with low condensed tannin levels. This experiment was conducted to identify which physiological variables showed the least variation in the absence of tannin. In a second experiment, we investigated the response of the same dietary and physiological parameters to the effects of high dietary condensed tannin ingestion in T. nigricauda. We hypothesized that DMb, daily feed intake, FE, and DEI of T. nigricauda would be adversely affected by high dietary tannin content. We predicted that detoxification activity by T. nigricauda would increase at higher tannin levels. Ingestion of tannins affected the nutritional status of T. nigricauda, as shown by a decrease in body mass at high tannin levels. We also found that fewer ammonium ions were excreted in the urine by T. nigricauda, as would be expected if this were a means of regulating metabolic acidosis. The urine produced was more alkaline. This result indicates that T. nigricauda is not metabolizing these allelochemicals. Urea production was initially reduced, indicating conservation of bicarbonate ions that will neutralize blood acidity if there is detoxification. A diet choice experiment showed that tree rats avoid high tannin diets, even to the extent that they lose body mass on an alternative diet. This last-mentioned result is noteworthy because previous studies of the effects of tannins on herbivorous mammals have shown that there is physiological control rather than behavioral avoidance of the negative effects of tannin ingestion.
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References
Alexander, R. McN. 1993. The relative merits of foregut and hindgut fermentation. J. Zool. London 231:391–401.
Barry, T. N., Manley, T. R., and Duncan, S. J. 1986. The role of condensed tannins in the nutritional value of Lotus pedunculatus for sheep. 4. Sites of carbohydrate and protein digestion as influenced by dietary reactive tannin concentration. Br. J. Nutr. 55:123–137.
Chung-MacCoubrey, A. L., Hagerman, A. E., and Kirkpatrick, R. L. 1997. Effects of tannins on digestion and detoxification activity in Grey Squirrels (Sciurus carolinensis). Physiol. Zool. 70:270–277.
Cooper, S. M. and Owen-Smith, N. 1985. Condensed tannins deter feeding by browsing ruminants in a South African savanna. Oecologia 67:142–146.
Cork, S. J., Hume, I. D., and Faichney, G. J. 1999. Digestive strategies of nonruminant herbivores: the role of the hindgut, pp. 210–260. in H. H. Jung, and G. C. Fahey (Eds.). Nutritional Ecology of Herbivores: Proceedings of the Vth International Symposium on the Nutrition of Herbivores, American Society of Animal Science, Savoy, Illinois.
Crawley, M. J. 1983. Herbivory: The Dynamics of Animal-Plant Interactions. Blackwell, Oxford.
Dearing, M. D. 1997. Effects of Acomastylis rossii tannins on a mammalian herbivore, the North American Pika, Ochotona princeps. Oecologia 109:122–131.
Dearing, M. D., Mangione, A. M., and Karasov, W. H 2000. Diet breadth of mammalian herbivores: tests of the nutrient-constraints and detoxification-limitations hypotheses. Oecologia 123:397–405.
De Graaff, G. 1981. The Rodents of Southern Africa. Butterworth, Johannesburg.
Downs, C. T. and Perrin, M. R. 1990. The effect of diet on water and energy turnover rates of four Gerbillurus species in captivity. J. Zool. London 222:215–233.
Feeny, P. P. 1976. Plant apparency and chemical defence, pp. 1–40, in J. Wallace and R. L. Manse (Eds.). Biochemical Interactions Between Plants and Insects: Recent advances in phytochemistry, Vol. 10, Plenum Press, New York.
Foley, W. J. 1992. Nitrogen and energy retention and acid-base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals. Physiol. Zool. 65:403–421.
Foley, W. J. and Hume, I. D. 1987. Nitrogen requirements and urea metabolism in two arboreal marsupials, the greater glider (Petauroides volans) and the brushtail possum (Trichosurus vulpecula), fed Eucalyptus foliage. Physiol. Zool. 60:241–250.
Foley, W. J. and McArthur, C. 1994. The effects and costs of allelochemicals for mammalian herbivores: an ecological perspective, pp. 370–391, in D. J. Chivers and P. Langer (Eds.). The Digestive System in Mammals: Food, Form and Function. Cambridge University Press, Cambridge.
Foley, W. J., McLean, S., and Cork, S. J. 1995. Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals—a final common pathway? J. Chem. Ecol. 21:721–774.
Foley, W. J., Iason, G., and McArthur, C. 1999. Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores-how far have we come in 25 years? pp. 203–274, in H.-J. G. Jung and G. C. Fahey, Jr. (Eds.). Nutritional Ecology of Herbivores, Vth International Symposium on the Nutrition of Herbivores. American Society for Animal Science, Savoy Illinois.
Freeland, W. J. and Janzen, D. H. 1974. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat. 108:269–289.
Grodzinski, W. and Wunder, B. A. 1975. Ecological bioenergetics of small mammals. pp. 173–204, in F. B. Golley, K. Petrusiwicz, and L. Ryskowski (Eds.). Small Mammals: Their Productivity and Population Dynamics, Cambridge University Press, London.
Guglielmo, C. G., Karasov, W. H., and Jakubas, W. J. 1996. Nutritional costs of a plant secondary metabolite explain selective foraging by ruffed grouse. Ecology 77:1103–1115.
Hagerman, A. E. and Butler, L. G. 1989. Choosing appropriate methods and standards for assaying tannins. J. Chem. Ecol. 15:1795–1810.
Hagerman, A. E., Robbins, C. T., Weerasuriya, Y. Wilson, T. C., and McArthur, C. 1992. Tannin chemistry in relation to digestion. J. Range Manage. 45:57–62.
Hanley, T. A., Robbins, C. T., Hagerman, A. E., and McArthur, C. 1992. Predicting digestible protein and digestible dry matter in tannin-containing forages consumed by ruminants. Ecology 73:537–541.
Mole, S. and Waterman, P. G. 1985. Stimulatory effects of tannins and cholic acid on tryptic hydrolysis of proteins: ecological implications. J. Chem. Ecol. 11:1323–1332.
Mole, S., Rogler, J. C., Morell, J., and Butler, L. G. 1990. Herbivore growth reduction by tannins: use of the Waldbauer ratio techniques and manipulation of salivary protein production to elucidate mechanisms of actions. Biochem. Syst. Ecol. 18:183–197.
Owen-Smith, N. 1993. Woody plants, browsers and tannins in southern African savannas. S. Afr. J. Sci. 89:505–510.
Owen-Smith, N., Robbins, C. T., and Hagerman, A. E. 1993. Browse and browsers: interactions between woody plants and mammalian herbivores. Trends Ecol. Evol. 8:158–160.
Palo, R. T., Gowda, J., and Hogberg, P. 1993. Species height and root symbiosis, two factors influencing antiherbivore defense of woody plants in East African savanna. Oecologia 93:322–326.
Perrin, M. R. and Curtis, B. A. 1980. Comparative morphology of the digestive system of 19 species of southern African myomorph rodents in relation to diet and evolution. S. Afr. J. Zool. 15:22–33.
Perrin, M. R. and Maddock, A. H. 1983. Anatomical and nutritional adaptations in African rodents. S. Afr. J. Anim. Sci. 13:23–25.
Rhoades, D. F. 1979. Evolution of plant chemical defence against herbivores, pp. 4–55, in G. A. Rosenthal and D. H. Janzen (Eds.). Herbivores: Their Interaction with Secondary Plant Metabolites, Academic Press, New York.
Rhoades, D. F. and Cates, R. G. 1976. Toward a general theory of plant antiherbivore chemistry. pp. 168–213, in J. Wallace and R. L. Mansell (Eds.). Biochemical Interactions Between Plants and Insects: Recent Advances in Phytochemistry. Vol. 10. Plenum Press, New York.
Robbins, C. T. 1993. Wildlife Feeding and Nutrition, 2nd ed. Academic Press, New York.
Robbins, C. T., Hanley, T. A., Hagerman, A. E., Hjeljord, O., Baker, D. L., Schwartz, C. C., and Mautz, W. W. 1987. Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98–107.
Robbins, C. T., Hagerman, A. E., Austin, P. J., McArthur, C., and Hanley, T. A. 1991. Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J. Mammal. 72:480–486.
Rohner, C. and Ward, D. 1997. Chemical and mechanical defense against herbivory in two sympatric species of desert Acacia. J. Veg. Sci. 8:717–726.
Sipes, I. G. and Gandolfi, A. J. 1986. Biotransformation of toxicants pp. 64–98, in C. D. Klaasen, M. O. Amdur, and J. Doull (Eds.). Casarett and Doull's Toxicology: The Basic Science of Poisons. MaMillan, New York.
Skinner, J. D. and Smithers, R. H. N. 1990. The Mammals of the Southern African Subregion, 2nd ed. University of Pretoria, Pretoria.
Statsoft, Inc. 1996. Statistica for Windows. Tulsa, Oklahoma.
Thomas, D. W., Samson, C., and Bergeron, J. 1988. Metabolic costs associated with the ingestion of plant phenolics by Microtus pennsylvanicus. J. Mammal. 69:512–515.
Torres-Contreras, H. and Bozinovic, F. 1997. Food selection in an herbivorous rodent: balancing nutrition with thermoregulation. Ecology 78:2230–2237.
Ward, D. and Young, T. P. 2002. Effects of large mammalian herbivores and ant symbionts on condensed tannins of Acacia drepanolobium in Kenya. J. Chem. Ecol. 28:913–929.
Waterman, P. G. and Mole, S. 1994. Analysis of Phenolic Plant Metabolites. Blackwell, Oxford.
Wrangham, R. W. and Waterman, P. G. 1981. Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J. Anim. Ecol. 50:715–731.
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Downs, C.T., McDonald, P.M., Brown, K. et al. Effects of Acacia Condensed Tannins on Urinary Parameters, Body Mass, and Diet Choice of an Acacia Specialist Rodent, Thallomys Nigricauda . J Chem Ecol 29, 845–858 (2003). https://doi.org/10.1023/A:1022975531372
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DOI: https://doi.org/10.1023/A:1022975531372