Nutritional costs of a plant secondary metabolite explain selective foraging by ruffed grouse

Ecology

Volumn 77, Issue 4, 1996, Pages 1103-1115

  Guglielmo, Christopher G ^a,b   Karasov, William H ^a   Jakubas, Walter J ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

^c SOUTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

Acidosis; Coniferyl benzoate; Detoxication; Digestion; Energetics; Foraging; Herbivory; Metabolic load; Plant secondary metabolite; Quaking aspen; Ruffed grouse

Indexed keywords

ASPEN; CONIFERYL BENZOATE; NUTRITION; RUFFED GROUSE; SECONDARY METABOLITE;

BONASA UMBELLUS; POPULUS; SALICACEAE;

EID: 0030389134     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.2307/2265579     Document Type: Article

References (86)

1. Ahmad, S., L. B. Brattsen, C. A. Mullin, and S. J. Yu. 1986. Enzymes involved in the metabolism of plant allelochemicals. Pages 73-151 in L. B. Brattsen and S. Ahmad, editors. Molecular aspects of insect-plant associations. Plenum Press, New York, New York, USA.
2. Andreev, A. V. 1988. Ecological energetics of palearctic tetraonidae in relation to chemical composition and digestibility of their winter diets. Canadian Journal of Zoology 66:1382-1388.
3. Appel, H. M., and M. M. Martin. 1992. Significance of metabolic load in the evolution of host specificity of Manduca sexta. Ecology 73:216-228.
4. Baldwin, B. C., D. Robinson, and R. T. Williams. 1960. The fate of benzoic acid in some domestic and other birds. Biochemical Journal 76:595-599.
5. 14C] phenol by native Australian rodents and marsupials. Australian Journal of Zoology 28: 511-520.
6. Belovsky, G. E., and O. J. Schmitz. 1991. Mammalian herbivore optimal foraging and the role of plant defenses. Pages 1-28 in R. T. Palo and C. T. Robbins, editors. Plant defenses against mammalian herbivory. CRC Press, Boca Raton, Florida, USA.
7. Berenbaum, M. R. 1986. Target site insensitivity in insect-plant interactions. Pages 257-272 in L. B. Brattsen and S. Ahmad, editors. Molecular aspects of insect-plant associations. Plenum Press, New York, New York, USA.
8. Berenbaum, M. R., and A. R. Zangerl. 1994. Costs of inducible defense: protein limitation, growth, and detoxification in parsnip webworms. Ecology 75:2311-2317.
9. Blumenkrantz, N., and G. Asboe-Hansen. 1973. A new method for the quantitative determination of uronic acids. Analytical Biochemistry 54:484-489.
10. Brattsen, L. B. 1979. Biochemical defense mechanisms in herbivores against plant allelochemicals. Pages 200-270 in G. A. Rosenthal and D. H. Janzen, editors. Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, New York, USA.
11. _. 1988. Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. Journal of Chemical Ecology 14:1919-1939.
12. Bryant, J. P., and P. J. Kuropat. 1980. Selection of winter forage by subarctic browsing vertebrates: the role of plant chemistry. Annual Review of Ecology and Systematics 11: 261-285.
13. Carlisle, E. J. F., S. M. Donnelly, S. Vasuvattakul, K. S. Kamel, S. Tobe, and M. L. Halperin. 1991. Glue sniffing and renal tubular acidosis: sticking to the facts. Journal of the American Society of Nephrology 1:1019-1027.
14. Cresswell, J. E., S. Z. Merrit, and M. M. Martin. 1992. The effect of dietary nicotine on the allocation of assimilated food to energy metabolism and growth in fourth-instar larvae of the southern armyworm, Spodoptera eridania (Lepidoptera: Noctuidae). Occologia 89:449-453.
15. Dash, J. A. 1988. Effect of dietary terpenes on glucuronic acid excretion and ascorbic acid turnover in the brushtail possum (Trichosurus vulpecula). Comparative Biochemistry and Physiology 898:221-226.
16. Dauterman, W. C. 1986. Insect metabolism: extramicrosomal. Pages 713-730 in G. A. Kerkut and L. I. Gilbert, editors. Comprehensive insect physiology, biochemistry and pharmacology. Volume 12. Pergamon Press, New York, New York, USA.
17. Dethier, V. G. 1954. Evolution of feeding preferences in phytophagous insects. Evolution 8:33-54.
18. Diamond, J., and K. Hammond. 1992. The matches, achieved by natural selection, between biological capacities and their natural loads. Experientia 48:551-557.
19. Doerr, P. D., L. B. Keith, D. H. Rusch, and C. A. Fischer. 1974. Characteristics of winter feeding aggregations of ruffed grouse in Alberta. Journal of Wildlife Management 38:601-615.
20. Dorney, R. S., and H. M. Mattison. 1956. Trapping techniques for ruffed grouse. Journal of Wildlife Management 20:47-50.
21. Eberhard, I. H., J. McNamara, R. J. Pearse, and I. A. South-well. 1975. Ingestion and excretion of Eucalyptus punctata D. C. and its essential oil by the Koala, Phascolarctos cinereus (Goldfuss). Australian Journal of Zoology 23: 169-179.
22. 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. Physiological Zoology 65:403-421.
23. Foley, W. J., and I. D. Hume. 1987. Digestion and metabolism of high-tannin Eucalyptus foliage by the brushtail possum (Trichosurus vulpecula) (Marsupiala: Phalangeridae). Journal of Comparative Physiology B 157:67-76.
24. Foley, W. J., S. McLean, and S. J. Cork. 1995. Consequences of biotransformation of plant secondary metabolites on acid-base metabolism in mammals - a final common pathway. Journal of Chemical Ecology 21:721-743.
25. Freeland, W. J., and D. H. Janzen. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. American Naturalist 108:269-289.
26. Glick, Z., and M. A. Joselyn. 1970a. Food intake depression and other metabolic effects of tannic acid in the rat. Journal of Nutrition 100:509-515.
27. Glick, Z., and M. A. Joselyn. 19706. Effect of tannic acid and related compounds on the absorption and utilization of proteins in the rat. Journal of Nutrition 100:516-520.
28. Guglielmo, C. G. 1993. Winter nutritional ecology of ruffed grouse: interactions between nutritional value and chemical defenses of browse. Thesis. University of Wisconsin, Madison, Wisconsin, USA.
29. Guglielmo, C. G., and W. H. Karasov. 1993. Endogenous mass and energy losses in Ruffed Grouse. Auk 110:386-390.
30. Guglielmo, C. G., and W. H. Karasov. 1995. Nutritional quality of winter browse for ruffed grouse. Journal of Wildlife Management 59:427-436.
31. Gullion, G. W. 1966. A viewpoint concerning the significance of studies of game bird food habits. Condor 68:372-376.
32. _. 1970. Factors influencing ruffed grouse populations. Transactions of the North American Wildlife and Natural Resources Conference 35:93-105.
33. _. 1981. Rejuvenation and maintenance of forest habitats for the American ruffed grouse. Pages 11-24 in Proceedings of the Second International Symposium on Grouse. World Pheasant Association, Edinburgh, Scotland, UK.
34. Halperin, M. L., and K. S. Kamel. 1990. Ammonium metabolism: emphasis on energy considerations. Mineral and Electrolyte Metabolism 16:277-282.
35. Hanssen, I. 1979a. Micromorphological studies of the small intestine and caeca of wild and captive willow grouse (Lagopus lagopus lagopus). Acta Veterinaria Scandinavica 20: 351-364.
36. _. 1979b. A comparison of the microbiological conditions in the small intestine and caeca of captive and wild willow grouse (Lagopus lagopus lagopus). Acta Veterinaria Scandinavica 20:365-371.
37. Hinks, N. T., and A. Bollinger. 1957. Glucuronuria in marsupials. Australian Journal of Science 19:228-229.
38. Huempfner, R. A. 1981. Winter arboreal feeding behavior of ruffed grouse in east-central Minnesota. Thesis. University of Minnesota, Minneapolis, Minnesota, USA.
39. Jakubas, W. J., and G. W. Gullion. 1990. Coniferyl benzoate in quaking aspen: a ruffed grouse feeding deterrent. Journal of Chemical Ecology 16:1077-1087.
40. Jakubas, W. J., and G. W. Gullion. 1991. Use of quaking aspen flower buds by Ruffed Grouse: its relationship to grouse densities and bud chemical composition. Condor 93: 473-485.
41. Jakubas, W. J., G. W. Gullion, and T. P. Clausen. 1989. Ruffed grouse feeding behavior and its relationship to secondary metabolites of quaking aspen flower buds. Journal of Chemical Ecology 15:1899-1917.
42. Jakubas, W. J., W. H. Karasov, and C. G. Guglielmo. 1993a. Coniferyl benzoate in quaking aspen: its effect on energy and nitrogen digestion and retention in ruffed grouse. Physiological Zoology 66:580-601.
43. Jakubas, W. J., W. H. Karasov, and C. G. Guglielmo. 1993b. Ruffed Grouse tolerance and biotransformation of the plant secondary metabolite coniferyl benzoate. Condor 95:625-640.
44. Jakubas, W. J., and J. R. Mason. 1991. Avian detection of coniferyl benzoate: role of the trigeminal sensory system in detecting a plant allelochemical. Journal of Chemical Ecology 17:2213-2221.
45. Jakubas, W. J., B. C. Wentworth, and W. H. Karasov. 1993c. Physiological and behavioral effects of coniferyl benzoate on avian reproduction. Journal of Chemical Ecology 19: 2353-2377.
46. Jayle, M. F., and J. R. Pasqualini. 1966. Implication of conjugation of endogenous compounds - steroids and thyroxine. Pages 507-543 in G. J. Dutton, editor. Glucuronic acid free and combined. Academic Press, New York, New York, USA.
47. Karasov, W. H. 1989. Nutritional bottleneck in a herbivore, the desert woodrat (Neotoma lepida). Physiological Zoology 62:1351-1382.
48. _. 1990. Digestion in birds: chemical and physiological determinants and ecological implications. Studies in Avian Biology 13:391-415.
49. Keith, L. B., J. R. Cary, O. J. Rongstad, and M. C. Brittingham. 1984. Demography and ecology of a declining snowshoe hare population. Wildlife Monographs 90:1-43.
50. Kurtz, I., P. D. Dass, and S. Cramer. 1990. The importance of renal ammonia metabolism to whole body acid-base balance: a reanalysis of the pathophysiology of renal tubular acidosis. Mineral and Electrolyte Metabolism 16: 331-340.
51. Lindroth, R. L., and G. O. Batzli. 1984. Plant phenolics as chemical defenses: effects of natural phenolics on survival and growth of prairie voles (Microtus ochrogaster). Journal of Chemical Ecology 10:229-244.
52. Long, S., and E. Skadhauge. 1983. Renal acid excretion in the domestic fowl. Journal of Experimental Biology 104: 51-58.
53. Maddrell, S. H. P., and B. O. C. Gardiner. 1976. Excretion of alkaloids by malpighian tubules of insects. Journal of Experimental Biology 64:267-281.
54. Marquardt, R. R. 1983. A simple spectrophotometric method for the direct determination of uric acid in avian excreta. Poultry Science 62:2106-2108.
55. McLean, S., W. J. Foley, N. W. Davies, S. Brandon, L. Duo, and A. J. Blackman. 1993. Metabolic fate of dietary terpenes from Eucalyptus radiata in common ringtail possum (Pseudocheirus peregrinus). Journal of Chemical Ecology 19:1625-1643.
56. National Forage Testing Association. 1993. Forage analysis procedures. National Forage Testing Association, Omaha, Nebraska, USA.
57. Neal, J. J. 1987. Metabolic costs of mixed-function oxidase induction in Heliothis zea. Entomologia Experimentalis et Applicata 43:175-179.
58. Okumura, J-I., and I. Tasaki. 1968. Urinary nitrogen excretion in fowls fed acid or alkali. Journal of Nutrition 95: 148-152.
59. Oliver, J., and E. Bourke. 1975. Adaptations in urea and ammonium excretion in metabolic acidosis in the rat: a reinterpretation. Clinical Science and Molecular Medicine 48:515-520.
60. Parsons, C. M., L. M. Potter, and B. A. Bliss. 1982. True metabolizable energy corrected to nitrogen equilibrium. Poultry Science 61:2241-2246.
61. Rausher, M. D. 1992. Natural selection and the evolution of plant-insect interactions. Pages 20-88 in B. D. Roitberg and M. B. Isman, editors. Insect chemical ecology: an evolutionary approach. Chapman and Hall, New York, New York, USA.
62. Redig, P. T. 1989. The avian caeca: obligate combustion chambers or facultative afterburners? - the conditioning influence of diet. Journal of Experimental Zoology Supplement 3:66-69.
63. Remington, T. E. 1990. Food selection and nutritional ecology of blue grouse during winter. Dissertation. University of Wisconsin, Madison, Wisconsin, USA.
64. Robbins, C. T. 1993. Wildlife feeding and nutrition. Second edition. Academic Press, New York, New York, USA.
65. Robbins, C. T., A. E. Hagerman, P. J. Austin, C. McArthur, and T. A. Hanley. 1991. Variation in mammalian physiological responses to a condensed tannin and its ecological implications. Journal of Mammalogy 72:480-486.
66. Robbins, C. T., T. A. Hanley, A. E. Hagerman, O. Hjeljord, D. L. Baker, C. C. Schwartz, and W. W. Mautz. 1987a. Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology 68:98-107.
67. Robbins, C. T., S. Mole, A. E. Hagerman, and T. A. Hanley. 1987e. Role of tannins in defending plants against ruminants: reduction in dry matter digestion? Ecology 68:1606-1615.
68. Robinson, D., J. N. Smith, and R. T. Williams. 1953. The apparent dissociation constants of some glucuronides, mercapturic acids, and related compounds. Journal of Biological Chemistry 55:151-155.
69. Scheline, R. R. 1978. Mammalian metabolism of plant xenobiotics. Academic Press, London, UK.
70. Schmid, R., and R. Lester. 1966. Implication of conjugation of endogenous compounds - bilirubin. Pages 493-506 in G. J. Dutton, editor. Glucuronic acid free and combined. Academic Press, New York, New York, USA.
71. Schoonhoven, L. M., and J. Meerman. 1978. Metabolic cost of changes in diet and neutralization of allelochemicals. Entomologia Experimentalis et Applicata 24:489-493.
72. Schulte, E. E., J. B. Peters, and P. R. Hodgson. 1987. Wisconsin procedure for soil testing, plant analysis, and feed and forage analysis. Soil fertility series, Number 6, Department of Soil Science, University of Wisconsin, College of Agriculture and Life Sciences, UW-Extension, Madison, Wisconsin, USA.
73. Scriber, J. M. 1978. Cyanogenic glycosides in Lotus corniculatus: their effect upon growth, energy budget, and nitrogen utilization of the southern armyworm, Spodoptera eridania. Oecologia 34:143-155.
74. _. 1981. Sequential diets, metabolic costs and growth of Spodoptera eridania (Lepidoptera: Noctuidae) feeding upon dill, lima bean and cabbage. Oecologia 51:175-180.
75. Servello, F. A., R. L. Kirkpatrick, and K. E. Webb, Jr. 1987. Predicting metabolizable energy in the diet of ruffed grouse. Journal of Wildlife Management 51:560-567.
76. Singleton, V. L., and J. A. Rossi, Jr. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticology 16:144-158.
77. Smith, R. L., and R. T. Williams. 1966. Implication of the conjugation of drugs and other exogenous compounds. Pages 457-492 in G. J. Dutton, editor. Glucuronic acid free and combined. Academic Press, New York, New York, USA.
78. Svoboda, F. J., and G. W. Gullion. 1972. Preferential use of aspen by ruffed grouse in northern Minnesota. Journal of Wildlife Management 36:1166-1180.
79. Sykes, A. H. 1971. Formation and composition of urine. Pages 223-278 in D. J. Bell and B. M. Freeman, editors. Physiology and biochemistry of the domestic fowl. Volume 1. Academic Press, London, UK.
80. Tallamy, D. W. 1986. Behavioral adaptations in insects to plant allelochemicals. Pages 273-300 in L. B. Brattsen and S. Ahmad, editors. Molecular aspects of insect-plant associations. Plenum Press, New York, New York, USA.
81. Temple, S. A. 1987. Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68:669-674.
82. Thompson, F. R. 1987. Ruffed grouse seasonal habitat use, survivorship, and winter energetics in Missouri. Dissertation. University of Missouri, Columbia, Missouri, USA.
83. Vanderschaegen, P. V. 1970. Food habits of ruffed grouse at the Cloquet Forest Research Center, Minnesota. Thesis. University of Minnesota, St. Paul, Minnesota, USA.
84. Wilkinson, L. 1990. SYSTAT: the system for statistics. SYSTAT, Evanston, Illinois, USA.
85. Whittaker, R. H., and P. P. Feeny. 1971. Allelochemics: chemical interactions between species. Science 171:757-770.
86. Zar, J. H. 1984. Biostatistical analysis. Second edition. Prentice-Hall, Englewood Cliffs, New Jersey, USA.