Interactions between woody plants and browsing mammals mediated by secondary metabolites

Annual Review of Ecology and Systematics

Volumn 22, Issue 1, 1991, Pages 431-446

  Bryant, John P ^a   Provenza, Frederick D ^b   Pastor, John ^c   Reichardt, Paul B ^a   Clausen, Thomas P ^a   Du Toit, Johan T ^d  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b UTAH STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MINNESOTA DULUTH   (United States)

^d UNIVERSITY OF ZIMBABWE   (Zimbabwe)

Author keywords

Chemical defense; Community; Ecosystem; Learning; Mammals; Secondary metabolite; Toxicity

Indexed keywords

ANTIHERBIVORE DEFENCE; BROWSING; MAMMAL; SECONDARY METABOLITE; WOODY PLANT;

EID: 0026396881     PISSN: 00664162     EISSN: None     Source Type: Journal    
DOI: 10.1146/annurev.es.22.110191.002243     Document Type: Article

References (124)

1. Agawal, I., Mathela, C. S. 1979. Study of antifungal activity of some terpenoids. Indian Drugs Pharm. Ind. 14:19-21
2. Bar-Zeev, M. 1980. Studies of repellents against Panstrogylus megistus (Hemiptera: Reduviidae) in Brazil. J. Med. Entomol. 17:70-74
3. Batzli, G. O., Jung, H. G. 1980. Nutritional ecology of microtine rodents: Resource utilization near Atkasook, Alaska, Arctic Alpine Rex. 12:483-99
4. Bergerud, A. T., Manuel, F. 1968. Moose damage to balsam fir-white birch forests in central Newfoundland. J. Wildl. Manage. 32:729-46
5. Beraays, E. A., Cooper-Driver, G., Bilgener, M. 1989. Herbivores and plant tannins. Adv. Ecol. Res. 19:263-302
6. Boyd, R., Richardson, P. J. 1985. Culture and the Evolutionary Process. Chicago: Univ. Chicago Press
7. Brandner, T. A., Peterson, R. O., Risenhoover, K. L. 1990. Balsam fir on Isle Royale: effects of moose herbivory and population density. Ecology 71: 155-64
8. Bryant, J. P., Chapin, F. S. III. 1986. Browsing-woody plant interactions during boreal forest plant succession. In Forest Ecosystems in the Alaskan Taiga, ed. K. Van Cleve, F. S. Chapin, III, P. W. Flanagan, L. A. Viereck, and C. T. Dyrness, pp. 313-25. New York: Springer-Verlag
9. Bryant, J. P., Chapin, F. S. III, Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-68
10. Bryant, J. P., Fox, J. F. 1991. Effects of browsing by mammals on the species composition of woody vegetation: importance of chemical defenses to functional responses by browsing mammals. Manuscript
11. Bryant, J. P., Kuropat, P. J. 1980. Selection of winter forage by subarctic browsing vertebrates: The role of plant chemistry, Annu. Rev. Ecol. Syst. 11:261-85
12. Bryant, J. P., Kuropat, P. J., Reichardt, P. B., Clausen, T. P. 1991. Controls over allocation of resources by woody plants to chemical antiherbivore defense. In Plant Defenses Against Mammalian Herbivory, ed. T. Palo, C. Robbins. Boca Raton: CRC. In press
13. 12a. Bryant, J. P., Reichardt, P. B., Clausen, T. P., Provenza, F. D., Kuropat, P. J. 1991. Woody plant-mammal interactions. In Herbivores: Their Interaction with Plant Metabolites, vol. 2, ed. G. A. Rosenthal and M. R. Berenbaum. New York: Academic. In press
14. Burritt, E. A., Provenza, F. D. 1989. Food aversion learning: Ability of lambs to distinguish safe from harmful foods. J. Anim. Sci. 67:1732-39
15. Burritt, E. A., Provenza, F. D. 1990. Food aversion learning in sheep: persistence of conditioned taste aversions to palatable shrubs (Cercocarpus montanus and Amelanchier alnifolia). J. Anim. Sci. 68:1003-7
16. Burritt, E. A., Provenza, F. D. 1991. Ability of lambs to learn with a delay between food ingestion and consequences given meals containing novel and familiar foods. Appl. Anim. Behav. Sic. In press
17. Butler, L. G., Rogler, J. C., Mehansho, H., Carlson, D. M. 1986. Dietary effects of tannins. In Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological and Structure-Activity Relationships, ed. V. Cody, E. Middleton, J. B. Harbome, pp. 141-157. New York: Liss
18. Chapin, F. S. III. 1980. The mineral nutrition of wild plants, Annu. Rev. Ecol. Syst. 11:233-60
19. Chapin, F. S. III, Vitousek, P. M., Van Cleve, K. 1986. The nature of nutrient limitation in plant communities. Am. Nat. 127:48-58
20. Clausen, T. P., Bryant, J. P., Reichardt, P. B. 1986. Defense of winter-dormant green alder against snowshoe hares. J. Chem. Ecol. 12:2117-31
21. Clausen, T. P., Provensa, F. D., Burritt, E. A., Bryant, J. P., Reichardt, P. B. 1990. Ecological implications of condensed tannin structure: a case study. J. Chem. Ecol. 16:2381-92
22. Clausen, T. P., Reichardt, P. B., Bryant, I. P., Werner, R. A., Post, K. 1989. Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J. Chem. Ecol. 15:2335-45
23. Coley, P. D., Bryant, J. P., Chapin, F. S. III. 1985. Resource availability and plant antiherbivore defense. Science 230:895-99
24. Conn, E. C. 1979. Cyanide and cyanogenic glycosides. In Herbivores: Their Interaction With Secondary Plant Metabolites, ed. G. A. Rosenthal, D. H. Janzen, pp. 387-412. New York: Academic. 718 pp.
25. Cox, P. H., Spanjers, F. 1970. Preparation of sterile implants by compression. Pharm. Weekbl. 105:681-84
26. Dassler, H. G., Dube, G. 1957. The action of terpene oxides on different classes of insects. Anz. Schadlingskunde 30:86-8
27. Day, T. A., Detling, J. K. 1990. Grassland patch dynamics and herbivore grazing preferences following urine deposition. Ecology 71:180-88
28. Distel, R. A., Provenza, F. D. 1990. Experience early in life affects voluntary intake of blackbrush by goats. J. Chem. Ecol. 17:431-50
29. Divers, T. J., Crowell, W. A., Duncan, J. R., Whitlock, R. H. 1982. Acute renal disorders in cattle: a retrospective study of 22 cases. J. Am. Vet. Met. Assoc. 181:694-99
30. Dull, G. G., Fairley, J. L. Jr., Gottshall, R. V., Lucus, E. H. 1957. Antibacterial substances in seed plants active against tubercle bacilli. IV. The antibacterial sesquiterpenes of Populus tacamahaca. Antibiotics Annu. 682:6
31. du Toit, J. T. 1991. Introduction of artificial waterpoints: potential impacts on nutrient cycling. In Management of the Hwange Ecosystem, ed. M. Jones, R. Martin. Harare, Zimbabwe: USAID/ Zimbabwe Dept. Natl. Parks Wildl. Manage.
32. du Toit, J. T., Provenza, F. D., Nastis, A. S. 1991. Conditioned food aversions: How sick must a ruminant get before it detects toxicity in food? Appl. Amm. Behav. Sci. 30:35-46
33. Feeny, P. 1976. Plant apparency and chemical defense. In Recent Advances in Phytochemistry, Vol. 10. Biochemical Interactions Between Plants and Insects, ed. J. W. Wallace, R. L. Mansell, 10:1-40. New York: Plenum. 425 pp.
34. Flanagan, P. W.. Van Cleve, K. 1983. Nutrient cycling in relation to decomposition of organic matter quality in taiga ecosystems. Can. J. For. Res. 13:795-817
35. Freeland, W. J., Janzen, D. H. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108:269-89
36. Frykholm, K. O. 1945. Bacteriological studies of pinosylvin, its monomethyl ether and dimethyl ethers, and toxicological studies of pinosylvin. Nature 155:454-55
37. Garcia, J. 1989. Food for Tolman: cognition and cathexis in concert. In Aversion, Avoidance and Anxiety, ed. T. Archer and L. Nilsson, pp. 45-85. Hillsdale, NJ: Erlbaum
38. Garcia, J., Hankins, W. G., Coil, J. D. 1977. Koalas, men, and other conditioned gastronomes. In Food Aversion Learning, ed. N. W. Milgram, L. Krames, T. M. Alloway, pp. 195-92. New York: Plenum
39. Garcia, J., Holder, M. D. 1985. Time, space and value. Hum. Neurobiol. 4:81-89
40. Green, G. C., Elwin, R. L., Mottershead, B. E., Keogh, R. G., Lynch, J. J. 1984. Long-term effects of early experience to supplementary feeding in sheep. Proc. Aust. Soc. Anim. Prod. 15:373-75
41. Grime, J. P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111: 1169-94
42. Habersang, S., Leuschner, F., Issac, O., Thiemer, K. 1979. Pharmacological studies of chamomile constituents. IV. Studies on the toxicity of (-)-a-bisabolol. Planta Medico 37:115-23
43. Haggerman, A. E., Butler, L. G. 1989. Choosing appropriate methods and standards for assaying tannin. J. Chem. Ecol. 15:1795-1810
44. Haley, T. J. 1982. Cineole (1,8-cineole). Dangerous Prop. Ind. Mater. Rep. 2:10-12
45. Hatton, J. C., Smart, N. O. E. 1984. The effect of long-term exclusion of large herbivores on soil nutrient status in Murchison Falls National Park, Uganda. Afr. J. Ecol. 22:23-30
46. Heady, F. H. 1964. Payability of herbage and animal preference. J. Range. Manage. 17:76-82
47. Hemingway, R. W., McGraw, G. W. 1983. Kinetics of acid-catalyzed cleavage of procyanidins. J. Wood. Chem. Technol. 3:421-35
48. Holling, C. S. 1959. The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can. Entomol. 91: 293-320
49. Hunter, R. F., Milner, C. 1963. The behavior of individual, related and groups of south country Cheviot hill sheep. Anim. Behav. 11:507-513
50. Jachman, H., Croes, T. 1991. Effects of browsing by elephants on the Combretum/Terminalia woodland at the Nazinga Game Ranch, Burkina Faso. Biol. Conserv. In press
51. Jefferies, R. L. 1988. Vegetational mosaics, plant-animal interactions and resources for plant growth. In Plant Evolutionary Biology, ed. L. D. Gottlieb, S. K. Jain, pp. 341-69. London: Chapman & Hall
52. Jefferies, R. L. 1989. Pattern and process in arctic coastal vegetation in response to foraging by Lesser Snow Geese. In Plant Form and Vegetation Structure, Adaptation. Plasticity and Relation to Herbivory, ed. M. J. A. Werger, pp. 1-20. the Hague: SPB Academic Publ.
53. Jogia, M. K., Sinclair, A. R. E., Anderson, R. J. 1989. An antifeedent in balsam poplar inhibits browsing by snowshoe hares. Oecologia (Berl.) 79: 189-92
54. Jung, H. G., Batzli, G. O. 1981. Nutritional ecology of microtine rodents: Effects of plant extracts in the growth of Arctic microtines. J. Mamm. 62:286-92
55. Key, C., MacIver, R. M. 1980. The effects of maternal influences on sheep: breed differences in grazing, resting and courtship behavior. Appl. Anim. Ethol. 6:33-48
56. Kingsbury, J. M. 1964. Poisonous Plants of the United States and Canada. Englewood Cliffs, NJ: Prentice-Hall
57. Kramer, P. J., Kozlowski, T. T. 1979. Physiology of Woody Plants. New York: Academic. 811 pp.
58. Krefting, L. W. 1974. The Ecology of Isle Royale Moose. Univ. Minn. Agric. Exp. Stn. Tech. Bull. 297, Forestry Series 15. 75 pp.
59. Kumar, R., Singh, M. 1984. Tannins: their adverse role in ruminant nutrition. J. Agric. Food Chem. 32:447-53
60. Lane, M. A., Ralphs, M. H., Olsen, J. D., Provenza, F. D., Pfister, J. A. 1990. Conditioned taste aversion: Potential for reducing cattle loss to larkspur. J. Range Manage. 43:127-31
61. Launchbaugh, K. L., Provenza, F. D. 1991. Can plants practice mimicry to avoid mammalian herbivory? Am. Nat. Submitted
62. Lindroth, R. L. 1988. Adaptations of mammalian herbivores to plant chemical defenses. In Chemical Mediation of Coevolution, ed. K. C. Spencer, pp. 415-45. New York: Academic. 609 pp.
63. Lindroth, R. L. 1989. Mammalian herbivore-plant interactions. In Plant-Animal Interactions, ed. W. G. Abrahamson, pp. 163-204. New York: McGraw-Hill. 480 pp.
64. Lynch, J. J. 1987. The transmission from generation to generation in sheep of the learned behaviour for eating grain supplements. Aust. Vet. J. 64:291-292
65. Lynch, J. J., Keogh, R. G., Elwin, R. L., Green, G. C., Mottershead, B. E. 1983. Effects of early experience on the post-weaning acceptance of whole grain wheat by fine-wool Merino lambs. Anim. Prod. 36:175-183
66. MacAvinchey, R. J. P. 1991. Winter herbivory by snowshoe hares and moose as a process affecting primary succession on an Alaskan floodplain. Thesis. Univ. Alaska, Fairbanks. 69 pp.
67. Mattson, W. J. Jr. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11:119-61
68. McArthur, C., Haggerman, A. E., Robbins, C. T. 1991. Physiological strategies of mammalian herbivores against plant defenses. In Plant Defenses Against Mammalian Herbivory, ed. T. Palo, C. Robbins. Boca Raton: CRC. In press
69. Mclnnes, P. F., Naimen, R. J., Pastor, J., Cohen, Y. 1991. Effects of moose browsing on vegetation and litterfall of the boreal forest, Isle Royale, Michigan, USA. Manuscript
70. McKey, D. 1979. The distribution of secondary compounds within plants. In Herbivores: Their Interaction With Secondary Plant Metabolites, ed. G. A. Rosenthal, D. H. Janzen, pp. 55-133. New York: Academic
71. McLeod, M. N. 1974. Plant tannins - their role in forage quality. Nutr. Abstr. Rev. 44:803-15
72. McNaughton, S. J., Ruess, R. W., Seagle, S. W. 1988. Large mammals and process dynamics in African ecosystems. BioScience 38:794-800
73. Meetemeyer, V. 1978. Macroclimate and lignin control of litter decomposition. Ecology 59:465-72
74. Melillo, J. M., Aber, J. D., Muratore, J. F. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621-26
75. Meyer, M. W., Karazov, W. H. 1989. Antiherbivore chemistry of Larrea tridentata: Effects of woodrat (Neotoma lepida) feeding and nutrition. Ecology 70:953-61
76. Meyer, M. W., Karazov, W. H. 1991. Deserts. In Plant Defenses Against Mammalian Herbivory, ed. T. Palo, C. Robbins. Boca Raton: CRC. In press
77. Mirza, S. N., Provenza, F. D. 1990. Preference of the mother affects selection and avoidance of foods by lambs differing in age. Appl. Anim. Behav. Sci. 28:255-63
78. Mirza, S. N., Provenza, F. D. 1991. Effects of age and conditions of exposure on maternally mediated food selection in lambs. Appl. Anim. Behav. Sci. In press
79. Mirza, S. N., Provenza, F. D. 1991. Socially-induced food avoidance in lambs: Direct or indirect maternal influence? Appl. Anim. Behav. Sci. In press
80. Moore, T. R. 1984. Litter decomposition in a subarctic spruce-lichen woodland, eastern Canada. Ecologv 65:299-308
81. Müller-Dombois, D. 1972. Crown distortion and elephant distribution in the woody vegetation of Ruhuna National Park, Ceylon. Ecology 53:208-26
82. Palo, T., Robbins, C 1991. Plant Defenses Against Mammalian Herbivory. Boca Raton: CRC. In press
83. Pastor, J., Aber, J. D., McClaugherty, C. A., Melillo, J. M. 1984. Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:256-68
84. Pastor, J., Dewey, B., Naimen, R. J., McInnes, P. F., Cohen, Y. 1991. Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Manuscript
85. Pastor, J., Naimem, R. J. 1991. Selective foraging and ecosystem processes in boreal forests. Manuscript
86. Pastor, J., Naimen, R. J., Dewey, B., Mclnnes, P. 1988. Moose, microbes, and the boreal forest. BioScience 38:770-77
87. Pehrson, A. 1983. Digestibility and retention of food components in caged mountain hares (Lepus timidus L.) during the winter. Holarctic Ecol. 6:395-403
88. Pehrson, A. 1987. Maximal winter browse intake in captive mountain hares. Finn. Game Res. 41:47-55
89. Pfister, J. A., Provenza, F. D., Manners, G. D. 1990. Ingestion of tall larkspur by cattle: separating the effects of flavor from post-ingestive consequences. J. Chem. Ecol. 16:1697-1705
90. Price, E. O. 1984. Behavioral aspects of animal domestication. Q. Rev. Biol. 59:1-32
91. Provenza, F. D., Balph, D. F. 1987. Diet learning by domestic ruminants: theory, evidence and practical implications. Appl. Anim. Behav. Sci. 18:211-32
92. Provenza, F. D., Balph, D. F. 1990. Applicability of five diet-selection models to various foraging challenges ruminants encounter. In Behavioral Mechanisms of Food Selection, ed. R. N. Hughes, Vol. 20, NATO ASI Series G: Ecological Sciences, pp. 423-59. Heildelberg: Springer-Verlag
93. Provenza, F. D., Burritt, E. A., Clausen, T. P., Bryant, J. P., Reichardt, P. B. 1990. Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. Am. Nat. 136:810-28
94. Provenza, F. D., Pfister, J. A., Cheney, C. D. 1991. Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. J. Range Manage. In press
95. Pyke, G. H. 1984. Optimal foraging theory: a critical review. Annu. Rev. Ecol. Syst. 15:523-75
96. Reichardt, P. B., Bryant, J. P., Anderson, B. J., Phillips, D., Clausen, T. P. 1990. Germacrone defends Labrador tea from browsing by snowshoe hares. J. Chem. Ecol. 16:1961-70
97. Reichardt, P. B., Bryant, J. P., Clausen, T. P., Wieland, G. D. 1984. Defense of winter-dormant Alaska paper birch against snowshoe hares. Oecologia 65: 58-69
98. Reichardt, P. B., Bryant, J. P., Mattes, B. R., Clausen, T. P., Chapin, F. S. III. 1990. The winter chemical defense of balsam poplar against snowshoe hares. J. Chem. Ecol. 16:1941-60
99. Reichardt, P. B., Clausen, T. P., Bryant, J. P. 1987. Plant secondary metabolites as feeding deterrents to vertebrate herbivores. In Proceedings-Symposium on Plant-Herbivore Interactions. USDA Forest Service Gen. Tech. Rept. INT-222, ed. F. D. Provenza, J. T. Flinders, E. D. McArthur, pp. 37-42. Ogden/Intermontain Res. Sta. 179 pp.
100. Reut, N. A., Danvsevich, I. K., Zakharovskii, A. S., Kuzmitskii, B. B., Kevra, M. K. 1975. Toxicological properties of synthetic camphor prepared from pine tree oleoresins. Farmakol. Toksikol. Nov. Prod. Khim. Sint., Mater. Resp. Korf. 3:185-7
101. Rhoades, D. F., Cates, R. G. 1976. Toward a general theory of plant antiherbivore chemistry. In Recent Advances in Phytochemistry, Vol 10. Biochemical Interactions Between Plants and Insects, ed. J. W. Wallace, R. L. Mansell, 10:168-213. New York: Plenum. 425 pp.
102. Roath, L. R., Krueger, W. C. 1982. Cattle grazing and behavior on forested range. J. Range Manage. 35:332-38
103. Robbins, C. T. 1983. Wildlife Nutrition. New York: Academic. 343 pp.
104. Rosenthal, G. A., Janzen, D. H. 1979. Herbivores: Their Interaction with Secondary Plant Metabolites. New York: Academic. 718 pp.
105. Ruess, R. W. 1987. Grazing and the dynamics of nutrient and energy regulated microbial processes in the Serengeti grasslands. Oikos 49:101-10
106. Ruess, R. W., Hik, D. S., Jefferies, R. L. 1989. The role of lesser snow geese as nitrogen processors in a sub-arctic salt marsh. Oecologia 79:23-9
107. Ruess, R. W., McNaughton, S. J. 1984. Urea as a promotive coupler of plant-herbivore interactions. Oecologia 63: 331-37
108. Schimel, D. S., Parton, W. J., Adamsen, F. J., Woodmansee, R. G., Senft, R. L. 1986. The role of cattle in the volatile loss of nitrogen from a shortgrass steppe. Biogeochemistry 2:39-52
109. Senft, R. L., Coughenour, M. B., Bailey, D. W., Rittenhouse, L. R., Sala, O. E. 1987. Large herbivore foraging and ecological hierarchies. Bioscience 37:789-99
110. Sinclair, A. R. E., Jogia, M. K., Anderson, R. J. 1989. Camphor from juvenile white spruce as an antifeedent for snowshoe hares. J. Chem. Ecol. 14: 1505-14
111. Sinclair, A. R. E., Krebs, C. J., Smith, J. N. M., Boutin, S. 1988. Population biology of snowshoe hares. III. Nutrition, plant secondary compounds and food limitation. J. Anim. Ecol. 57:787-806
112. Skinner, B. F. 1981. Selection by consequences. Science 213:501-04
113. Snyder, J. D., Janke, R. A. 1976. Impact of moose browsing on boreal-type forests of Isle Royale National Park. Am. Mid. Nat. 95:79-92
114. Squibb, R. C., Provenza, F. D., Balph, D. F. 1990. Effect of age of exposure to a shrub on the subsequent feeding response of sheep. J. Anim. Sci. 68:987-97
115. Stoddart, L. A., Smith, A. D., Box, T. W. 1975. Range Management. New York: McGraw-Hill
116. Swift, M. J., Heal, O. W., Anderson, J. M. 1979. Decomposition in Terrestrial Ecosystems. Oxford: Blackwell
117. Thorhallsdottir, A. G., Provenza, F. D., Balph, D. F. 1987. Food aversion learning in lambs with or without a mother: discrimination, novelty and persistence. Appl. Anim. Behav. Sci. 18:327-40
118. Thorhallsdottir, A. G., Provenza, F. D., Balph, D. F. 1990. Ability of lambs to leam about novel foods while observing or participating with social models. Appl. Anim. Behav. Sci. 25:25-33
119. Tiedmann, A. R., Berndt, H. W. 1972. Vegetation and soils of a 30-year deer and elk exclosure in central Washington. Northwest Sci. 46:59-66
120. Van Soest, P. 1982. Nutritional Ecology of the Ruminant. Corvalis, Oregon: O & B Books. 374 pp.
121. Vitousek, P. 1982. Nutrient cycling and nutrient use efficiency. Am. Nat. 119:553-72
122. Von Rudloff, E. 1975. Volatile leaf oil analysis in chemosystematic studies of North American Conifers. Biochem. Syst. Ecol. 2:131-67
123. Waage, S. K., Hedin, P. A., Grimley, G. 1984. A biologically active procyanidin from Machsarium floribundum. Phytochemistry 23:2785-87
124. Wolcott, G. N. 1953. Stilbenes and comparable materials for dry-wood termite control. J. Econ. Entomol. 46:374-75