Plant defense syndromes

Ecology

Volumn 87, Issue 7 SUPPL., 2006, Pages

  Agrawal, Anurag A ^a   Fishbein, Mark ^b,c  

^a Department of Obstetrics Gynecology   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c PORTLAND STATE UNIVERSITY   (United States)

Author keywords

Asclepias; Cardenolides; Chemical ecology; Cluster analysis; Coevolution; Danaus plexippus; Herbivory; Latex; Milkweed; Monarch butterfly; Phylogenetically independent contrasts; Phytochemistry; Plant insect interactions

Indexed keywords

BUTTERFLY; CATERPILLAR; DEFENSE MECHANISM; EVOLUTIONARY BIOLOGY; HERBIVORY; NUTRITIONAL REQUIREMENT; PHYLOGENETICS; PLANT DEFENSE; PLANT-INSECT INTERACTION;

APOCYNACEAE; ASCLEPIAS; DANAUS PLEXIPPUS; INSECTA;

EID: 33749858234     PISSN: 00129658     EISSN: 00129658     Source Type: Journal    
DOI: 10.1890/0012-9658(2006)87[132:pds]2.0.co;2     Document Type: Article

References (115)

1. Ackerly, D. D., and M. J. Donoghue. 1998. Leaf size, sapling allometry, and Corner's rules: phylogeny and correlated evolution in maples (Acer). American Naturalist 152:767-791.
2. Adler, L. S., J. Schmitt, and M. D. Bowers. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75-85.
3. Agrawal, A. A. 2004a. Plant defense and density dependence in the population growth of herbivores. American Naturalist 164:113-120.
4. Agrawal, A. A. 2004b. Resistance and susceptibility of milk-weed: competition, root herbivory, and plant genetic variation. Ecology 85:2118-2133.
5. Agrawal, A. A. 2005. Natural selection on common milk-weed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research 7:651-667.
6. Agrawal, A., and R. Karban. 2000. Specificity of constitutive and induced resistance: pigment glands influence mites and caterpillars on cotton plants. Entomologia Experimentalis et Applicata 96:39-49.
7. Agrawal, A. A., and N. S. Kurashige. 2003. A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. Journal of Chemical Ecology 29:1403-1415.
8. Agrawal, A. A., and S. B. Malcolm. 2002. Once upon a milkweed. Natural History 111(7):48-53.
9. Agrawal, A. A., and D. A. Spiller. 2004. Polymorphic button-wood: effects of disturbance on resistance to herbivores in green and silver morphs of a Bahamian shrub. American Journal of Botany 91:1990-1997.
10. Agrawal, A. A., and P. A. Van Zandt. 2003. Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. Journal of Ecology 91:1049-1059.
11. Armbruster, W. S., C. Pélabon, T. F. Hansen, and C. P. H. Mulder. 2004. Floral integration, modularity, and accuracy. Pages 23-49 in M. Pigliucci and K. Preston, editors. Phenotypic integration. Oxford University Press, Oxford, UK.
12. Beardsley, P. M., A. Yen, and R. G. Olmstead. 2003. AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57:1397-1410.
13. Becerra, J. X. 1997. Insects on plants: macroevolutionary chemical trends in host use. Science 276:253-256.
14. Becerra, J. X., and D. L. Venable. 1999. Macroevolution of insect-plant associations: the relevance of host biogeography to host affiliation. Proceedings of the National Academy of Sciences (USA) 96:12626-12631.
15. Becerra, J. X., D. L. Venable, P. H. Evans, and W. S. Bowers. 2001. Interactions between chemical and mechanical defenses in the plant genus Bursera and their implications for herbivores. American Zoologist 41:865-876.
16. Bennett, R. N., and R. M. Wallsgrove. 1994. Tansley review no. 72. Secondary metabolites in plant defence mechanisms. New Phytologist 127:617-633.
17. Berenbaum, M. R. 2001. Chemical mediation of coevolution: phylogenetic evidence for Apiaceae and associates. Annals of the Missouri Botanical Garden 88:45-59.
18. Berenbaum, M. R., J. K. Nitao, and A. R. Zangerl. 1991. Adaptive significance of furanocoumarin diversity in Pastinaca sativa (Apiaceae). Journal of Chemical Ecology 17:207-215.
19. Berenbaum, M. R., A. R. Zangerl, and K. Lee. 1989. Chemical barriers to adaptation by a specialist herbivore. Oecologia 80:501-506.
20. Berenbaum, M. R., A. R. Zangerl, and J. K. Nitao. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40:1215-1228.
21. Blakley, N. R., and H. Dingle. 1978. Competition: butterflies eliminate milkweed bugs from a Caribbean island. Oecologia 37:133-136.
22. Bollwinkel, C. W. 1969. A revision of the South American species of Asclepias L. Dissertation. Southern Illinois University, Carbondale, Illinois, USA.
23. Broadway, R. M., and S. S. Duffey. 1988. The effects of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. Journal of Insect Physiology 34:1111-1118.
24. Bromham, L., M. Woolfit, M. S. Y. Lee, and A. Rambaut. 2002. Testing the relationships between morphological and molecular rates of change along phylogenies. Evolution 56:1921-1930.
25. Brower, L. P., P. B. McEvoy, K. L. Williamson, and M. A. Flannery. 1972. Variation in cardiac glycoside content of monarch butterflies from natural populations in eastern North America. Science 177:426-429.
26. Brower, L. P., J. Van Zandt, and J. M. Corvino. 1967. Plant poisons in a terrestrial food chain. Proceedings of the National Academy of Science (USA) 57:893-898.
27. Bryant, J. P., F. S. Chapin, and D. R. Klein. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-368.
28. Castellanos, M. C., P. Wilson, and J. D. Thomson. 2003. Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57:2742-2752.
29. Castellanos, M. C., P. Wilson, and J. D. Thomson. 2004. "Antibee" and "pro-bird" changes during the evolution of hummingbird pollination in Penstemon flowers. Journal of Evolutionary Biology 17:876-885.
30. Cavender-Bares, J., D. D. Ackerly, D. A. Baum, and F. A. Bazzaz. 2004. Phylogenetic overdispersion in Floridian oak communities. American Naturalist 163:823-843.
31. Chapin, F. S., K. Autumn, and F. Pugnaire. 1993. Evolution of suites of traits in response to environmental stress. American Naturalist 142:S78-S92.
32. Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53:209-233.
33. Coley, P. D. 1987. Interspecific variation in plant anti-herbivore properties: the role of habitat quality and rate of disturbance. New Phytologist 106:251-264.
34. Coley, P. D., J. P. Bryant, and F. S. Chapin. 1985. Resource availability and plant antiherbivore defense. Science 230:895-899.
35. Conway-Morris, S. 2003. Life's solution: inevitable humans in a lonely universe. Cambridge University Press, Cambridge, UK.
36. Cunningham, S. A., B. Summerhayes, and M. Westoby. 1999. Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69:569-588.
37. Da Costa, C. P., and C. M. Jones. 1971. Cucumber beetle resistance and mite susceptibility controlled by the bitter gene in Cucumis sativus L. Science 172:1145-1146.
38. Dobzhansky, T. G. 1970. Genetics of the evolutionary process. Columbia University Press, New York, New York, USA.
39. Duffey, S. S., and M. J. Stout. 1996. Antinutritive and toxic components of plant defense against insects. Archives of Insect Biochemistry and Physiology 32:3-37.
40. Dussourd, D. E., and T. Eisner. 1987. Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898-900.
41. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
42. Fægri, K., and L. van der Pijl. 1979. The principles of pollination ecology. Third edition. Pergamon Press, New York, New York, USA.
43. Farrell, B. D., D. E. Dussourd, and C. Mitter. 1991. Escalation of plant defense: Do latex and resin canals spur plant diversification? American Naturalist 138:881-900.
44. Farrell, B. D., and C. Mitter. 1993. Phylogenetic determinants of insect/plant community diversity. Pages 253-266 in R. Ricklefs and D. Schluter, editors. Historical and geographical determinants of community diversity. University of Chicago Press, Chicago, Illinois, USA.
45. Farrell, B. D., and C. Mitter. 1998. The timing of insect-plant diversification: Might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 63:553-577.
46. Feeny, P. P. 1976. Plant apparency and chemical defense. Pages 1-40 in J. W. Wallace and R. L. Mansell, editors. Biochemical interaction between plants and insects. Plenum, New York, New York, USA.
47. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
48. Fenster, C. B., W. S. Armbruster, M. R. Dudash, P. Wilson, and J. D. Thomson. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology and Systematics 35:375-403.
49. Fine, P. V. A., I. Mesones, and P. D. Coley. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663-665.
50. Fine, P. V. A., Z. J. Miller, I. Mesones, S. Irazuzta, H. M. Appel, M. H. H. Stevens, I. Sääksjärvi, J. C. Schultz, and P. D. Coley. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87:S150-S162.
51. Fishbein, M. 1996. Phylogenetic relationships of North American Asclepias L. and the role of pollinators in the evolution of the milkweed inflorescence. Dissertation, University of Arizona, Tucson, Arizona, USA.
52. Fishbein, M., C. Hibsch-Jetter, D. E. Soltis, and L. Hufford. 2001. Phylogeny of Saxifragales (angiosperms, eudicots): analysis of a rapid, ancient radiation. Systematic Biology 50:817-847.
53. Fishbein, M., and D. E. Soltis. 2004. Further resolution of the rapid radiation of Saxifragales (angiosperms, eudicots) supported by mixed-model Bayesian analysis. Systematic Botany 29:883-891.
54. Fordyce, J. A., and S. B. Malcolm. 2000. Specialist weevil, Rhyssomatus lineaticollis, does not spatially avoid cardenolide defenses of common milkweed by ovipositing into pith tissue. Journal of Chemical Ecology 26:2857-2874.
55. Fornoni, J., P. L. Valverde, and J. Núñez-Fárfan. 2004. Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 58:1696-1704.
56. Giamoustaris, A., and R. Mithen. 1995. The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Annals of Applied Biology 126:347-363.
57. Goldman, N., J. P. Anderson, and A. G. Rodrigo. 2000. Likelihood-based tests of topologies in phylogenetics. Systematic Biology 49:652-670.
58. Grime, J. P. 1977. Evidence for existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111:1169-1194.
59. Gunasena, G. H., S. B. Vinson, H. J. Williams, and R. D. Stipanovic. 1988. Effects of caryophyllene, caryophyllene oxide, and their interaction with gossypol on the growth and development of Heliothis virescens (F) (Lepidoptera, Noctuidae). Journal of Economic Entomology 81:93-97.
60. Haddad, N. M., and W. M. Hicks. 2000. Host pubescence and the behavior and performance of the butterfly Papilio troilus (Lepidoptera: Papilionidae). Environmental Entomology 29:299-303.
61. Heil, M., T. Delsinne, A. Hilpert, S. Schurkens, C. Andary, K. E. Linsenmair, M. S. Sousa, and D. McKey. 2002. Reduced chemical defence in ant-plants? A critical re-evaluation of a widely accepted hypothesis. Oikos 99:457-468.
62. Heil, M., S. Greiner, H. Meimberg, R. Kruger, J.-L. Noyer, G. Heubl, K. E. Linsenmair, and W. Boland. 2004. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205-208.
63. Heil, M., C. Staehelin, and D. McKey. 2000. Low chitinase activity in Acacia myrmecophytes: A potential trade-off between biotic and chemical defences? Naturwissenschaften 87:555-558.
64. Herms, D. A., and W. J. Mattson. 1992. The dilemma of plants: to grow or defend. Quarterly Review of Biology 67:283-335.
65. Housworth, E. A., and E. P. Martins. 2001. Random sampling of constrained phylogenies: conducting phylogenetic analyses when the phylogeny is partially known. Systematic Biology 50:628-639.
66. Janzen, D. H. 1974. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6:69-103.
67. Koricheva, J., H. Nykänen, and E. Gianoli. 2004. Metaanalysis of trade-offs among plant antiherbivore defenses: Are plants jacks-of-all-trades, masters of all? American Naturalist 163:E64-E75.
68. Kursar, T. A., and P. D. Coley. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochemical Systematics and Ecology 31:929-949.
69. Lavoie, B., and K. S. Oberhauser. 2004. Compensatory feeding in Danaus plexippus (Lepidoptera: Nymphalidae) in response to variation in host plant quality. Environmental Entomology 33:1062-1069.
70. Legendre, P., and L. Legendre. 1998. Numerical ecology. Second English edition. Elsevier Science BV, Amsterdam, The Netherlands.
71. Lewis, P. L. 2001. Maximum likelihood phylogenetic inference: modeling discrete morphological characters. Systematic Biology 50:913-925.
72. Maddison, D. R., and W. P. Maddison. 2003. MacClade. Version 4.06. Sinauer Associates, Sunderland, Massachusetts, USA.
73. Malcolm, S. B. 1991. Cardenolide-mediated interactions between plants and herbivores. Pages 251-296 in G. A. Rosenthal and M. R. Berenbaum, editors. Herbivores: their interactions with secondary plant metabolites. Volume 1. Academic Press, San Diego, California, USA.
74. Malcolm, S. B., B. J. Cockrell, and L. P. Brower. 1989. Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. Journal of Chemical Ecology 15:819-853.
75. Mattson, W. J., Jr. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11:119-161.
76. McDade, L. A. 1992. Pollinator relationships, biogeography, and phylogenetics. BioScience 42:21-26.
77. Mooers, A. Ø., S. M. Vamosi, and D. Schluter. 1999. Using phylogenies to test macroevolutionary hypotheses of trait evolution in cranes (Gruinae). American Naturalist 154:249-259
78. Morse, D. H. 1985. Milkweeds and their visitors. Scientific American 253:112-119.
79. Nelson, C. J. 1993. Sequestration and storage of cardenolides and cardenolide glycosides by Danaus plexippus and D. chrysippus petila when reared on Asclepias fruticosa: with a review of some factors that influence sequestration. Pages 91-105 in S. B. Malcolm and M. P. Zalucki, editors. Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County, Los Angeles, California, USA.
80. Pagel, M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology. 48:612-622.
81. Price, P., and M. Willson. 1979. Abundance of herbivores on six milkweed species in Illinois. American Midland Naturalist 101:76-86.
82. Rapini, A., M. W. Chase, D. J. Goyder, and J. Griffiths. 2003. Asclepiadeae classification: evaluating the phylogenetic relationships of New World Asclepiadoideae (Apocynaceae). Taxon 52:33-50.
83. Rehr, S. S., P. P. Feeny, and D. H. Janzen. 1973. Chemical defence in Central American non-ant-Acacias. Journal of Animal Ecology 42:405-416.
84. Romeo, J. T., J. A. Saunders, and P. Barbosa, editors. 1996. Phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York, New York, USA.
85. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
86. Root, R. B. 1967. The niche exploitation pattern of the Blue-gray Gnatcatcher. Ecological Monographs 37:317-350.
87. Rothschild, M., J. V. Euw, and T. Reichste. 1970. Cardiac glycosides in Oleander aphid, Aphis nerii. Journal of Insect Physiology 16:1141-1145.
88. Rudgers, J. A., S. Y. Strauss, and J. F. Wendel. 2004. Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). American Journal of Botany 91:871-880.
89. Schädler, M., G. Jung, H. Auge, and R. Brandl. 2003. Palatability, decomposition and insect herbivory: patterns in a successional old-field plant community. Oikos 103:121-132.
90. Schemske, D. W., and H. D. Bradshaw. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proceedings of the National Academy of Sciences (USA) 96:11910-11915.
91. Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford, UK.
92. Seigler, D. S., and J. E. Ebinger. 1987. Cyanogenic glycosides in ant-Acacias of Mexico and Central America. Southwestern Naturalist 32:499-503.
93. Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16:1114-1116.
94. Silvertown, J., and M. Dodd. 1996. Comparing plants and connecting traits. Philosophical Transactions of the Royal Society of London B 351:1233-1239.
95. Simberloff, D., and T. Dayan. 1991. The guild concept and the structure of ecological communities. Annual Review of Ecology and Systematics 22:115-143.
96. Stapley, L. 1998. The interaction of thorns and symbiotic ants as an effective defence mechanism of swollen-thorn acacias. Oecologia 115:401-405.
97. Steward, J. L., and K. H. Keeler. 1988. Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)? Oikos 53:79-86.
98. Swofford, D. L. 2001. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts, USA.
99. Thaler, J. S., and R. Karban. 1997. A phylogenetic reconstruction of constitutive and induced resistance in Gossypium. American Naturalist 149:1139-1146.
100. Thomson, J. D., P. Wilson, M. Valenzuela, and M. Malzone. 2000. Pollen presentation and pollination syndromes, with special reference to Penstemon. Plant Species Biology 15:11-29.
101. Tilman, D., and S. Pacala. 1993. The maintenance of species richness in plant communities. Pages 13-25 in R. Ricklefs and D. Schulter, editors. Species diversity in ecological communities. University of Chicago Press, Chicago, Illinois, USA.
102. Twigg, L. E., and L. V. Socha. 1996. Physical versus chemical defence mechanisms in toxic Gastrolobium. Oecologia 108:21-28.
103. Van Dam, N. M., and J. D. Hare. 1998. Differences in distribution and performance of two sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecological Entomology 23:22-32.
104. van der Meijden, E., M. Wijn, and H. J. Verkaar. 1988. Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355-363.
105. Van Zandt, P. A., and A. A. Agrawal. 2004a. Specificity of induced plant responses to specialist herbivores of the common milkweed, Asclepias syriaca. Oikos 104:401-409.
106. Van Zandt, P. A., and A. A. Agrawal. 2004b. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616-2629.
107. Waser, N. M., L. Chittka, M. V. Price, N. M. Williams, and J. Ollerton. 1996. Generalization in pollination systems, and why it matters. Ecology 77:1043-1060.
108. Weiss, H. B., and E. L. Dickerson. 1921. Notes on milkweed insects in New Jersey. Journal of the New York Entomological Society 20:123-145.
109. Wilbur, H. 1976. Life history evolution in seven milkweeds of the genus Asclepias. Journal of Ecology 64:223-240.
110. Wilkinson, L. 1997. SYSTAT 7.0: the system for statistics. SPSS, Chicago, Illinois, USA.
111. Wilson, P., M. C. Castellanos, J. N. Hogue, J. D. Thomson, and W. S. Armbruster. 2004. A multivariate search for pollination syndromes among penstemons. Oikos 104:345-361.
112. Woodman, R. L., and G. W. Fernandes. 1991. Differential mechanical defense: herbivory, evapotranspiration, and leaf hairs. Oikos 60:11-19.
113. Woodson, R. E., Jr. 1954. The North American species of Asclepias L. Annals of the Missouri Botanical Garden 41:1-211.
114. Zalucki, M. P., L. P. Brower, and A. Alonso. 2001. Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecological Entomology 26:212-224.
115. Zar, J. H. 1996. Biostatistical analysis. Prentice Hall, Englewood Cliffs, New Jersey, USA.