Reducing predation through chemically mediated camouflage: Indirect effects of plant defenses on herbivores

Ecology

Volumn 80, Issue 2, 1999, Pages 495-509

  Stachowicz, John J ^a,c   Hay, Mark E ^b,c  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Associational defense; Chemical camouflage; Decorator crab; Dictyota; Enemy free space; Herbivory; Libinia; Marine chemical ecology; North Carolina, USA; Plant herbivore predator interactions; Seaweed; Specialization

Indexed keywords

ALGA; ANTIPREDATOR DEFENSE; CRUSTACEAN; HOST SPECIFICITY; PLANT DEFENSE; SYMBIONT;

DECAPODA; DICTYOTA MENSTRUALIS; LIBINIA DUBIA;

EID: 0033058957     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/0012-9658(1999)080[0495:RPTCMC]2.0.CO;2     Document Type: Article

References (91)

1. Adams, S. M. 1976a. Feeding ecology of celgrass fish communities. Transactions of the American Fisheries Society 105:514-519.
2. _. 1976b. The ecology of celgrass. Zostera marina (L.), fish communities. I. Structural analysis. Journal of Experimental Marine Biology and Ecology 22:269-291.
3. Aldredge, J. R., and J. T. Ratti. 1986. Comparison of some statistical techniques for analysis of resource selection. Journal of Wildlife Management 50:157-165.
4. Barbosa, P. 1988. Some thoughts on "the evolution of host range." Ecology 69:912-915.
5. Bernays, E. A. 1989. Host range in phytophagous insects: the potential role of generalist predators. Evolutionary Ecology 3:299-311.
6. Bernays, E. A., and R. F. Chapman. 1987. Chemical deterrence of plants. Pages 100-141 in Coevolution of plants and animals. J. B. Harborne, editor. Academic Press, New York, New York, USA.
7. Bernays, E. A., G. C. Driver, and M. Bilgener. 1989. Herbivores and plant tannins. Advances in Ecological Research 19:263-302.
8. Bernays, E. A., and M. Graham. 1988. On the evolution of host specificity in phytophagous insects. Ecology 69:886-892.
9. Bertness, M. D., S. D. Garrity, and S. C. Levings. 1981. Predation pressure and gastropod foraging: a tropical-temperate comparison. Evolution 35:995-1007.
10. Bolser, R. C., and M. E. Hay. 1996. Are tropical plants better defended? Palatability and defenses of temperate vs. tropical seaweeds. Ecology 77:2269-2286.
11. Breed, M. D., L. E. Snyder, T. L. Lynn, and J. A. Morhart. 1992. Acquired chemical camouflage in a tropical ant. Animal Behaviour 44:519-523.
12. Bryant, J. P., P. B. Reichardt, T. P. Clausen, F. D. Provenza, and P. J. Kuropat. 1992. Woody plant-mammal interactions. Pages 344-371 in G. A. Rosenthal and M. R. Berenbaum, editors. Herbivores: their interactions with plant secondary metabolites. Second edition. Volume two: Ecological and evolutionary processes. Academic Press. San Diego, California, USA.
13. Coley, P. D., and T. M. Aide. 1990. Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. Pages 25-49 in P. W. Price, T. M. Lewinsotin, G. W. Fernandes, and W. W. Benson, editors. Plant-animal interactions: evolutionary ecology in tropical and temperate regions. John Wiley and Sons, New York, New York, USA.
14. Conover, W. J. 1980. Practical nonparametric statistics. Second edition. John Wiley and Sons, New York, New York, USA.
15. Courtney, S. 1988. If it's not coevolution it must be predation? Ecology 69:910-911.
16. Cronin, G. C., and M. E. Hay. 1996a. Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531-1543.
17. Cronin, G. C., and M. E. Hay. 1996b. Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287-2301.
18. Cronin, G. C., N. Lindquist, M. E. Hay, and W. Fenical. 1995. Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis. Marine Ecology Progress Series 119:265-273.
19. Darcy, G. H. 1985. Synopsis of biological data on the pinfish Lugodon rhomboides (Pisces: Sparidae). National Oceanic and Atmospheric Administration Technical Report, National Marine Fisheries Service No. 23, U.S. Department of Commerce, National Technical Information Service, Springfield, Virginia, USA.
20. Dicke, M., M. W. Sabelis, J. Takabayashi, J. Bruin, M. A. Posthumus. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16:3091-3118.
21. Duffy, J. E., and M. E. Hay. 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286-1298.
22. Duffy, J. E., and M. E. Hay. 1994. Herbivore resistance to seaweed chemical defense: the roles of mobility and predator risk. Ecology 75:1304-1319.
23. Ehrlich, P. R., and D. D. Murphy. 1988. Plant chemistry and host range in insect herbivores. Ecology 69:908-909.
24. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
25. Eisner, T., K. Hicks, M. Eisner, and D. S. Robson. 1978. "Wolf-in-sheep's-clothing" strategy of a predaceous insect larva. Science 199:790-794.
26. Endler, J. A. 1986. Defense against predators. Pages 109-134 in Predator-prey relationships. M. E. Feder and G. V. Lauder, editors. University of Chicago Press, Chicago, Illinois, USA.
27. Fishlyn, D. A., and D. W. Phillips. 1980. Chemical camouflaging and behavioral defenses against a predatory seastar by three species of gastropods from the surfgrass Phyllospadix community. Biological Bulletin 158:34-48.
28. Fox, L. R. 1988. Diffuse coevolution within complex communities. Ecology 69:906-907.
29. Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207-233.
30. Gilliam, J. F. and D. F. Fraser. 1987. Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856-1862.
31. Gil-Turnes, M. S., M. E. Hay, and W. Fenical. 1989. Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungus. Science 246:116-118.
32. Hay, M. E. 1992. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. Pages 93-118 in Ecological roles of marine natural products. V. J. Paul, editor. Comstock, Ithaca, New York, USA.
33. _. 1996. Marine chemical ecology: what is known and what is next? Journal of Experimental Marine Biology and Ecology 200:103-134.
34. Hay, M. E., J. E. Duffy, and W. Fenical. 1990. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology 71:733-743.
35. Hay, M. E., J. E. Duffy, C. A. Pfister, and W. Fenical. 1987. Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567-1580.
36. Hay, M. E., and W. Fenical. 1988. Marine plant-herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics 19:111-145.
37. Hay, M. E., and W. Fenical. 1996. Chemical ecology and marine biodiversity: insights and products from the sea. Oceanography 9:10-20.
38. Hay, M. E., P. E. Renaud, and W. Fenical. 1988. Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defense. Oecologia 75:246-252.
39. Hay, M. E., and P. D. Steinberg. 1992. The chemical ecology of plant-herbivore interactions in marine vs. terrestrial communities. Pages 372-413 in G. A. Rosenthal and M. R. Berenbaum, editors. Herbivores: their interactions with plant secondary metabolites. Second edition. Volume two: Ecological and evolutionary processes. Academic Press, San Diego, California, USA.
40. Heck, K. L., Jr., and K. A. Wilson. 1987. Predation rates on decapod crustaceans in latitudinally separated seagrass communities: a study of spatial and temporal variation using tethering techniques. Journal of Experimental Marine Biology and Ecology 107:87-100.
41. Hughes, R. N., and R. W. Elner. 1979. Tactics of a predator, Carcinus maenas and morphological responses of the prey, Nucella lapillus. Journal of Animal Ecology 48:65-78.
42. Hunter, M. D., and J. C. Schultz. 1993. Inducible defenses breached? Phytochemical induction protects an herbivore from disease. Oecologia 94:195-203.
43. Janzen, D. H. 1973. Dissolution of mutualism between Cecropia and its Azteca ants. Biotropica 5:15-28.
44. Jenny, T. 1988. Can predation lead to narrow food specialization in phytophagous insects. Ecology 69:902-904.
45. Kibota, T. T., and S. P. Courtney. 1991. Jack of one trade, master of none: host choice by Drosophila magnaquinaria. Oecologia 86:251-260.
46. Kilar, J. A., and R. M. Lou. 1986. The subtleties of camouflage and dietary preference of the decorator crab, Microphyrs bicornutus Latreille (Decapoda: Brachyura). Journal of Experimental Marine Biology and Ecology 101:143-160.
47. Kobayashi, T., and M. Watanabe. 1986. An analysis of snakescent application behaviour in Siberian chipmunks (Eutamias sibiricus asiaticus). Ethology 72:40-52.
48. Lubchenco, J., and S. D. Gaines. 1981. A unified approach to plant-herbivore interactions. I. Populations and communities. Annual Review of Ecology and Systematics 12:405-437.
49. McMahan, E. A. 1982. Bait-and-capture strategy of a termite-eating assassin bug. Insectes Sociaux 29:346-351.
50. Menge, B. A., and J. Lubchenco. 1981. Community organization in temperate and tropical rocky intertidal habitats: prey refuges in relation to consumer pressure gradients. Ecological Monographs 51:429-450.
51. Motta, P. J., K. B. Clifton, P. Hernandez, B. T. Eggold, S. D. Giordano, and R. Wilcox. 1995. Feeding relationships among nine species of seagrass fishes of Tampa Bay, Florida. Bulletin of Marine Science 56:185-200.
52. Paul, V. J. 1992. Ecological roles of marine natural products. Comstock, Ithaca, New York, USA.
53. Peterson, C. H., and P. E. Renaud. 1989. Analysis of feeding preference experiments. Oecologia 80:82-86.
54. Price, P. W., C. E. Bouton, P. Gross, B. A. McPherson, J. N. Thompson, and A. E. Weiss. 1980. Interactions among three trophic levels: influence of plants on interactions between herbivores and natural enemies. Annual Review of Ecology and Systematics 11:41-65.
55. Price, P. W., M. Westoby, B. Rice, P. R. Atsatt, R. S. Fritz, J. N. Thompson, and K. Mobley. 1986. Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics 17:487-505.
56. Rausher, M. D. 1988. Is coevolution dead? Ecology 69:898-901.
57. Renaud, P. E., M. E. Hay, and T. M. Schmitt. 1990. Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217-226.
58. Rickson, F. R. 1977. Progressive loss of ant-related traits of Cecropia peltata on selected Caribbean Islands. American Journal of Botany 64:585-592.
59. Rosenthal, G. A., and M. R. Berenbaum. 1992. Herbivores: their interactions with plant secondary metabolites. Second edition. Volume two: Ecological and evolutionary processes. Academic Press, San Diego, California, USA.
60. Ross, S. W., and M. L. Moser. 1995. Life history of juvenile gag, Mycteroperca microlepis, in North Carolina estuaries. Bulletin of Marine Science 56:222-237.
61. Rowell-Rahier, M., and J. M. Pasteels. 1992. Third trophic level influences of plant allelochemicals. Pages 243-278 in G. A. Rosenthal and M. R. Berenhaum, editors. Herbivores: their interactions with plant secondary metabolites. Second edition. Volume two: Ecological and evolutionary processes. Academic Press, San Diego, California, USA.
62. Rozema, J., J. van de Staaij, L. O. Bjorn, and M. Caldwell. 1997. UV-B as an environmental factor in plant life: stress and regulation. Trends in Ecology and Evolution 12:22-28.
63. Schmitt, T. M., M. E. Hay, and N. Lindquist. 1995. Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107-123.
64. Schneider, C. W., and R. B. Searles. 1991. Seaweeds of the southeastern United States: Cape Hatteras to Cape Canaveral. Duke University Press, Durham, North Carolina, USA.
65. Schultz, J. C. 1988. Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69:896-897.
66. _. 1992. Factoring natural enemies into plant tissue availability to herbivores. Pages 175-199 in M. D. Hunter, T. Ohgushi, and P. W. Price, editors. Effects of resource distribution on animal-plant interactions. Academic Press, San Diego, California, USA.
67. Schultz, J. C., M. A. Foster, and M. E. Montgomery. 1990. Host-plant mediated impacts of a baculovirus on gypsy moth populations. Pages 303-313 in A. D. Watt, S. R. Leather, M. D. Hunter, and N. A. C. Kidd, editors. Population dynamics of forest insects. Intercept Press, Andover, UK.
68. Schwartz, F. J., and B. W. Dutcher. 1963. Age, growth, and food of the oyster toadfish near Solomons, Maryland, Transactions of the American Fisheries Society 92:170-173.
69. Sih, A. 1986. Anti-predator responses and the perception of danger by mosquito larvae. Ecology 67:434-441.
70. _. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. Pages 203-224 in W. C. Kerfoot and A. Sih, editors. Predation: direct and indirect impacts on aquatic communities. University Press of New England. Hanover, New Hampshire, USA.
71. Sih, A., L. B. Kats, and R. D. Moore. 1992. Effects of predatory sunfish on the density, drift, and refuge use of stream salamander larvae. Ecology 73:1418-1430.
72. Slansky, F. 1992. Allelochemical-nutrient interactions in herbivore nutritional ecology. Pages 135-174 in G. A. Rosenthal and M. R. Berenbaum, editors. Herbivores: their interactions with plant secondary metabolites. Second edition. Volume two: Ecological and evolutionary processes. Academic Press, San Diego, California, USA.
73. Stachowicz, J. J., and M. E. Hay. 1996. Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105:377-387.
74. Stowe, M. K. 1988. Chemical mimicry. Pages 513-580 in K. C. Spencer, editor. Chemical mediation of coevolution. Academic Press, San Diego, California, USA.
75. Stowe, M. K., J. H. Tumlinson, and R. R. Heath. 1987. Chemical mimicry: bolas spiders emit components of moth prey species sex pheromones. Science 236:964-967.
76. Strong, D. R., J. H. Lawton, and T. R. E. Southwood. 1984. Insects on plants: community patterns and mechanisms. Blackwell Scientific, Oxford, UK.
77. Thompson, J. N. 1988. Coevolution and alternative hypotheses on insect/plant interactions. Ecology 69:893-895.
78. _. 1994. The revolutionary process. University of Chicago Press, Chicago, USA.
79. Travis, J. 1996. The significance of geographical variation in species interactions. American Naturalist 148:S1-S8.
80. Vadas, R. L., Sr., M. T. Burrows, and R. N. Hughes. 1994. Foraging strategies of dogwhelks, Nucella lapillus (L.): interacting effects of age, diet and chemical cues to the threat of predation. Oecologia 100:439-450.
81. Vince, S., I. Valiela, N. Backus, and J. M. Teal. 1976. Predation by the salt marsh killifish Fundulus heteroclitus (L.) in relation to prey size and habitat structure: consequences for prey distribution and abundance. Journal of Experimental Marine Biology and Ecology 23:255-266.
82. Wainwright, P. C. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77:1336-1343.
83. Wainwright, P. C., and B. A. Richard. 1995. Predicting patterns of prey use from morphology with fishes. Environmental Biology of Fishes 44:97-113.
84. Werner, E. E. 1974. The fish size, prey size, and handling time relation in several sunfishes and some implications. Journal of the Fisheries Research Board of Canada 31:1531-1536.
85. _. 1977. Species packing and niche complementarity in three sunfishes. American Naturalist 111:553-578.
86. Werner, E. E., J. F. Gilliam, D. J. Hall, and G. G. Mittelbach, 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540-1548.
87. Wicksten, M. K. 1979. Decorating behavior in Loxorhynchus crispatus Stimpson and Loxorhynchus grandis Stimpson (Brachyura: Majidae). Crustaceana 5(supplement):37-46.
88. _. 1980. Decorator crabs. Scientific American 242:146-154.
89. _. 1983. Camouflage in marine invertebrates. Oceanography and Marine Biology Annual Review 21:177-193.
90. Williams, A. B. 1984. Shrimps, lobsters and crabs of the Atlantic coast. Smithsonian Press, Washington, D.C., USA.
91. Wilson, C. A., J. M. Dean, and R. Radtke. 1982. Age, growth rate and feeding habits of the oyster toadfish, Opsanus tau, in South Carolina. Journal of Experimental Marine Biology and Ecology 62:251-259.