Survival trade-offs associated with inducible defences in snails: The roles of multiple predators and developmental plasticity

Functional Ecology

Volumn 23, Issue 6, 2009, Pages 1179-1188

  Hoverman, Jason T ^a   Relyea, Rick A ^b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Developmental plasticity; Fitness; Functional trade off; Gastropod; Predator specific defence; Size refuge

Indexed keywords

ADAPTATION; ANTIPREDATOR DEFENSE; ECOMORPHOLOGY; FITNESS; FRESHWATER ECOSYSTEM; HYPOTHESIS TESTING; PHENOTYPIC PLASTICITY; REPRODUCTIVE COST; SNAIL; SURVIVAL; TRADE-OFF;

BASOMMATOPHORA; GASTROPODA;

EID: 70449341478     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2009.01586.x     Document Type: Article

References (71)

1. Alexander, J.E.J. Covich, A.P. (1991) Predation risk and avoidance behavior in two freshwater snails. Biological Bulletin Woods Hole, 180, 387 393.
2. Appleton, R.D. Palmer, A.R. (1988) Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shell in marine gastropods. Proceedings of the National Academy of Sciences (USA), 85, 4387 4391.
3. Benard, M.F. (2006) Survival trade-offs between two predator-induced phenotypes in Pacific treefrogs (Pseudacris regilla). Ecology, 87, 340 346.
4. Brönmark, C. Hansson, L.A. (2000) Chemical communication in aquatic systems: an introduction. Oikos, 88, 103 109.
5. Brönmark, C. Miner, J.G. (1992) Predator-induced phenotypical cange in body morphology in crucian carp. Science, 258, 1348 1350.
6. Chalcraft, D.R. Resetarits, W.J. (2003) Predator identity and ecological impacts: Functional redundancy or functional diversity? Ecology, 84, 2407 2418.
7. Chivers, D.P. Smith, R.J.F. (1998) Chemical alarm signaling in aquatic predator-prey systems: A review and prospectus. Ecoscience, 5, 338 352.
8. Dewitt, T.J. Langerhans, R.B. (2003) Multiple prey traits, multiple predators: Keys to understanding complex community dynamics. Journal of Sea Research, 49, 143 155.
9. Dewitt, T.J., Robinson, B.W. Wilson, D.S. (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research, 2, 129 148.
10. Dewitt, T.J., Sih, A. Hucko, J.A. (1999) Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour. Animal Behaviour, 58, 397 407.
11. Dill, L.M. (1987) Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Canadian Journal of Zoology, 65, 803 811.
12. Dodson, S.I. Havel, J.E. (1988) Indirect prey effects some morphological and life history responses of Daphnia pulex exposed to Notonecta undulata. Limnology and Oceanography, 33, 1274 1285.
13. Dodson, S.I., Crowl, T.A., Peckarsky, B.L., Kats, L.B., Covich, A.P. Culp, J.M. (1994) Non-visual communication in freshwater benthos: an overview. Journal of the North American Benthological Society, 13, 268 282.
14. Donohue, K., Messiqua, D., Pyle, E.H., Heschel, M.S. Schmitt, J. (2000) Evidence of adaptive divergence in plasticity: Density- and site-dependent selection on shade-avoidance responses in Impatiens capensis. Evolution, 54, 1956 1968.
15. Dudley, S.A. Schmitt, J. (1996) Testing the adaptive plasticity hypothesis: Density-dependent selection on manipulated stem length in Impatiens capensis. American Naturalist, 147, 445 465.
16. Gabriel, W., Luttbeg, B., Sih, A. Tollrian, R. (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. American Naturalist, 166, 339 353.
17. Gavrilets, S. (1986) An approach to modeling the evolution of populations with consideration of genotype-environment interactions [Trans. from Russian]. Soviet Genetics, 22, 28 36.
18. Gotthard, K. Nylin, S. (1995) Adaptive plasticity and plasticity as an adaptation: A selective review of plasticity in animal morphology and life-history. Oikos, 74, 3 17. (Pubitemid 3005220)
19. Henry, P.Y. Jarne, P. (2007) Marking hard-shelled gastropods: tag loss, impact on life-history traits, and perspectives in biology. Invertebrate Biology, 126, 138 153.
20. Hoverman, J.T., Auld, J.R. Relyea, R.A. (2005) Putting prey back together again: Integrating predator-induced behavior, morphology, and life history. Oecologia, 144, 481 491.
21. Hoverman, J.T. Relyea, R.A. (2007a) How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal. Ecology, 88, 693 705.
22. Hoverman, J.T. Relyea, R.A. (2007b) The rules of engagment: How to defend against combinations of predators. Oecologia, 154, 551 560.
23. Hoverman, J.T. Relyea, R. A. (2008) Temporal environmental variation and phenotypic plasticity: a mechanism underlying priority effects. Oikos, 117, 23 32.
24. Karban, R. Baldwin, I.T. (1997) Induced Responses to Herbivory. The University of Chicago Press, Chicago, Illinois, U.S.A.
25. Kats, L.B. Dill, L.M. (1998) The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience, 5, 361 394.
26. Kesler, D.K. Munns, W.R. Jr. (1989) Predation by Belostoma flumineum (Hemiptera): an important cause of mortality in freshwater snails. Journal of the North American Benthological Society, 8, 342 350.
27. Kingsolver, J.G. (1995a) Fitness consequences of seasonal polyphenism in western white butterflies. Evolution, 49, 942 954.
28. Kingsolver, J.G. (1995b) Viability selection on seasonally polyphenic traits: wing melanin pattern in western white butterflies. Evolution, 49, 932 941.
29. Kishida, O. Nishimura, K. (2005) Multiple inducible defences against multiple predators in the anuran tadpole, Rana pirica. Evolutionary Ecology Research, 7, 619 631.
30. Krueger, D.A. Dodson, S.I. (1981) Embryological induction and predation ecology in Daphnia pulex. Limnology and Oceanography, 26, 219 223.
31. Kuhlmann, H.W. Heckmann, K. (1985) Interspecific morphogens regulating prey-predator relationships in protozoa. Science, 1985, 1347 1349.
32. Kusch, J. (1995) Adaptation of inducible defense in Euplotes daidaleos (Ciliophora) to predation risks by various predators. Microbial Ecology, 30, 79 88.
33. Laforsch, C. Tollrian, R. (2004) Inducible defenses in multipredator environments: Cyclomorphosis in Daphnia cucullata. Ecology, 85, 2302 2311.
34. Lima, S.L. Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology, 68, 619 640.
35. Lively, C.M. (1986) Canalization versus developmental conversion in a spatially variable environment. American Naturalist, 128, 561 572.
36. McCollum, S.A. Van Buskirk, J. (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution, 50, 583 593.
37. McIntosh, A.R. Peckarsky, B.L. (1999) Criteria determining behavioural responses to multiple predators by a stream mayfly. Oikos, 85, 554 564.
38. McPeek, M.A. (1998) The consequences of changing the top predator in a food web: a comparative experimental approach. Ecological Monographs, 68, 1 23.
39. Moran, N.A. (1992) The evolutionary maintenance of alternative phenotypes. American Naturalist, 139, 971 989.
40. Nilsson, P.A., Brönmark, C. Pettersson, L.B. (1995) Benefits of a predator-induced morphology in crucian carp. Oecologia, 104, 291 296.
41. Padilla, D.K. Adolph, S.C. (1996) Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evolutionary Ecology, 10, 105 117.
42. Pettersson, L.B., Nilsson, P.A. Bronmark, C. (2000) Predator recognition and defence strategies in Crucian carp, Carassius carassius. Oikos, 88, 200 212.
43. Poitrineau, K., Brown, S.P. Hochberg, M.E. (2003) Defence against multiple enemies. Journal of Evolutionary Biology, 16, 1319 1327.
44. Poitrineau, K., Brown, S.P. Hochberg, M.E. (2004) The joint evolution of defence and inducibility against natural enemies. Journal of Theoretical Biology, 231, 389 396.
45. Relyea, R.A. (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology, 82, 523 540.
46. Relyea, R.A. (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology, 84, 1840 1848.
47. Rochette, R., Doyle, S.P. Edgell, T.C. (2007) Interaction between an invasive decapod and a native gastropod: predator foraging tactics and prey architectural defenses. Marine Ecology-Progress Series, 330, 179 188.
48. Schmitz, O.J. Sokol-Hessner, L. (2002) Linearity in the aggregate effects of multiple predators in a food web. Ecology Letters, 5, 168 172.
49. Sih, A. (1987) Predators and prey lifestyles: an evolutionary and ecological overview. Predation: Direct and Indirect Impacts on Aquatic Communities (eds W.C. Kerfoot A. Sih pp. 203 224. University Press of New England, Handover, New Hampshire.
50. Sih, A., Englund, G. Wooster, D. (1998) Emergent impacts of multiple predators on prey. Trends in Ecology & Evolution, 13, 350 355.
51. Spitze, K. Sadler, T.D. (1996) Evolution of a generalist genotype: multivariate analysis of the adaptiveness of phenotypic plasticity. American Naturalist, 148, S108 S123.
52. Sultan, S.E. Spencer, H.G. (2002) Metapopulation structure favors plasticity over local adaptation. American Naturalist, 160, 271 283.
53. Tollrian, R. (1995) Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability? Oecologia, 101, 151 155.
54. Tollrian, R. Dodson, S.I. (1999) Inducible defenses in cladocera: Constraints, costs, and multipredator environments. The Ecology and Evolution of Inducible Defenses (eds R. Tollrian C.D. Harvell pp. 177 202. Princeton, New Jersey, USA.
55. Tollrian, R. Harvell, D. (1999) The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, New Jersey, U.S.A.
56. Traw, M.B. Dawson, T.E. (2002) Reduced performance of two specialist herbivores (Lepidoptera : Pieridae, Coleoptera : Chrysomelidae) on new leaves of damaged black mustard plants. Environmental Entomology, 31, 714 722.
57. Trussell, G.C. (2000a) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution, 54, 151 166.
58. Trussell, G.C. (2000b) Predator-induced plasticity and morphological trade-offs in latitudinally separated populations of Littorina obtusata. Evolutionary Ecology Research, 2, 803 822.
59. Trussell, G.C. Smith, L.D. (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proceedings of the National Academy of Sciences of the United States of America, 97, 2123 2127.
60. Tufto, J. (2000) The evolution of plasticity and nonplastic spatial and temporal adaptations in the presence of imperfect environmental cues. American Naturalist, 156, 121 130.
61. Turner, A.M., Fetterolf, S.A. Bernot, R.J. (1999) Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail. Oecologia, 118, 242 247.
62. Van Buskirk, J. McCollum, S.A. (2000) Functional mechanisms of an inducible defence in tadpoles: Morphology and behaviour influence mortality risk from predation. Journal of Evolutionary Biology, 13, 336 347.
63. Van Buskirk, J. Relyea, R.A. (1998) Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biological Journal of the Linnean Society, 65, 301 328.
64. Van Buskirk, J. Schmidt, B.R. (2000) Predator-induced phenotypic plasticity in larval newts: trade- offs, selection, and variation in nature. Ecology, 81, 3009 3028.
65. Van Tienderen, P.H. (1991) Evolution of generalists and specialists in spatially heterogeneous environments. Evolution, 45, 1317 1331.
66. Van Tienderen, P.H. (1997) Generalists, specialists, and the evolution of phenotypic plasticity in sympatric populations of distinct species. Evolution, 51, 1372 1380.
67. Vermeij, G.J. Covich, A.P. (1978) Coevolution of freshwater gastropods and their predators. American Naturalist, 112, 833 843.
68. Via, S. (1987) Genetic constraints on the evolution of phenotypic plasticity. Genetic Constraints on Adaptive Evolution (ed V. Loeschcke pp. 47 71. Springer-Verlag, Berlin.
69. Via, S. Lande, R. (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 502 522.
70. Via, S. Lande, R. (1987) Evolution of genetic variability in a spatially heterogeneous environment: effects of genotype-environment interaction. Genetic Research, 49, 147 156.
71. Werner, E.E. Anholt, B.R. (1993) Ecological consequences of the trade-off between growth and mortality-rates mediated by foraging activity. American Naturalist, 142, 242 272.