Divergent walleye (Sander vitreus)-mediated inducible defenses in the centrarchid pumpkinseed sunfish (Lepomis gibbosus)

Biological Journal of the Linnean Society

Volumn 90, Issue 1, 2007, Pages 25-36

  Januszkiewicz, Andrzej J ^a   Robinson, Beren W ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Adaptive divergence; Evolution; Phenotypic plasticity; Predation; Resource polymorphism; Selection; Sympatric divergence; Trophic polymorphism

Indexed keywords

DEFENSE MECHANISM; DIVERGENCE; MORPHOLOGY; PERCIFORM; PHENOTYPIC PLASTICITY; POLYMORPHISM; PREDATION;

CENTRARCHIDAE; LEPOMIS GIBBOSUS; PISCES; SANDER VITREUS; STIZOSTEDION VITREUM;

EID: 33846141128     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2007.00708.x     Document Type: Article

References (110)

1. Agrawal AA. 2001. Phenotypic plasticity in the interaction and evolution of species. Science 294: 321-326.
2. Amundrud JR, Faber DJ, Keast A. 1974. Seasonal succession of free-swimming perciform larvae in Lake Opinicon, Ontario. Journal of the Fisheries Research Board of Canada 31: 1661-1665.
3. Appleton RD, Palmer RA. 1988. Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proceedings of the National Academy of Sciences USA 85: 4387-4391.
4. Attayde JL, Hansson L. 2001. Fish mediated nutrient recycling and the trophic cascade in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58: 1924-1931.
5. Beacham JL. 1988. The relative importance of body size and aggressive experience as determinants of dominance in pumpkinseed sunfish, Lepomis gibbosus. Animal Behavior 36: 621-623.
6. Bernatchez L, Wilson CC. 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Molecular Ecology 7: 431-452.
7. Blanckenhorn WU. 1992. Group size and the cost of agonistic behavior in pumpkinseed sunfish. Ethology, Ecology and Evolution 4: 255-271.
8. Bolding B, Bonar SA, Marc D. 1998. Walleye diet in a shallow impoundment: relative importance of pumpkinseed sunfish and yellow perch. Journal of Freshwater Ecology 13: 9-14.
9. Brönmark C, Miner JG. 1992. Predator-induced phenotypical change in body morphology in crucian carp. Science 258: 1348-1350.
10. Brönmark C, Pettersson LB. 1994. Chemical cues from piscivores induce a change in morphology in crucian carp. Oikos 70: 396-402.
11. Brönmark C, Pettersson LB, Nilsson PA. 1999. Predatorinduced defense in crucian carp. In: Tollrian R, Harvell CD, eds. The ecology and evolution of inducible defenses. Princeton: Princeton University Press, 203-217.
12. Brown GE, Brennan S. 2000. Chemical alarm signals in juvenile green sunfish (Lepomis cyanellus, Centrarchidae). Copeia 4: 1079-1082.
13. Brown GE, Chivers DP, Smith RJF. 1995. Fathead minnows avoid conspecific and heterospecific alarm pheromones in the feces of northern pike. Journal of Fish Biology 47: 387-393.
14. Brown GE, Golub JL, Plata DL. 2001. Attack cone avoidance during predator inspection visits by wild finescale dace (Phoxinus neogaeus): the effects of predator diet. Journal of Chemical Ecology 27: 1657-1666.
15. Brown J, Wilson EO. 1956. Character displacement. Systematic Zoology 5: 49-64.
16. Brown GE, Zachar MM. 2002. Chemical predator inspection in a characin fish (Hemingrammus erythrozonus, Characidae, Ostariophysi): the effects of mixed predator diets. Ethology 108: 451-461.
17. Chipps SR, Dunbar JA, Wahl DH. 2004. Phenotypic variation and vulnerability to predation in juvenile bluegill sunfish (Lepomis macrochirus). Oecologia 138: 32-38.
18. Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM. 2001. Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Canadian Journal of Zoology 79: 867-873.
19. Chivers DP, Smith RJF. 1998. Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5: 338-352.
20. Cote IM. 1995. Effects of predatory crab effluent on byssus production in mussels. Journal of Experimental Marine Biology and Ecology 188: 233-241.
21. DeWitt TJ. 1998. Costs and limits of phenotypic plasticity: tests with predator-induced morphology and life history in a freshwater snail. Journal of Evolutionary Biology 11: 465-480.
22. Dill LM. 1983. Adaptive flexibility in the foraging behavior of fishes. Canadian Journal of Fisheries and Aquatic Sciences. 40: 398-408.
23. Dzialowski AR, Lennon JT, O'Brien WJ, Smith VH. 2003. Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Journal of Freshwater Biology 48: 1593-1602.
24. Ehlinger TJ. 1990. Habitat choice and phenotype-limited feeding efficiency in bluegill: individual differences and trophic polymorphism. Ecology 71: 886-896.
25. Ehlinger TJ, Wilson DS. 1988. Complex polymorphism in bluegill sunfish. Proceedings of the National Academy of Sciences USA 85: 1878-1882.
26. Ehrlich PR, Raven PH. 1969. Differentiation of populations. Science 165: 1228-1232.
27. Einfalt LM, Wahl DH. 1997. Prey selection by juvenile walleye as influenced by prey morphology and behavior. Canadian Journal of Fisheries and Aquatic Sciences 54: 2618-2626.
28. Endler JA. 1977. Geographic variation, speciation, and clines. Princeton: Princeton University Press.
29. Endler JA. 1995. Multiple-trait coevolution and environmental gradients in guppies. Trends in Ecology and Evolution 10: 22-29.
30. Gabriel W. 1999. Evolution of reversible plastic responses: inducible defenses and environmental tolerance. In: Tollrian R, Harvell CD, eds. The ecology and evolution of inducible defenses. Princeton: Princeton University Press, 286-305.
31. Gilbert JJ. 1966. Rotifer ecology and embryological induction. Science 151: 1234-1237.
32. Gillespie GJ, Fox MG. 2003. Morphological and life-history differentiation between littoral and pelagic forms of pumpkinseed. Journal of Fish Biology 62: 1099-1115.
33. Grand TC, Dill LM. 1999. Predation risk, unequal competitors and the ideal free distribution. Evolutionary Ecology Research 1: 389-409.
34. Grant JWG, Bayly IAE. 1981. Predator induction of crests in morphs of the Daphnia carinata King complex. Limnology and Oceanography 26: 201-218.
35. Hanson JM, Qadrio SU. 1984. Feeding ecology of age 0 pumpkinseed (Lepomis gibbosus) and black crappie (Pomosix nigromaculatus) in the Ottawa river. Canadian Journal of Zoology 62: 613-621.
36. Harvell CD. 1986. The ecology and evolution of inducible defenses in a marine bryozoan: cues, costs, and consequences. The American Naturalist 128: 810-823.
37. Harvell CD. 1990. The ecology and evolution of inducible defenses. Quarterly Review of Biology 65: 323-340.
38. Hoyle JA, Keast A. 1987. The effect of prey morphology and size on handling time in a piscivore, the largemouth bass (Micropterus salmoides). Canadian Journal of Zoology 65: 1972-1977.
39. Hubbs CL, Lagler KF. 1941. Guide to the fishes of the Great lakes and tributary waters. Cranbrook Institute of Science Bulletin 18: 1-100.
40. Jastrebski CJ, Robinson BW. 2004. Natural selection and the evolution of replicated trophic polymorphisms in pumpkinseed sunfish (Lepomis gibbosus). Evolutionary Ecology Research 6: 285-305.
41. Jeffries MJ, Lawton JH. 1984. Enemy free space and the structure of ecological communities. Biological Journal of the Linnean Society 23: 269-286.
42. Johansson F, Samuelsson L. 1994. Fish-induced variation in abdominal spine length of Leucorrhinia dubia (Odonata) larvae? Oecologia 100: 74-79.
43. Johansson F, Wahlstrom E. 2002. Induced morphological defense: evidence from whole-lake manipulation experiments. Canadian Journal of Zoology 80: 199-206.
44. Johnson JB. 2001. Adaptive life-history evolution in the livebearing fish Brachyrhaphis rhabdophora: genetic basis for parallel divergence in age and size at maturity and a test of predator induced plasticity. Evolution 55: 1486-1491.
45. Johnson JB, Belk MC. 2001. Predation environment predicts divergent life-history phenotypes among populations of the livebearing fish Brachyrhaphi rhabdophora. Oecologia 126: 142-149.
46. Johnson BL, Smith DL, Carline RF. 1988. Habitat preferences, survival, growth, foods, and harvests of walleyes and walleye X sauger hybrids. North American Journal of Fisheries Management 8: 292-304.
47. Kerfoot WC, Sih A. 1987. Predation: direct and indirect impacts on aquatic communities. Hanover, NH: University Press of New England.
48. Kiesecker JM, Chivers DP, Anderson M, Blaustein AR. 2002. Effect of predator diet on life history shifts of red-legged frogs, Rana aurora. Journal of Chemical Ecology 28: 1007-1015.
49. Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ. 2004. Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58: 2305-2318.
50. Leduc AOHC, Noseworthy MK, Adrian JC, Brown GE. 2003. Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions. Journal of Fish Biology 63: 1331-1336.
51. Lemly AD, Dimmick JF. 1982. Growth of young-of-the-year and yearling Centrarchids in relation to zooplankton in the littoral zone of lakes. Copeia 1982: 305-321.
52. Leonard GH, Bertness MD, Yund PO. 1999. Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80: 1-14.
53. Levins R. 1968. Evolution in changing environments. Princeton: Princeton University Press.
54. Lima SL, Dill LM. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68: 619-640.
55. Lyons J. 1987. Prey choice among piscivorous juvenile walleyes (Stizostedion vitreum). Canadian Journal of Fisheries and Aquatic Sciences 44: 758-764.
56. Magurran A, Seghers BH, Carbalho GR, Shaw PW. 1993. Evolution of adaptive variation in antipredator behavior. Marine and Freshwater Behavior and Physiology 23: 29-44.
57. Marcus JP, Brown GE. 2003. Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration. Canadian Journal of Zoology 81: 1671-1677.
58. Mathis A, Smith RJF. 1993. Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behavioral Ecology 4: 260-265.
59. McCairns SRJ, Fox MG. 2004. Habitat and home range fidelity in a trophically dimorphic pumpkinseed sunfish (Lepomis gibbosus) population. Oecologia 140: 271-279.
60. McPeek MA. 1997. Measuring phenotypic selection on an adaptation: lamellae of damselflies experiencing dragonfly predation. Evolution 51: 459-466.
61. McPeek MA, Schrot AK, Brown JM. 1996. Adaptation to predators in a new community: swimming performance and predator avoidance in damselflies. Ecology 77: 617-629.
62. Mirza RS, Chivers DP. 2002. Brook charr (Salvelinus fontinalis) can differentiate chemical alarm cues produced by different age/classes of conspecifics. Journal of Chemical Ecology 28: 555-564.
63. Mittelbach GG. 1984. Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65: 499-513.
64. Mittelbach GG, Osenberg CW, Wainwright PC. 1999. Variation in feeding morphology between pumpkinseed populations: Phenotypic plasticity or evolution? Evolutionary Ecology Research 1: 111-128.
65. Moyle PB, Cech JJ. 2004. Fishes: an introduction to ichthyology. Harlow: Prentice Hall.
66. Nelson JS, Crossman EJ, Espinosa-Perez H, Findley LT, Gilbert CR, Lea RN, Williams JD. 2003. The 'names of fishes' list, including recommended changes in fish names: Chinook salmon for chinook salmon, and Sander to replace Stizostedion for the sauger and walleye. Fisheries 28: 38-39.
67. Nilsson PA, Brönmark C, Pettersson LB. 1995. Benefits of a predator-induced morphology in crucian carp. Oecologia 104: 291-296.
68. Reimchen TE. 1991. Evolutionary attributes of headfirst prey manipulation and swallowing in piscivores. Canadian Journal of Zoology 69: 2912-2916.
69. Reimchen TE, Nosil P. 2004. Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58: 1274-1281.
70. Relyea RA. 2002. Costs of phenotypic plasticity. American Naturalist 159: 272-282.
71. Relyea RA. 2003. Predators come and predators go: the reversibility of predator-induced traits. Ecology 84: 1840-1848.
72. Reznick DA, Bryga H, Endler JA. 1990. Experimentally induced life-history evolution in a natural population. Nature 346: 357-359.
73. Reznick DA, Butler MJ, Rodd H. 2001. Life-history evolution in guppies. VII. The comparative ecology of high- and low- predation environments. American Naturalist 157: 126-140.
74. Reznick DA, Endler JA. 1982. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36: 160-177.
75. Robinson BW, Parsons KJ. 2002. Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1819-1833.
76. Robinson BW, Schluter D. 2000. Natural selection and the evolution of adaptive genetic variation in northern freshwater fishes. In: Mousseau TA, Sinervo B, Endler JA, eds. Adaptive genetic variation in the wild. New York: Oxford University Press, 65-94.
77. Robinson BW, Wilson DS. 1994. Character release and displacement in fishes: a neglected literature. American Naturalist 144: 596-627.
78. Robinson BW, Wilson DS. 1996. Genetic variation and phenotypic plasticity in a trophically polymorphic population of pumpkinseed sunfish (Lepomis gibbosus). Evolutionary Ecology 10: 631-652.
79. Robinson BW, Wilson DS, Margosian AS. 2000. A pluralistic analysis of character release in pumpkinseed sunfish (Lepomis gibbosus). Ecology 81: 2799-2812.
80. Robinson BW, Wilson DS, Margosian AS, Lotito PT. 1993. Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evolutionary Ecology 7: 451-464.
81. Sadzikowski MR, Wallace DC. 1976. A comparison of the food habits of size classes of three sunfishes (Lepomis macrochirus Rafinesque, L. gibbosus (Linnaeus) and L. cyanellus Rafinesque). American Midland Naturalist 95: 220-225.
82. Savino JF, Stein RA. 1982. Predator-prey interactions between largemouth bass and bluegills as influenced by simulated submersed vegetation. Transactions of the American Fisheries Society 111: 255-266.
83. Savino JF, Stein RA. 1989a. Behavior of fish predators and their prey: habitat choice between open water and dense vegetation. Environmental Biology of Fishes 24: 287-293.
84. Savino JF, Stein RA. 1989b. Behavioural interactions between fish predators and their prey: effects of plant density. Animal Behavior 37: 311-321.
85. Schindler DE, Scheuerell MD. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177-189.
86. Schlichting C, Pigliucci M. 1998. Phenotypic evolution: a reaction norm perspective. Boston: Sunderland.
87. Schluter D. 2000. The ecology of adaptive radiation. Oxford: Oxford University Press.
88. Schluter D. 2001. Ecology and the origin of species. Trends in Ecology and Evolution 16: 372-380.
89. Scott WB, Crossman EJ. 1998. Freshwater fishes of Canada. Oakville: Galt House Publications.
90. Skelly DK. 1992. Field evidence for a cost of behavioral antipredator response in a larval amphibian. Ecology 73: 704-708.
91. Skulason S, Smith TB. 1995. Resource polymorphisms in vertebrates. Trends in Ecology and Evolution 10: 366-370.
92. Smith ME, Belk MC. 2001. Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behavioral Ecology and Sociobiology 51: 101-107.
93. Smith GR, Todd TN. 1984. Evolution of fish species flocks of fishes in north temperate lakes. In: Echelle AA, Kornfield I, eds. The evolution of fish species flocks. Orono: University of Maine Press, 45-68.
94. Spencer RJ, Thompson MB. 2003. The significance of predation in nest site selection in turtles: an experimental consideration of macro- and microhabitat preferences. Oikos 102: 592-600.
95. Stabell OB, Lwin MS. 1997. Predator-induced phenotypic changes in crucian carp are caused by chemical signals for conspecifics. Environmental Biology of Fishes 49: 145-149.
96. Stearns SC. 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436-445.
97. Strauss SY, Agrawal AA. 1999. Ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution 14: 179-185.
98. Svanback R. 2004. Ecology and evolution of adaptive morphological variation in fish populations. PhD Thesis, Umea University, Umea, Sweden.
99. Tollrian R, Harvell CD. 1999. The evolution of inducible defenses: current ideas. In: Tollrian R, Harvell CD, eds. The ecology and evolution of inducible defenses. Princeton: Princeton University Press, 306-321.
100. Van Buskirk J, McCollum SA. 2000. Functional mechanisms of an inducible defense in tadpoles: morphology and behaviour influence mortality risk from predators. Journal of Evolutionary Biology 13: 336-347.
101. Vanni MJ, Layne CD, Arnott SE. 1997. 'Top down' trophic interactions in lakes: effects of fish on nutrient dynamics. Ecology 78: 1-20.
102. Wahl DH, Stein RA. 1988. Selective predation by three esocides: the role of prey behavior and morphology. Transactions of the American Fisheries Society 117: 142-151.
103. Webb PW. 1983. Speed, acceleration and maneuverability of two teleost fishes. Journal of Experimental Biology 102: 115-122.
104. Webb PW. 1984. Body and fin form and strike tactics of four teleost predators attacking fathead minnow (Pimephales promelas) prey. Canadian Journal of Fisheries and Aquatic Sciences 41: 157-165.
105. Webb PW. 1986. Effect of body form and response threshold on the vulnerability of four species of teleost prey attacked by largemouth bass (Micropterus salmoides). Canadian Journal of Fisheries and Aquatic Sciences 43: 763-771.
106. Weese DJ. 2004. Tests of replicated phenotypic divergence in polymorphic pumpkinseed sunfish, Lepomis gibbosus, using microsatellite markers. MSc Thesis, University of Guelph, Guelph, Canada.
107. Werner EE. 1986. Species interactions in freshwater fish communities. In: Diamond J, Case TJ, eds. Community ecology. New York: Harper & Row Publishers, 344-358.
108. Werner EE, Gilliam JF, Hall DJ, Mittelbach GG. 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64: 1540-1548.
109. West-Eberhard MJ. 1989. Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20: 249-278.
110. Yoshioka PM. 1982. Predator-induced polymorphism in the bryozoan Membranipora membranacea (L.). Journal of Experimental Marine Biology and Ecology 61: 233-242.