EVOLUTION OF PREY BEHAVIOR IN RESPONSE TO CHANGES IN PREDATION REGIME: DAMSELFLIES IN FISH AND DRAGONFLY LAKES
R. Stoks
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Laboratory of Aquatic Ecology, University of Leuven, Ch. De Beriotstraat 32, B-3000 Leuven, Belgium E-mail: [email protected]
Search for more papers by this authorM. A. McPeek
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Corresponding author. E-mail: [email protected].
Search for more papers by this authorJ. L. Mitchell
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Department of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109; E-mail: [email protected].
Search for more papers by this authorR. Stoks
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Laboratory of Aquatic Ecology, University of Leuven, Ch. De Beriotstraat 32, B-3000 Leuven, Belgium E-mail: [email protected]
Search for more papers by this authorM. A. McPeek
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Corresponding author. E-mail: [email protected].
Search for more papers by this authorJ. L. Mitchell
Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755
Department of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109; E-mail: [email protected].
Search for more papers by this authorAbstract
Abstract In a large behavioral experiment we reconstructed the evolution of behavioral responses to predators to explore how interactions with predators have shaped the evolution of their prey—behavior. All Enallagma damselfly species reduced both movement and feeding in the presence of coexisting predators. Some Enallagma species inhabit water bodies with both fish and dragonflies, and these species responded to the presence of both predators, whereas other Enallagma species inhabit water bodies that have only large dragonflies as predators, and these species only responded to the presence of dragonflies. Lineages that shifted to live with large dragonflies showed no evolution in behaviors expressed in the presence of dragonflies, but they evolved greater movement in the absence of predators and greater movement and feeding in the presence of fish. These results suggest that Enallagma species have evolutionarily lost the ability to recognize fish as a predator. Because species coexisting with only dragonfly predators have also evolved the ability to escape attacking dragonfly predators by swimming, the decreased predation risk associated with foraging appears to have shifted the balance of the foraging/predation risk trade-off to allow increased activity in the absence of mortality threats to evolve in these lineages. Our results suggest that evolution in response to changes in predation regime may have greater consequences for characters expressed in the absence of mortality threats because of how the balance between the conflicting demands of growth and predation risk are altered.
Literature Cited
- Abrams, P. A. 1991. Life-history and the relationship between food availability and foraging effort. Ecology. 72: 1242–1252.
- Anholt, B. R., E. E. Werner, and D. K. Skelly 2000. Effect of food and predators on the activity of four larval ranid frogs. Ecology. 81: 3509–3521.
- Baker, R. L. 1981. Behavioral interactions and use of feeding areas by nymphs of Coenagrion resolutum (Coenagrionidae, Odonata) Oecologia 49: 353–358.
- Baker, R. L., C. M. Elkin, and H. A. Brennan 1999. Aggressive interactions and risk of fish predation for larval damselflies. J. Insect. Behav.. 12: 213–223.
- Berger, J. 1999. Antropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose, and ravens. Proc. R. Soc. Lond. B. 266: 2261–2267.
- Berger, J., J. E. Swenson, and I.-L. Persson 2001. Recolonizing carnivores and nä?ve prey: conservation lessons from Pleistocene extinctions. Science. 291: 1036–1039.
- Breden, F., M. Scott, and E. Michel 1987. Genetic differentiation for anti-predator behaviour in the Trinidad guppy, Poecilia reticulata. Anim. Behav.. 35: 618–620.
- Brodie, E. D., 1992. Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution. 46: 1284–1298.
- Brodie, E. D., 1993. Homogeneity of the genetic variance-covari-ance matrix for antipredator traits in two natural-populations of the garter snake Thamnophis ordinoides. Evolution. 47: 844–854.
-
Brown, C. J. D., and
R. C. Ball
1942. A fish population study of Third Sister Lake.
Trans. Am. Fish. Soc.. 72: 177–186.
10.1577/1548-8659(1942)72[177:AFPSOT]2.0.CO;2 Google Scholar
- Brown, J. M., M. A. McPeek and M.L. May 2000. A phylogenetic perspective on habitat shifts and diversity in the North American Enallagma damselflies. Syst. Biol.. 49: 697–712.
- Chivers, D. P., B. D. Wisenden, and R. J. F. Smith 1996. Damselfly larvae learn to recognize predators from chemical cues in the predator's diet. Anim. Behav.. 52: 315–320.
- Cooper, E. L., C. C. Wagner, and G. E. Krantz 1971. Bluegills dominate production in a mixed population of fishes. Ecology. 52: 280–290.
- Coss, R. G. 1999. Effects of relaxed natural selection on the evolution of behavior. Pp. 180–208 in S. A. Foster, and J. A. Endler, eds Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford Univ. Press, Oxford , U.K .
- Cousyn, C., L. de Meester, J. K. Colbourne, L. Brendonck, D. Verschuren, and F. Volckaert 2001. Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc. Natl. Acad. Sci. USA. 98: 6256–6260.
- de Meester, L. 1996. Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical par-thenogen, Daphnia magna. Evolution. 50: 1293–1298.
- Diehl, S., S. D. Cooper, K. W. Kratz, R. M. Nisbet, S. K. Roll, S. W. Wiseman, and T. M. Jenkins 2000. Effects of multiple, predator-induced behaviors on short-term producer-grazer dynamics in open systems. Am. Nat.. 156: 293–313.
- Downes, S. J., and M. Adams 2001. Geographic variation in antisnake tactics: the evolution of scent-mediated behavior in a lizard. Evolution. 55: 605–615.
- Edmunds, M. 1974. Defense in animlas: a survey of anti-predator defenses. Longman Press, London .
- Eklov, P., and L. Persson 1996. The response of prey to the risk of predation: proximate cues for refuging juvenile fish. Anim. Behav.. 51: 105–115.
- Elkin, C. M., and R. L. Baker 2000. Lack of preference for low-predation-risk habitats in larval damselflies explained by costs of intraspecific interactions. Anim. Behav.. 60: 511–521.
- Endler, J. A. 1986. Defense against predators. Pp. 109–134 in M. E. Feder and G. V. Lauder, eds. Predator-prey relationships. Univ. of Chicago Press, Chicago , IL .
- Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat.. 125: 1–15.
- 1988. Phylogenies and quantitative characters. Annu. Rev. Ecol. Syst.. 19: 445–471.
- Hagen, H. A. 1861. Synopsis of the Neuroptera of North America, with a list of the South American species. Smithson. Misc. Collect.. 4: 1–347.
-
Hasagawa, M.,
H. Kishino, and
T. Yano
1985. Dating of the human-ape splitring by a molecular clock of mitochondrial DNA.
J. Mol. Evol.. 21: 160–174.
10.1007/BF02101694 Google Scholar
- Hooper, K. R. 2001. Flexible antipredator behavior in a dragonfly species that coexists with different predator types. Oikos. 93: 470–476.
- Jakobsson, S., O. Brick, and C. Kullberg 1995. Escalated fighting behavior incurs increased predation risk. Anim. Behav. 49: 235–239.
- Jeffries, M. 1990. Interspecific differences in movement and hunting success in damselfly larvae (Zygoptera: Insects): responses to prey availability and predation threat. Freshwater Biol. 23: 191–196.
- Johansson, F., R. Stoks, L. Rowe, and M. de Block 2001. Life history plasticity in a damselfly: effects of combined time and biotic constraints. Ecology. 82: 1857–1869.
- Johnson, D. M., and P. H. Crowley 1980. Habitat and seasonal segregation among coexisting odonate larvae. Odonatologica. 9: 297–308.
- Juliano, S. A., and M. E. Gravel 2002. Predation and the evolution of prey behavior: an experiment with tree hole mosquitos. Behav. Ecol.. 13: 301–311.
- Knapp, R. A., K. R. Matthews, and O. Sarnelle 2001. Resistance and resilience of alpine lake fauna to fish introductions. Ecol. Monogr.. 71: 401–421.
- Kohler, S. L., and M. A. McPeek 1989. Predation risk and the foraging behavior of competing stream insects. Ecology. 70: 1811–1825.
- Lima, S. L. 1998. Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv. Study Behav.. 27: 215–290.
- Lima, S. L., and L. M. Dill 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 619–640.
- Magurran, A. E., B. H. Seghers, G. R. Carvalho, and P. W. Shaw 1992. Behavioral consequences of an artificial introduction of guppies (Poecilia reticulata) in North Trinidad: evidence for the evolution of antipredator behavior in the wild. Proc. R. Soc. Lond. B. 248: 117–122.
- Martins, E. P., and T. Garland, Jr. 1991. Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution. 45: 534–557.
- McPeek, M. A. 1990a. Behavioral differences between Enallagma species (Odonata) influencing differential vulnerability to predators. Ecology. 71: 1714–1726.
- 1990b. Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology. 71: 83–98.
- 1995a. Morphological evolution mediated by behavior in the damselflies of two communities. Evolution. 49: 749–769.
- 1995b. Testing hypotheses about evolutionary change on single branches of a phylogeny using evolutionary contrasts. Am. Nat.. 145: 686–703.
- 1997. Measuring phenotypic selection on adoptation: lamellae of damselflies experiencing dragonfly predation. Evolution. 51: 459–466.
- 1998. The consequences of changing the top predator in a food web: a comparative experimental approach. Ecol. Monogr.. 68: 1–23.
- 1999. Biochemical evolution associated with antipredator adaptation in damselflies. Evolution. 53: 1835–1845.
- 2000. Predisposed to adapt Cladelevel differences in characters affecting swimming performance in damselflies Evolution. 54: 2072–2080.
- McPeek, M. A., and J. M. Brown 2000. Building a regional species pool: diversification of the Enallagma damselflies in eastern North American waters. Ecology. 81: 904–920.
- McPeek, M. A., A. K. Schrot, and J. M. Brown 1996. Adaptation to predators in a new community: Swimming performance and predator avoidance in damselflies. Ecology. 77: 617–629.
- McPeek, M. A., M. Grace, and J. M. L. Richardson 2001. Physiological and behavioral responses to predators shape the growth/ predation risk trade-off in damselflies. Ecology. 82: 1535–1545.
- Morin, P. J. 1984a. Odonate guild composition: experiments with colonization history and fish predation. Ecology. 65: 1866–1873.
- Morin, P. J. 1984b. The impact of fish exclusion on the abundance and species composition of larval odonates: results of short-term experiments in a North Carolina farm pond. Ecology. 65: 53–60.
- Morrison, D. F. 1990. Multivatiate statistical methods. 3rd ed. McGraw-Hill, New York .
- Osenberg, C. W., E. E. Werner, G. G. Mittelbach and D. J. Hall 1988. Growth patterns in bluegill (Lepomis macrochirus) and pumpkinseed (L. gibbosus) sunfish: environmental variation and the importance of ontogenetic niche shifts. Can. J. Fish. Aquat. Sci.. 45: 17–26.
- O'Steen, S., A. J. Cullum, and A. F. Bennett 2002. Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata). Evolution. 56: 776–784.
- Peacor, S. D., and E. E. Werner 1997. Trait-mediated indirect interactions in a simple aquatic food web. Ecology. 78: 1146–1156.
- 2000. Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology. 81: 1998–2010.
- Peckarsky, B. L. 1996. Alternative predator avoidance syndromes in stream-dwelling mayflies. Ecology. 77: 1888–1905.
- Peckarsky, B. L., C. A. Cowan, M. A. Penton, and C. Anderson 1993. Sublethal consequences of predator-avoidance by stream-dwelling mayfly larvae to adult fitness. Ecology. 74: 1836–1846.
- Pierce, C. L., P. H. Crowley, and D. M. Johnson 1985. Behavior and ecological interactions of larval Odonata. Ecology. 66: 1504–1512.
- Purvis, A., and T. Garland, Jr. 1993. Polytomies in comparative analyses of continuous characters. Syst. Biol.. 42: 569–575.
- Relyea, R. A. 2000. Trait-mediated indirect effects in larval anurans: Reversing competition with the threat of predation. Ecology. 81: 2278–2289.
- 2001. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology. 82: 523–540.
- Relyea, R. A., and E. E. Werner 1999. Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology. 80: 2117–2124.
- Richardson, J. M. L. 2001a. A comparative study of activity levels in larval anurans and response to the presence of different predators. Behav. Ecol.. 12: 51–58.
- 2001b. The relative roles of adaptation and phylogeny in determination of larval traits in diversifying anuran lineages. Am. Nat.. 157: 282–299.
- Richardson, J. M. L., and B. R. Anholt 1995. Ontogenetic behaviour changes in larvae of the damselfly Ischnura verticalis (Odonata: Coenagrionidae). Ethology. 101: 308–334.
- Richardson, J. M. L., and R. L. Baker 1996. Function of abdomen wave behavior in larval Ischnura verticalis (Odonata: Coena-grionidae). J. Ins. Behav.. 9: 183–195.
- Riechert, S. E., and A. Hedrick 1990. Levels of predation and genetically based anti-predator behavior in the spider, Agelen-opsis aperta. Anim. Behav.. 40: 679–687.
- SAS Institute, Inc. 1990. SAS/STAT User's Guide, Version 6, Fourth Edition, Volume 2. Cary, North Carolina .
- Schmitz, O. J., and K. B. Suttle 2001. Effects of top predator species on direct and indirect interactions in a food web. Ecology. 82: 2072–2081.
- Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. Pages 203–224 in W. C. Kerfoot and A. Sih (eds.), Predation: direct and indirect impacts on aquatic communities. University of New England Press, Hanover , New Hampshire , USA .
- 1992. Prey uncertainty and the balancing of antipredator and feeding needs. Am. Nat.. 139: 1052–1069.
- Sih, A., L. B. Kats, and E. F. Maurer 2000. Does phylogenetic inertia explain the evolution of ineffective antipredator behavior in a sunfish-salamander system Behav Ecol. Sociobiol. 49: 48–56.
- Skelly, D. K. 1992. Field evidence for a cost of behavioral anti-predator response in a larval amphibian. Ecology. 73: 704–708.
- Skelly, D. K., and E. E. Werner 1990. Behavioral and life-historical responses of larval american toads to an odonate predator. Ecology. 71: 2313–2322.
- Sokal, R. R., and F. J. Rohlf 1995. Biometry: third edition. W. H. Freeman and Co., New York .
- Steiner, C., B. Siegert, S. Schulz, and F. Suhling 2000. Habitat selection in the larvae of two species of Zygoptera (Odonata): biotic interactions and abiotic limitation. Hydrobiologia. 427: 167–176.
- Stoks, R., and M. de Block 2000. The influence of predator species and prey age on the immediate survival value of antipredator behaviours in a damselfly. Arch. Hydrobiol.. 147: 417–430.
- Stoks, R., and F. Johansson 2000. Trading off mortality risk against foraging effort in damselflies that differ in life cycle length. Oikos. 91: 559–567.
- Storfer, A., and A. Sih 1998. Gene flow and ineffective antipredator behavior in a stream-breeding salamander. Evolution. 52: 558–565.
- Turgeon, J., and M. A. McPeek 2002. Phylogeographic analyses of a recent radiation of Enallagma damselflies (Odonata: Coen-agrionidae). Mol. Ecol.. 11: 1989–2002.
- van Buskirk, J., S. A. McCollum, and E. E. Werner 1997. Natural selection for environmentally induced phenotypes in tadpoles. Evolution. 51: 1983–1992.
- Watkins, T. B. 1996. Predator-mediated selection on burst swimming performance in tadpoles of the Pacific tree frog, Pseudacris regilla. Physiol. Zool.. 69: 154–167.
- 2001. A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla. Evolution. 55: 1668–1677.
- Werner, E. E., and B. R. Anholt 1993. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am. Nat.. 142: 242–272.
- 1996. Predator-induced behavioral indirect effects in anuran larvae. Ecology. 77: 157–169.
- Werner, E. E., and J. F. Gilliam 1984. The ontogenetic niche and species interactions in size-structured populations. Annu. Rev. Ecol. Syst.. 15: 393–425.
- Werner, E. E., and M. A. McPeek 1994. The roles of direct and indirect effects on the distributions of two frog species along an environmental gradient. Ecology. 75: 1368–1382.
- Wisenden, B. D., D. P. Chivers, and R. J. F. Smith 1997. Learned recognition of predation risk by Enallagma damselfly larvae (Odonata, Zygoptera) on the basis of chemical cues. J. Chem. Ecol.. 23: 137–151.