Abstract
Studies of inducible defenses have traditionally examined prey responses to one predator at a time. However, prey in nature encounter combinations of predators that should force them to produce phenotypic compromises. We examined how snails (Helisoma trivolvis) alter their phenotype in the presence of three different predator species that were presented alone and in pairwise combinations. When snails were exposed to each predator alone, they formed predator-specific defenses that reflected the differences in each predator’s foraging mode. When snails were exposed to pairwise combinations of predators, their phenotype was dependent on their ability to detect each predator, the risk posed by each predator, and the effectiveness of a given defense against each predator. Consequently, responses to combined predators were typically biased towards one of the predators in the pair. This suggests that prey facing combined predators do not form simple intermediate defenses and, as a result, may experience enhanced mortality risk when they encounter natural predator regimes.
Similar content being viewed by others
References
Anholt BR, Skelly DK, Werner EE (1996) Factors modifying antipredator behavior in larval toads. Herpetologica 52:301–313
Brown GE, Poirier JF, Adrian JC (2004) Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues. Behav Ecol 15:810–815
Chalcraft DR, Resetarits WJ (2003) Mapping functional similarity of predators on the basis of trait similarities. Am Nat 162:390–402
Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352
DeWitt TJ (1998) Costs and limits of phenotypic plasticity: Tests with predator-induced morphology and life history in a freshwater snail. J Evol Biol 11: 465-480
DeWitt TJ, Langerhans RB (2003) Multiple prey traits, multiple predators: keys to understanding complex community dynamics. J Sea Res 49:143–155
DeWitt TJ, Robinson BW, Wilson DS (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evol Ecol Res 2:129–148
Dudley SA, Schmitt J (1996) Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. Am Nat 147:445–465
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
Griffen BD (2006) Detecting emergent effects of multiple predator species. Oecologia 148:702–709
Griffen BD, Byers JE (2006) Intraguild predation reduces redundancy of predator species in multiple predator assemblage. J Anim Ecol 75:959–966
Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86
Hoverman JT, Relyea RA (2007) How flexible is phenotypic plasticity? Developmental windows for the induction and reversal of inducible defenses. Ecology 88:693–705
Hoverman JT, Auld JR, Relyea RA (2005) Putting prey back together again: integrating predator-induced behavior, morphology, and life history. Oecologia 144:481–491
Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Kesler DK, Munns WR Jr (1989) Predation by Belostoma flumineum (Hemiptera): an important cause of mortality in freshwater snails. J North Am Benthol Soc 8:342–350
Kingsolver JG (1995a) Fitness consequences of seasonal polyphenism in western white butterflies. Evolution 49:942–954
Kingsolver JG (1995b) Viability selection on seasonally polyphenic traits: Wing melanin pattern in western white butterflies. Evolution 49:932–941
Kishida O, Nishimura K (2005) Multiple inducible defences against multiple predators in the anuran tadpole, Rana pirica. Evol Ecol Res 7:619–631
Krupa JJ, Sih A (1998) Fishing spiders, green sunfish, and a stream-dwelling water strider: male-female conflict and prey responses to single versus multiple predator environments. Oecologia 117:258–265
Kusch J (1993) Induction of defensive morphological changes in ciliates. Oecologia 94:571–575
Lima SL (1992) Life in a multipredator environment: some considerations for antipredatory vigilance. Ann Zool Fenn 29:217–226
Lively CM (1986) Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40:232–242
Matsuda H, Abrams Pa, Hori H (1993) The effect of adaptive anti-predator behavior on exploitative competition and mutualism between predators. Oikos 68:549–559
Matsuda H, Hori M, Abrams PA (1994) Effects of predator-specific defense on community complexity. Evol Ecol 8:628–638
Matsuda H, Hori M, Abrams PA (1996) Effects of predator-specific defence on biodiversity and community complexity in two-trophic-level communities. Evol Ecol 10:13–28
McCoy MW, Bolker BM, Osenberg CW, Miner BG, Vonesh JR (2006) Size correction: comparing morphological traits among populations and environments. Oecologia 148:547–554
McGarigal K, Cushman S, Stafford SG (2000) Multivariate statistics for wildlife and ecology research. Springer, New York
McIntosh AR, Peckarsky BL (1999) Criteria determining behavioural responses to multiple predators by a stream mayfly. Oikos 85:554–564
McKelvey LM, Forward RB (1995) Activation of brine shrimp nauplii photoresponses involved in diel vertical migration by chemical cues from visual and non-visual planktivores. J Plankton Res 17:2191–2206
Mirza RS, Chivers DP (2003) Response of juvenile rainbow trout to varying concentrations of chemical alarm cue: response thresholds and survival during encounters with predators. Can J Zool 81:88–95
Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989
Osenberg CW, Mittelbach GG (1989) Effects of body size on the predator-prey interaction between pumpkinseed sunfish and gastropods. Ecol Monogr 59:405–432
Peckarsky BL, McIntosh AR (1998) Fitness and community consequences of avoiding multiple predators. Oecologia 113:565–576
Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147:813–846
Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540
Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839
Relyea RA (2004) Integrating phenotypic plasticity when death is on the line: insights from predator-prey systems. In: Pigliucci M, Preston K (eds) The evolutionary biology of complex phenotypes. Oxford University Press, New York, pp 176–194
Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355
Snyder N (1967) An alarm reaction of aquatic gastropods to intraspecific extract. Memoir 403, Cornell University Agricultural Experiment Station, Ithaca, p 122
Teplitsky C, Plenet S, Joly P (2004) Hierarchical responses of tadpoles to multiple predators. Ecology 85:2888–2894
Tollrian R (1993) Neckteeth formation in Daphnia pulex as an example of continuous phenotypic plasticity: morphological effects of Chaoborus kairomone concentration and their quantification. J Plankton Res 15:1309–1318
Tollrian R, Harvell D (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton
Turner AM (1996) Freshwater snails alter habitat use in response to predation. Anim Behav 51:747–756
Turner AM, Bernot RJ, Boes CM (2000) Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails. Oikos 88:148–158
Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585
Vance-Chalcraft HD, Soluk DA, Ozburn N (2004) Is prey predation risk influenced more by increasing predator density or predator species richness in stream enclosures? Oecologia 139:117–122
Wiackowski K, Fyda J, Pajdak-Stos A, Adamus K (2003) Predator-induced morphological defence in ciliates: interclonal variation for sensitivity to the inducing factors. Oikos 100:534–540
Acknowledgements
We thank Kerry Edwards, Helena Rosenlew, Dani Rosenberger, and Nancy Schoeppner for their assistance with the experiment. Josh Auld, Craig Osenberg, Nancy Schoeppner, Stephen Tonsor, Andy Turner and several anonymous reviewers provided many helpful comments. The Conchologists of America, the Pennsylvania Academy of Science, Sigma Xi Grants-in-aid of research, the University of Pittsburgh McKinley Research Award, and the National Science Foundation provided support for this work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Craig Osenberg.
Rights and permissions
About this article
Cite this article
Hoverman, J.T., Relyea, R.A. The rules of engagement: how to defend against combinations of predators. Oecologia 154, 551–560 (2007). https://doi.org/10.1007/s00442-007-0847-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-007-0847-3