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Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology?

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Abstract

Inducible defences have long been considered as a polyphenism opposing defended and undefended morphs. However, in nature, preys are exposed to various levels of predation risk and scale their investment in defence to actual predation risk. Still, among the traits that are involved in the defence, some are specific to one predator type while others act as a more generalised defence. The existence of defence costs could prevent an individual investing in all these traits simultaneously. In this study, we investigate the impact of an increasing level of predator density (stickleback, Gasterosteus aculeatus) on the expression of morphological inducible defences in tadpoles of Rana dalmatina. In this species, investment in tail length and tail muscle is a stickleback-specific response while increased tail fin depth is a more general defence. As expected, we found a relationship between investment in defence and level of risk through the responses of tail fin depth and tail length. We also found an exponential increase of defence cost, notably expressed by convex decrease of growth and developmental rates. We found a relative independence of investment in the different traits that compose the defence, revealing a high potential for fine tuning the expression of defended phenotypes with respect to local ecological conditions.

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References

  • Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882

    PubMed  Google Scholar 

  • Anholt BR, Skelly DK, Werner EE (1996) Factors modifying antipredator behavior in larval toads. Herpetologica 52:301–313

    Google Scholar 

  • Barata C, Baird DJ, Soares A (2001) Phenotypic plasticity in Daphnia magna straus: variable maturation instar as an adaptive response to predation pressure. Oecologia 129:220–227

    Article  Google Scholar 

  • Berven KA (1990) Factors affecting populations fluctuations in larval and adult stages of the woodfrog (Rana sylvatica). Ecology 71:1599–1608

    Article  Google Scholar 

  • Boersma M, Spaak P, DeMeester L (1998) Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: The uncoupling of responses. Am Nat 152:925–927

    Article  Google Scholar 

  • Dahl J, Peckarsky BL (2002) Induced morphological defenses in the wild: predator effects on a mayfly, Drunella coloradensis. Ecology 83:1620–1634

    Google Scholar 

  • DeWitt TJ, Sih A, Hucko JA (1999) Trait compensation and cospecialisation in a freshwater snail: size, shape and antipredator behaviour. Anim Behav 58:397–407

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proc R Soc Lond B 266:1549–1553

    Article  Google Scholar 

  • Goater CP (1994) Growth and survival of postmetamorphic toads—interactions among larval history, density, and parasitism. Ecology 75:2264–2274

    Article  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340

    Article  PubMed  CAS  Google Scholar 

  • Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86

    Article  Google Scholar 

  • Horat P, Semlitsch RD (1994) Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav Ecol Sociobiol 34:393–401

    Article  Google Scholar 

  • Joly P, Morand A (1994) Theoretical habitat templets, species traits, and species richness: amphibian in the Upper Rhône and its floodplain. Freshw Biol 31:455–468

    Article  Google Scholar 

  • Komers PE (1997) Behavioural plasticity in variable environments. Can J Zool 75:161–169

    Google Scholar 

  • Lardner B (2000) Morphological and life history response to predators in larvae of seven anurans. Oikos 88:169–180

    Article  Google Scholar 

  • Laurila A, Järvi-Laturi M, Pakkasmaa S, Merilä J (2004) Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences. Oikos 107:90–99

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Magurran A, Nowak MA (1991) Another battle of sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poecilia reticulata. Proc R Soc Lond B 246:31–38

    Article  CAS  Google Scholar 

  • Nesbitt LM, Riessen HP, Ramcharan CW (1996) Opposing predation pressures and induced vertical migration responses in Daphnia. Limnol Oceanogr 41:1306–1311

    Article  Google Scholar 

  • Petterson LB, Brönmark C (1997) Density-dependent costs of an inducible morphological defense in crucian carp. Ecology 78:729–736

    Google Scholar 

  • Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540

    Article  Google Scholar 

  • Relyea RA (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology 84:1840–1848

    Article  Google Scholar 

  • Relyea RA (2004) Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85:172–179

    Article  Google Scholar 

  • Riessen HP (1999) Predator-induced life history shifts in Daphnia: a synthesis of studies using meta-analysis. Can J Fish Aquat Sci 56:2487–2494

    Article  Google Scholar 

  • SAS Institute Inc (1999) SAS OnlineDoc, Version 8. SAS Institute Inc, Cary

  • Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350

    Article  Google Scholar 

  • Smith LD, Jennings JA (2000) Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes. Mar Biol 136:461–469

    Article  Google Scholar 

  • Teplitsky C, Plénet S, Joly P (2003) Tadpoles responses to the risk of fish introduction. Oecologia 134:270–277

    PubMed  CAS  Google Scholar 

  • Teplitsky C, Plénet S, Léna J-P, Malet E, Joly P (2005) Escape behaviour and ultimate causes of specific induced defenses in an anuran tadpole. J Evol Biol 18:180–190

    Article  PubMed  CAS  Google Scholar 

  • Tollrian R (1993) Necteeth formation in Daphnia pulex as an example of continuous plasticity Morphological effects of Chaoborus kairomones concentration and their quantification. J Plankton Res 15:1309–1318

    Article  Google Scholar 

  • Tollrian R, Dodson S (1999) Inducible defenses in cladocera: constraints, costs and multiple predator environments. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • Van Buskirk J (2000) The costs of an inducible defense in anuran larvae. Ecology 81:2813–2821

    Google Scholar 

  • Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489

    Article  Google Scholar 

  • Van Buskirk J (2002a) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102

    Article  PubMed  Google Scholar 

  • Van Buskirk J, (2002b) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370

    PubMed  Google Scholar 

  • Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk?. Ecology 83:1580–1585

    Google Scholar 

  • Van Buskirk J, Relyea RA (1998) Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biol J Linn Soc 65:301–328

    Article  Google Scholar 

  • Van Buskirk J, McCollum SA, Werner EE (1997) Natural selection for environmentally induced phenotypes in tadpoles. Evolution 51:1983–1992

    Article  Google Scholar 

  • Van Buskirk J, Anderwald P, Lüpold S, Reinhardt L, Schuler H (2003) The lure effect, tadpole tail shape, and the target of dragonfly strikes. J Herpetol 37:420–424

    Article  Google Scholar 

  • Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363

    Article  Google Scholar 

  • Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and speces interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  • Wiackowski K, Staronska A (1999) The effect of predator and prey density on the induced defence of a ciliate. Funct Ecol 13:59–65

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to A. Laurila and two anonymous referees for helpful comments on earlier drafts of the manuscript. We thank J.-P. Léna for help in statistics, L. Canario and A. Renouf for field assistance. We also thank UPRA fishery for providing three-spined sticklebacks. C. Teplitsky was supported by a grant from the French Ministry for Education and Research. R. dalmatina eggs were collected with permits from the French Ministry of Environment and local environmental services. Experiments complied with the current French laws.

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Correspondence to Céline Teplitsky.

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Communicated by Roland Brandl

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Teplitsky, C., Plénet, S. & Joly, P. Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology?. Oecologia 145, 364–370 (2005). https://doi.org/10.1007/s00442-005-0132-2

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