Oecologia

, Volume 152, Issue 2, pp 335–343 | Cite as

Behavioural versus physiological mediation of life history under predation risk

  • Andrew P. Beckerman
  • Kazimierz Wieski
  • Donald J. Baird
Community Ecology

Abstract

Predator-generated variation in prey energy intake remains the dominant explanation of adaptive response to predation risk in prey life history, morphology and physiology across a wide range of taxa. This “behavioural hypothesis” suggest that chemical or visual signals of predation risk reduce prey energy intake leading to a life history characterized by a small size and late age at maturity. However, size-selective predation can induce either smaller size–early age or large size–late age life history. The alternative “physiological hypothesis” suggests that size-selective cues decouple the relationship between energy and life history, acting instead directly on development. Here we use a series of experiments in a fish–daphnid predator–prey system to ask whether size-selective predator cues induce a physiological mediation of development, overshadowing behaviourally based changes in food intake. We found fish chemical cues reduce the net energy intake in Daphnia magna, suggesting a behaviourally mediated reduction in energy. Experimental manipulation of food levels show further that reductions in food lead to later but smaller size at maturity. However, in line with the physiological hypothesis, we show that D. magna matures earlier and at a smaller size when exposed to fish predation cues. Furthermore, our data shows that they do this by increasing their development rate (earlier maturity) for a given growth rate, resulting in a smaller size at maturity. Our data, from a classic size-selective predation system, indicate that predator-induced changes in this system are driven by physiological mediation of development rather than behavioural mediation of energy intake.

References

  1. Abrams PA, Rowe L (1996) The effects of predation on the age and size of maturity of prey. Evolution 50:1052–1061CrossRefGoogle Scholar
  2. ASTM (1989) Standard guide for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Annual book of ASTM standards, vol 11.04, pp 379–397Google Scholar
  3. Baird DJ, Barber I, Calow P (1990) Clonal variation in general responses of Daphnia magna straus to toxic stress .1. Chronic life-history effects. Funct Ecol 4:399–407CrossRefGoogle Scholar
  4. Ball SL, Baker RL (1995) The nonlethal effects of predators and the influence of food availability on life-history of adult Chironomus tentans (Diptera, Chironomidae). Freshwater Biol 34:1–12CrossRefGoogle Scholar
  5. Ball SL, Baker RL (1996) Predator-induced life history changes: antipredator behavior costs or facultative life history shifts? Ecology 77:1116–1124CrossRefGoogle Scholar
  6. Barata C, Baird DJ, Soares A (2001) Phenotypic plasticity in Daphnia magna straus: variable maturation instar as an adaptive response to predation pressure. Oecologia 129:220–227CrossRefGoogle Scholar
  7. Beckerman AP, Benton TG, Lapsley CT, Koesters N (2005) How effective are maternal effects at having effects? Proc R Soc Lond Ser B 273:485–493CrossRefGoogle Scholar
  8. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673CrossRefGoogle Scholar
  9. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a fresh-water snail. Science 247:949–951CrossRefPubMedGoogle Scholar
  10. Fox GA (2000) Failure time analysis: studying times-to-events and rates at which events occur. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  11. Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard—test of a model with foraging minnows. Ecology 68:1856–1862CrossRefGoogle Scholar
  12. Gliwicz ZM, Pijanowska J (1993) The role of predation in zooplankton succession. In: Sommer U (ed) Plankton ecology: succession in plankton communities. Springer, Berlin Heidelberg New York, pp 253–296Google Scholar
  13. Hall DJ, Threkeld ST, Burns CW, Crowley PH (1976) The size efficiency hypothesis and the size structure of zooplankton communities. Annu Rev Ecol Syst 7:177–208CrossRefGoogle Scholar
  14. Hoverman J, Auld J, Relyea R (2005) Putting prey back together again: integrating predator-induced behavior, morphology, and life history. Oecologia 144:481–491PubMedCrossRefGoogle Scholar
  15. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314CrossRefGoogle Scholar
  16. Johansson F, Stoks R, Rowe L, De Block M (2001) Life history plasticity in a damselfly: effects of combined time and biotic constraints. Ecology 82:1857–1869CrossRefGoogle Scholar
  17. Laforsch C, Tollrian R (2004) Embryological aspects of inducible morphological defenses in Daphnia. J Morphol 262:701–707PubMedCrossRefGoogle Scholar
  18. Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239CrossRefGoogle Scholar
  19. Lima SL (1998a) Nonlethal effects in the ecology of predator–prey interactions—What are the ecological effects of anti-predator decision-making? Bioscience 48:25–34CrossRefGoogle Scholar
  20. Lima SL (1998b) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. In: Stress and behavior, vol 27. pp 215–290Google Scholar
  21. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  22. Ludwig D, Rowe L (1990) Life-history strategies for energy gain and predator avoidance under time constraints. Am Nat 135:686–707CrossRefGoogle Scholar
  23. McCauley E, Murdoch WW, Nisbet RM (1990) Growth, reproduction, and mortality of Daphnia-Pulex Leydig. Life Low Food 4:505–514Google Scholar
  24. McPeek MA, Crowley PH (1987) The effects of density and relative size on the aggressive—behavior, movement and feeding of damselfly larvae (Odonata, Coenagrionidae). Anim Behav 35:1051–1061CrossRefGoogle Scholar
  25. NIH (2004) Image J—NIH Image program (developed at the U.S. National Institutes of Health and available on the Internet at http://www.rsb.info.nih.gov/nih-image/)”. In, pp http://www.rsb.info.nih.gov/nih-image/
  26. Noonburg EG, Nisbet RM (2005) Behavioural and physiological responses to food availability and predation risk. Evol Ecol Res 7:89–104Google Scholar
  27. Parejko K (1992) Embryology of chaoborus-induced spines in Daphnia pulex. Hydrobiologia 231:77–84CrossRefGoogle Scholar
  28. Ramcharan CW, Dodson SI, Lee J (1992) Predation risk, prey behavior, and feeding rate in Daphnia pulex. Can J Fish Aquat Sci 49:159–165CrossRefGoogle Scholar
  29. Relyea RA (2002) The many faces of predation: how induction, selection, and thinning combine to alter prey phenotypes. Ecology 83:1953–1964CrossRefGoogle Scholar
  30. Reznick D, Bryant MJ, Bashey F (2002) r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509–1520CrossRefGoogle Scholar
  31. Riessen HP (1999) Predator-induced life history shifts in Daphnia: a synthesis of studies using meta-analysis. Can J Fish Aquat Sci 56:2487–2494CrossRefGoogle Scholar
  32. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life-cycles—time constraints and variation. Ecology 72:413–427CrossRefGoogle Scholar
  33. Sih A (1987) Predators and prey lifestyles: an evolutionary and ecological overview. In: Kerfoot WC, Sih A (eds) Predation: direct and indirect impacts on aquatic communties. University of New England Press, Hanover, pp 203–244Google Scholar
  34. Skelly DK (1992) Field evidence for a cost of behavioral antipredator response in a larval amphibian. Ecology 73:704–708CrossRefGoogle Scholar
  35. Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Anim Behav 47:465–468CrossRefGoogle Scholar
  36. Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322CrossRefGoogle Scholar
  37. Stibor H (2002) The role of yolk protein dynamics and predator kairomones for the life history of Daphnia magna. Ecology 83:362–369CrossRefGoogle Scholar
  38. Stibor H, Luning J (1994) Predator-induced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea, Cladocera). Funct Ecol 8:97–101CrossRefGoogle Scholar
  39. Stibor H, Machacek J (1998) The influence of fish-exuded chemical signals on the carbon budget of Daphnia. Limnol Oceanogr 43:997–1000CrossRefGoogle Scholar
  40. Stoks R, McPeek MA (2003) Predators and life histories shape Lestes damselfly assemblages along a freshwater habitat gradient. Ecology 84:1576–1587Google Scholar
  41. Taylor BE, Gabriel W (1992) To grow or not to grow—optimal resource-allocation for Daphnia. Am Nat 139:248–266CrossRefGoogle Scholar
  42. Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, N.J.Google Scholar
  43. Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363CrossRefGoogle Scholar
  44. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–425CrossRefGoogle Scholar
  45. Winder M, Boersma M, Spaak P (2003) On the cost of vertical migration: are feeding conditions really worse at greater depths? Freshwater Biol 48:383–393CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Andrew P. Beckerman
    • 1
  • Kazimierz Wieski
    • 2
  • Donald J. Baird
    • 3
  1. 1.Department of Animal and Plant ScienceUniversity of SheffieldSheffieldUK
  2. 2.Department of Fish BiologyAgricultural University of SzczecinSzczecinPoland
  3. 3.Department of BiologyNWRI/Environment Canada—Canadian Rivers Institute, University of New BrunswickFrederictonCanada

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