Evolutionary Ecology

, Volume 12, Issue 6, pp 729–738 | Cite as

Predictable changes in predation mortality as a consequence of changes in food availability and predation risk

  • Bradley R. Anholt
  • E.E. Werner


Theory predicts that animals will have lower activity levels when either the risk of predation is high or the availability of resources in the environment is high. If encounter rates with predators are proportional to activity level, then we might expect predation mortality to be affected by resource availability and predator density independent of the number of effective predators. In a factorial experiment, we tested whether predation mortality of larval wood frogs, Rana sylvatica, caused by a single larval dragonfly, Anax junius, was affected by the presence of additional caged predators and elevated resource levels. Observations were consistent with predictions. The survival rate of the tadpoles increased when additional caged predators were present and when additional resources were provided. There was no significant interaction term between predator density and food concentration. Lower predation rates at higher predator density is a form of interference competition. Reduced activity of prey at higher predator density is a potential general mechanism for this widespread phenomenon. Higher predation rates at low food levels provides an indirect mechanism for density-dependent predation. When resources are depressed by elevated consumer densities, then the higher activity levels associated with low resource levels can lead to a positive association between consumer density and consumer mortality due to predation. These linkages between variation in behaviour and density-dependent processes argue that variation in behaviour may contribute to the dynamics of the populations. Because the capture rate of predators depends on the resources available to prey, the results also argue that models of food-web dynamics will have to incorporate adaptive variation in behaviour to make accurate predictions.

Anax junius anti-predator behaviour behavioural indirect effects density dependence growth rate/mortality rate trade-offs interaction modification interference competition Rana sylvatica 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrams, P.A. (1982) Functional response of optimal foragers. Am. Nat. 120, 382–390.Google Scholar
  2. Abrams, P.A. (1984) Foraging time optimization and interactions in food webs. Am. Nat. 124, 80–96.Google Scholar
  3. Abrams, P.A. (1990) The effects of adaptive behaviour on the type-2 functional response. Ecology 71, 877–885.Google Scholar
  4. Abrams, P.A. (1991a) Strengths of indirect effects generated by optimal foraging. Oikos 62, 167–176.Google Scholar
  5. Abrams, P.A. (1991b) The relationship between food availability and foraging effort: Effects of life history and time scale. Ecology 72, 1242–1252.Google Scholar
  6. Abrams, P.A. (1992) Why don’t predators have positive effects on prey populations? Evol. Ecol. 6, 56–72.Google Scholar
  7. Abrams, P.A. (1993a) Why predation rates should not be proportional to predator density. Ecology 74, 726–733.Google Scholar
  8. Abrams, P.A. (1993b) Indirect effects arising from optimal foraging. In Mutualism and Community Organization: Behavioural, Theoretical and Food-web Approaches (H. Kawanabe, J.E. Cohen and K. Iwasaka, eds), pp. 255–279. Oxford University Press, Oxford.Google Scholar
  9. Aitkin, M., Anderson, D., Francis, B. and Hinded, J. (1989) Statistical Modelling in GLIM. Clarendon Press, Oxford.Google Scholar
  10. Anholt, B.R. (1990) An experimental separation of interference and exploitative competition in a larval damselfly. Ecology 71, 1483–1493.Google Scholar
  11. Anholt, B.R. and Werner, E.E. (1995) Interaction between food availability and predation mortality mediated by adaptive behaviour. Ecology 76, 2230–2234.Google Scholar
  12. Anholt, B.R., Skelly, D.K. and Werner, E.E. (1996) Factors modifying antipredator behaviour in larval toads. Herpetologica 52, 301–313.Google Scholar
  13. Azevedo-Ramos, C., Van Sluys, M., Hero, J.-M. and Magnusson, W.E. (1992) Influence of tadpole movement on predation by odonate naiads. J. Herpet. 26, 335–338.Google Scholar
  14. Beddington, J.R. (1975) Mutual interference between parasites and predators and its effect on searching efficiency. J. Anim. Ecol. 44, 331–340.Google Scholar
  15. Berven, K.A. (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71, 1599–1608.Google Scholar
  16. Berven, K.A. and Gill, D.E. (1983) Interpreting geographic variation in life-history traits. Am. Zool. 23, 85–97.Google Scholar
  17. Charnov, E.L., Orians, G.H. and Hyatt, K. (1976) Ecological implications of resource depression. Am. Nat. 110, 247–259.Google Scholar
  18. Crawley, M.J. (1993) GLIM for Ecologists. Blackwell Scientific, Oxford.Google Scholar
  19. Curio, E. (1976) The Ethology of Predation. Springer, Berlin.Google Scholar
  20. Gerritsen, J. and Strickler, J.R. (1977) Encounter probabilities, and community structure in zooplankton: A mathematical model. J. Fish. Res. Board Can. 34, 73–82.Google Scholar
  21. Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
  22. Horat, P. and Semlitsch, R.D. (1994) Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav. Ecol. Sociobiol. 34, 393–401.Google Scholar
  23. Huey, R. and Pianka, E.C. (1981) Ecological consequences of foraging mode. Ecology 62, 991–999.Google Scholar
  24. Ives, A.R. and Dobson, A.P. (1987) Antipredator behaviour and the population dynamics of simple predator-prey systems. Am. Nat. 130, 431–447.CrossRefGoogle Scholar
  25. Lawler, S.P. (1989) Behavioural responses to predators and predation risk in four species of larval anuran. Anim. Behav. 38, 1039–1047.Google Scholar
  26. Lima, S.L. and Dill, L.M. (1990) Behavioural decisions made under the risk of predation: A review and prospectus. Can. J. Zool. 68, 619–640.Google Scholar
  27. May, R.M. (1981) Models for single populations. In Theoretical Ecology: Principles and Applications, 2nd edn (R.M. May, ed.), pp. 7–29. Sinauer Associates, Sunderland, MA.Google Scholar
  28. McCollom, S.A. and Van Buskirk, J. (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50, 583–593.Google Scholar
  29. McCullagh, P. and Nelder, J.A. (1989) Generalized Linear Models, 2nd edn. Chapman & Hall, London.Google Scholar
  30. McNamara, J.M. and Houston, A.I. (1987) Starvation and predation as factors limiting population size. Ecology 68, 1515–1519.Google Scholar
  31. McNamara, J.M. and Houston, A.I. (1994) The effect of a change in foraging options on intake rate and predation rate. Am. Nat. 144, 978–1000.Google Scholar
  32. Milinski, M. (1986) Constraints placed by predators on feeding behaviour. In The Behaviour of Teleost Fishes (T.J. Pitcher, ed.), pp. 236–250. Croom-Helm, London.Google Scholar
  33. Morin, P.J. (1983) Predation, competition, and the composition of larval anuran guilds. Ecol. Monogr. 53, 119–138.Google Scholar
  34. Murdoch, W.W. and Oaten, A. (1975) Predation and population stability. Adv. Ecol. Res. 9, 1–131.Google Scholar
  35. Numerical Algorithms Group (1987) The GLIM System Release 3.77 (C.D. Payne, ed.). Numerical Algorithms Group, Oxford.Google Scholar
  36. Peacor, S.D. and Werner E.E. (1997) Trait-mediated indirect interactions in a simple aquatic community. Ecology 78, 1146–1156.Google Scholar
  37. Ruxton, G.D. (1995) Short term refuge use and stability of predator-prey models. Theor. Pop. Biol. 47, 1–17.Google Scholar
  38. Schaffner, A.K. (1996) Influence of predator presence and prey density on behaviour and growth of damselfly larvae (Ischnura elegans). Dipl. thesis, University of Zürich, Zürich.Google Scholar
  39. Sih, A. (1987a) Predators and prey lifestyles: An evolutionary and ecological overview. In Predation: Direct and Indirect Impacts on Aquatic Communities (W.C. Kerfoot and A. Sih, eds), pp. 203–224. University of New England Press, Hanover, NH.Google Scholar
  40. Sih, A. (1987b) Prey refuges and predator-prey stability. Theor. Pop. Biol. 31, 1–12.Google Scholar
  41. Skelly, D.K. (1992) Larval distributions of spring peepers and chorus frogs: Regulating factors and the role of larval behaviour. PhD dissertation, University of Michigan, Ann Arbor, MI.Google Scholar
  42. Skelly, D.K. (1994) Activity level and the susceptibility of anuran larvae to predation. Anim. Behav. 48, 465–468.Google Scholar
  43. Skelly, D.K. and Werner, E.E. (1990) Behavioural and life-historical responses of larval american toads to an odonate predator. Ecology 71, 2313–2322.Google Scholar
  44. Smith, D.C. (1983) Factors controlling tadpole populations of the chorus frog, Pseudacris triseriata, on the Isle Royale. Ecology 64, 501–510.Google Scholar
  45. Smith, D.C. (1987) Adult recruitment in chorus frogs: E.ects of size and date at metamorphosis. Ecology 68, 344–350.Google Scholar
  46. Van Buskirk, J. (1989) Density-dependent cannibalism in larval dragonflies. Ecology 70, 1442–1449.Google Scholar
  47. Weisser, W.W., Wilson, H.B. and Hassell, M.P. (1997) Interference among parasitoids: A clarifying note. Oikos 70, 173–178.Google Scholar
  48. Werner, E.E. (1991) Nonlethal effects of a predator on competitive interactions between two anuran larvae. Ecology 72, 1709–1720.Google Scholar
  49. Werner, E.E. (1992a) Competitive interactions between woodfrog and northern leopard frog larvae: The influence of size and activity. Copeia 1992, 26–35.Google Scholar
  50. Werner, E.E. (1992b) Individual behaviour and higher-order interactions. Am. Nat. 140, S5–S32.Google Scholar
  51. Werner, E.E. and Anholt, B.R. (1993) Ecological consequences of the tradeo. between growth and mortality rates mediated by foraging activity. Am. Nat. 142, 242–272.Google Scholar
  52. Werner, E.E. and Anholt, B.R. (1996) Predator induced behavioural indirect effects: Consequences to competitive interactions in anuran larvae. Ecology 77, 157–169.Google Scholar
  53. Wilbur, H.M. (1987) Regulation of structure in complex systems: Experimental temporary pond communities. Ecology 68, 1437–1452.Google Scholar
  54. Wissinger, S.A. (1989) Seasonal variation in the intensity of competition and predation among dragonfly larvae. Ecology 70, 1017–1027.Google Scholar
  55. Wissinger, S.A. and McGrady, J. (1993) Intraguild predation and competition between larval dragonflies: Direct and indirect effects on shared prey. Ecology 74, 207–218.Google Scholar
  56. Woodward, B.D. (1983) Predator-prey interactions and breeding-pond use of temporary-pond species in a desert anuran community. Ecology 64, 1549–1555.Google Scholar
  57. Wooton, J.T. (1993) Indirect effects and habitat use in an intertidal community: Interaction chains and interaction modification. Am. Nat. 141, 71–89.Google Scholar
  58. Wooton, J.T. (1994) The nature and consequences of indirect effects in ecological communities. Ann. Rev. Ecol. Syst. 25, 443–446.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Bradley R. Anholt
    • 1
  • E.E. Werner
    • 2
  1. 1.Department of Zoology, Erindale CollegeUniversity of TorontoMississaugaCanada
  2. 2.Department of BiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations