Skip to main content
Log in

Meta-analysis of foraging and predation risk trade-offs in terrestrial systems

  • Review
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Although there is ample evidence for the generality of foraging and predation trade-offs in aquatic systems, its application to terrestrial systems is less comprehensive. In this review, meta-analysis was used to analyze experiments on giving-up-densities in terrestrial systems to evaluate the overall magnitude of predation risk on foraging behavior and experimental conditions mediating its effect. Results indicate a large and significant decrease in foraging effort as a consequence of increased predation risk. Whether experiments were conducted under natural or artificial conditions produced no change in the overall effect predation had on foraging. Odor and live predators as a correlate of predation risk had weaker and nonsignificant effects compared to habitat characteristics. The meta-analysis suggests that the effect of predation risk on foraging behavior in terrestrial systems is strongly dependent on the type of predation risk being utilized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abrams PA (1992) Predators that benefit prey and prey that harm predators: Unusual effects of interacting foraging adaptations. Am Nat 140:573–600

    Article  Google Scholar 

  • Abrams PA (1993) Optimal traits when there are several costs: The interaction of mortality and energy costs in determining foraging behavior. Behav Ecology 4:246–253

    Article  Google Scholar 

  • Altendorf KB, Laundre JW, Lopez Gonzalez CA, Brown JS (2001) Assessing the effects of predation risk on foraging behavior of mule deer. J Mammal 82:430–439

    Article  Google Scholar 

  • Arthur AD, Pech RP, Dickman CR (2004) Habitat structure mediates the non-lethal effects of predation on enclosed populations of house mice. J Anim Ecol 73(5):867–877

    Article  Google Scholar 

  • Bateson M (2002) Recent advances in our understanding of risk-sensitive foraging preferences. Proc Nutr Soc 61(4):509–516

    Article  PubMed  Google Scholar 

  • Boinski S, Kauffman L, Westoll A, Stickler CM, Cropp S, Ehmke E (2003) Are vigilance, risk from avian predators and group size consequences of habitat structure? A comparison of three species of squirrel monkey (Saimiri oerstedii, S. boliviensis, and S. sciureus). Behav 140:1421–1467

    Article  Google Scholar 

  • Bouskila A (1995) Interactions between predation risk and competition—a field-study of kangaroo rats and snakes. Ecology 76(1):165–178

    Article  Google Scholar 

  • Bowers MA (1988) Seed removal experiments on desert rodents: The microhabitat by moonlight effect. J Mammal 69:201–204

    Article  Google Scholar 

  • Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47

    Article  Google Scholar 

  • Brown JS (1989) Mechanisms underlying the organization of a desert rodent community. J Arid Environ 17(2):211–218

    Google Scholar 

  • Brown JS (1992) Patch use under predation risk. I. Models and predictions. Ann Zool Fenn 29:301–309

    Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014

    Article  Google Scholar 

  • Brown JS, Kotler BP, Valone TJ (1994) Foraging under predation: a comparison of energetic and predation costs in a Negev and Sonoran Desert rodent community. Aust J Zool 42:435–448

    Article  Google Scholar 

  • Brown JS, Kotler BP, Mitchell WA (1997) Competition between birds and mammals: a comparison of giving-up densities between crested larks and gerbils. Evol Ecol 11(6):757–771

    Article  Google Scholar 

  • Brown JS, Kotler BP, Knight MH (1998) Patch use in the pygmy rock mouse (Petromyscus collinus). Mammalia 62(1):108–112

    Google Scholar 

  • Caraco T, Martindale S, Pulliam HR (1980) Avian time budgets and distance to cover. Auk 97(4):872–875

    Google Scholar 

  • Charnov EL (1976) Optimal foraging: the marginal value theorem. Theor Pop Bio 9:129–136

    Article  CAS  Google Scholar 

  • Cohen J (1969) Statistical power analysis for the behavioral sciences. Academic, New York

    Google Scholar 

  • Dill LM (1987) Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can J Zool 65:803–811

    Article  Google Scholar 

  • Engelhart A, Muller-Schwarze D (1995) Responses of beaver (Castor canadensis KUHL) to predator chemicals. J Chem Ecol 21:1349–1364

    Article  CAS  Google Scholar 

  • Epple G, Mason JR, Nolte DL, Campell DL (1993) Effects of predator odors on feeding in the mountain beaver (Aplodontia rufa). J Mammal 74:715–722

    Article  Google Scholar 

  • Gilliam JF, Frasier DF (1987) Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856–1862

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1993) Meta-analysis: Combining the results of independent experiments. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 1st edn. Chapman and Hall, New York, pp 378–398

    Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80(4):1142–1149

    Google Scholar 

  • Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: A meta-analysis of field experiments. Am Nat 155(4):435–453

    Article  PubMed  Google Scholar 

  • Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A Meta-analysis of competition in field experiments. Am Nat 140(4):539–572

    Article  Google Scholar 

  • Gutman R, Dayan T (2005) Temporal partitioning: an experiment with two species of spiny mice. Ecology 86(1):164–173

    Article  Google Scholar 

  • Hay ME, Fuller PJ (1981) Seed escape from heteromyid rodents: the importance of microhabitat and seed preference. Ecology 62:1395–1399

    Article  Google Scholar 

  • Hedges LV, Olkin I (1985) Statistical methods for Meta-analysis. Academic, New York

    Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental Ecology. Ecology 80(4):1150–1156

    Article  Google Scholar 

  • Hernández L, Laundre JW, Gurung M (2005) From the field: use of camera traps to measure predation risk in a puma-mule deer system. Wildl Soc Bull 33:353–358

    Article  Google Scholar 

  • Holtcamp WN, Grant WE, Vinson B (1997) Patch use under predation hazard: effect of the red imported fire ant on deer mouse foraging behavior. Ecology 78:308–317

    Google Scholar 

  • Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc Lond B 341:375–397

    Article  Google Scholar 

  • Jacob J, Brown JS (2000) Microhabitat use, giving-up densities and temporal activity as short- and long-term anti-predator behaviors in common voles. Oikos 91:131–138

    Article  Google Scholar 

  • Janson CH (1990) Ecological consequences of individual spatial choice in foraging groups of brown capuchin monkeys, Cebus Apella. Anim Behav 40:922–934

    Article  Google Scholar 

  • Jones M, Dayan T (2000) Foraging behavior and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in the presence of Blanford’s fox (Vulpes cana) odor. J Chem Ecol 26(2):455–469

    Article  CAS  Google Scholar 

  • Kotler BP (1997) Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 78(2):274–282

    Article  Google Scholar 

  • Kotler BP, Brown JS, Slotow RH, Goodfriend WL, Strauss M (1993) The influence of snakes on the foraging behavior of gerbils. Oikos 67:309–316

    Article  Google Scholar 

  • Kotler BP, Brown JS, Knight MH (1999) Habitat and patch use by hyraxes: there’s no place like home? Ecol Lett 2(2):82–88

    Article  Google Scholar 

  • Kotler BP, Brown JS, Hickey M (1999) Food storability and the foraging behavior of fox squirrels (Sciurus niger). Am Midl Nat 142(1):77–86

    Article  Google Scholar 

  • Kotler BP, Brown JS, Oldfield A, Thorson J, Cohen D (2001) Foraging substrate and escape substrate: Patch use by three species of gerbils. Ecology 82(6):1781–1790

    Google Scholar 

  • Kotler BP, Brown JS, Bouskila A (2004). Apprehension and time allocation in gerbils: The effects of predatory risk and energetic state. Ecology 85(4):917–922

    Article  Google Scholar 

  • Lima SL (1985) Maximizing feeding efficiency and minimizing time exposed to predators—a trade-off in the black-capped chickadee. Oecologia 66(1):60–67

    Article  Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions—what are the ecological effects of anti-predator decision-making? Bioscience 48(1):25–34

    Article  Google Scholar 

  • Lima SL, Valone TJ (1986) Influence of predation risk on diet selection: a simple example in the grey squirrel. Anim Behav 34:536–544

    Article  Google Scholar 

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

    Article  Google Scholar 

  • McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519

    Article  Google Scholar 

  • Millinski M (1986) Constraints placed by predators on feeding behavior. In: Pitcher T (ed) The behaviour of teleost fishes. Croom Helm, London, pp 236–252

    Google Scholar 

  • Mohr K, Vibe-Petersen S, Jeppesen LL, Bildsoe M, Leirs H (2003) Foraging of multimammate mice, Mastomys natalensis, under different predation pressure: cover, patch-dependent decisions and density-dependent GUDs. Oikos 100(3):459–468

    Article  Google Scholar 

  • Newman JA, Recer GM, Zwicker SM, Caraco T (1988) Effects of predation hazard on foraging constraints—patch-use strategies in grey squirrels. Oikos 53(1):93–97

    Article  Google Scholar 

  • Orrock JL, Danielson BJ (2004) Rodents balancing a variety of risks: invasive fire ants and indirect and direct indicators of predation risk. Oecologia 140(4):662–667

    Article  PubMed  Google Scholar 

  • Orrock JL, Danielson BJ, Brinkerhoff RJ (2004) Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav Ecol 15(3):433–437

    Article  Google Scholar 

  • Oyugi JO, Brown JS (2003) Giving-up densities and habitat preferences of European starlings and American robins. Condor 105(1):130–135

    Article  Google Scholar 

  • Pfister JA, Muller-Schwarze D, Balph DF (1990) Effects of predator fecal odors on feed selection by sheep and cattle. J Chem Ecol 16:573–583

    Article  Google Scholar 

  • Powell F, Banks PB (2004) Do house mice modify their foraging behaviour in response to predator odours and habitat? Anim Behav 67:753–759

    Article  Google Scholar 

  • Price MV, Correll RA (2001) Depletion of seed patches by Merriam’s kangaroo rats: Are GUD assumptions met? Ecol Lett 4:334–343

    Article  Google Scholar 

  • Pusenius J, Schmidt KA (2002) The effects of habitat manipulation on population distribution and foraging behavior in meadow voles. Oikos 98(2):251–262

    Article  Google Scholar 

  • Rosenberg MS, Adams DC, Gurevitch J (1999) MetaWin 2.0. Statistical software for conducting meta-analysis: fixed effects models, mixed effect models, and resampling tests. Sinauer Associates, Sunderland, Massachusetts

  • Rohner C, Krebs CJ (1996) Owl predation on snowshoe hares: consequences of antipredator behaviour. Oecologia 108(2):303–310

    Google Scholar 

  • Sih A (1980) Optimal behavior: can foragers balance two conflicting demands. Science 210:1041–1043

    Article  PubMed  Google Scholar 

  • Sih A (1982) Foraging strategies and the avoidance of predation by an aquatic insect. Ecology 63:786–796

    Article  Google Scholar 

  • Sih A (1987) Predators and prey lifestyles: an ecological overview. In: Kerfoot WC, Sih A (eds) Predation: direct and indirect impacts on aquatic communities. Univ. Press of New England, Hanover, New Hampshire, pp 203–224

    Google Scholar 

  • Sih A (1992) Prey uncertainty and the balancing of antipredator and feeding needs. Am Nat 5:1052–1069

    Article  Google Scholar 

  • Stephens DW, Krebs JR (1988) Foraging theory. Mono Behav Ecol. Princeton Univ. Press, New Jersey

    Google Scholar 

  • Stokes VL, Pech RP, Banks PB, Arthur AD (2004) Foraging behaviour and habitat use by Antechinus flavipes and Sminthopsis murina (Marsupialia : Dasyuridae) in response to predation risk in eucalypt woodland. Biol Conserv 117(3):331–342

    Article  Google Scholar 

  • Sullivan TP, Crump DR (1984) Influence of mustelid scent-gland compounds on suppression of feeding by snowshoe hares (Lepus americanus). J Chem Ecol 10:1809–1821

    Article  CAS  Google Scholar 

  • Sundell J, Dudek D, Klemme I, Koivisto E, Pusenius J, Ylonen H (2004) Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis. Oecologia 139(1):157–162

    Article  PubMed  Google Scholar 

  • Thorson JM, Morgan RA, Brown JS, Norman JE (1998) Direct and indirect cues of predatory risk and patch use by fox squirrels and thirteen-lined ground squirrels. Behav Ecol 9:151–157

    Article  Google Scholar 

  • Valone TJ, Lima SL (1987) Carrying food items to cover for consumption: the behavior of ten bird species feeding under the risk of predation. Oecologia 71:286–294

    Article  Google Scholar 

  • Yunger JA, Meserve PL, Gutiérrez JR (2002) Small mammal foraging behavior: mechanisms for coexistence and implications for population dynamics. Ecol Monogr 72(4):561–577

    Google Scholar 

Download references

Acknowledgements

This work is in partial fulfillment of the requirements for a doctorate in Ecology and Evolution at Stony Brook University. I thank my advisor, Dr. Charles Janson, for his scientific and editorial contributions, Dr. Jessica Gurevitch her for comments and guidance in conducting the statistical analyses, and Dr. Joel S. Brown and Dr. Burt P. Kotler for their insightful reviews which significantly improved the quality of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer L. Verdolin.

Additional information

Communicated by A. Cockburn

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verdolin, J.L. Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60, 457–464 (2006). https://doi.org/10.1007/s00265-006-0172-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0172-6

Keywords

Navigation