, Volume 180, Issue 4, pp 1205–1211 | Cite as

Contrasting effects of fish predation on benthic versus emerging prey: a meta-analysis

  • Jeff S. Wesner
Community ecology – original research


Predator–prey interactions are often studied entirely within the ecosystem of the predator. However, many prey transition between ecosystems during development, expanding the effects of predators across ecosystems. Prey are often vulnerable to predation during this transition, facing a predator gauntlet as they leave their source ecosystem. As a result of predation during this transition, predators may have stronger effects on prey fluxes to the neighboring ecosystem than on prey densities in the predator’s own ecosystem. I used meta-analysis of predator (fish) and prey (invertebrate) interactions in freshwater ecosystems to test the hypothesis that fish have stronger effects on prey flux to the terrestrial ecosystem, by reducing insect emergence biomass, than on prey densities in the aquatic ecosystem, by reducing benthic insect/invertebrate biomass. Fish reduced insect emergence by 39 % on average, more than twice as strong as their reductions of benthic prey (16 % reduction; averages are variance-weighted). In fact, fish effects on benthic prey were not significantly different from zero, but were significant for emergence. These results indicate that predator effects can not only cascade from one ecosystem to another but also that effects can be stronger outside than within the ecosystem of the predator. Failure to account for this may underestimate the effects of predators on prey.


Predation Metamorphosis Insect emergence Fish Cross-ecosystem subsidies 



I am grateful for all of the authors whose hard-won data were fundamental to this study. I am also grateful for the assistance of Erik Manke, Abraham Kanz, and Nathan Bedoya, who helped with data extraction. Dan Allen and David Walters provided helpful comments on an earlier version of this manuscript. This study was funded in part from startup funds provided to JSW from the University of South Dakota.

Author contribution statement

JSW conceived, designed, and executed this study and wrote the manuscript. No other person is entitled to authorship.

Supplementary material

442_2015_3539_MOESM1_ESM.docx (81 kb)
Supplementary material 1 (DOCX 91 kb)
442_2015_3539_MOESM2_ESM.xlsx (17 kb)
Supplementary material 2 (XLSX 17 kb)


  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42Google Scholar
  2. Allan JD (1982) The effects of reduction in trout density on the invertebrate community of a mountain stream. Ecology 63:1444–1455CrossRefGoogle Scholar
  3. Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022Google Scholar
  4. Baxter CV, Fausch KD, Murakami M, Chapman PL (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–2663CrossRefGoogle Scholar
  5. Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220CrossRefGoogle Scholar
  6. Benjamin JR, Lepori F, Baxter CV, Fausch KD (2013) Can replacement of native by non-native trout alter stream-riparian food webs? Freshw Biol 58:1694–1709CrossRefGoogle Scholar
  7. Campero M, De Block M, Ollevier F, Stoks R (2008) Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality. Funct Ecol 22:271–277CrossRefGoogle Scholar
  8. Crump ML (1984) Ontogenetic changes in vulnerability to predation in tadpoles of Hyla pseudopuma. Herpetologica 40:265–271Google Scholar
  9. Dahl J (1998) Effects of a benthivorous and a drift-feeding fish on a benthic stream assemblage. Oecologia 116:426–432CrossRefGoogle Scholar
  10. Dahl J, Greenberg L (1996) Impact on stream benthic prey by benthic vs drift feeding predators: a meta-analysis. Oikos 77:177–181Google Scholar
  11. Doherty P, Dufour V, Galzin R, Hixon M, Meekan M, Planes S (2004) High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology 85:2422–2428CrossRefGoogle Scholar
  12. Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463CrossRefPubMedGoogle Scholar
  13. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Br Med J 315:629–634CrossRefGoogle Scholar
  14. Englund G (2005) Scale dependent effects of predatory fish on stream benthos. Oikos 111:19–30CrossRefGoogle Scholar
  15. Englund G, Sarnelle O, Cooper SD (1999) The importance of data-selection criteria: meta-analyses of stream predation experiments. Ecology 80:1132–1141CrossRefGoogle Scholar
  16. Epanchin PN, Knapp RA, Lawler SP (2010) Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology 91:2406–2415CrossRefPubMedGoogle Scholar
  17. Fukui D, Murakami M, Nakano S, Aoi T (2006) Effect of emergent aquatic insects on bat foraging in a riparian forest. J Anim Ecol 75:1252–1258CrossRefPubMedGoogle Scholar
  18. Gaines SD, Roughgarden J (1987) Fish in offshore kelp forests affect recruitment to intertidal barnacle populations. Science 235:479–480CrossRefPubMedGoogle Scholar
  19. Gerking SD (1994) Feeding ecology of fish. Academic, San DiegoGoogle Scholar
  20. Hayden B, Harrod C, Kahilainen KK (2013) The effects of winter ice cover on the trophic ecology of whitefish (Coregonus lavaretus L.) in subarctic lakes. Ecol Freshw Fish 22:192–201CrossRefGoogle Scholar
  21. Hedges LV, Gurevitch J, Curtis PS (1999) The meta- analysis of response ratios in experimental ecology. Ecology 80:1150–1156Google Scholar
  22. Helfman G, Collette B, Facey D (1997) The diversity of fishes. Blackwell, MaldenGoogle Scholar
  23. Hulbert L, Aires-da-Silva A, Gallucci V, Rice J (2005) Seasonal foraging movements and migratory patterns of female Lamna ditropis tagged in Prince William Sound, Alaska. J Fish Biol 67:490–509CrossRefGoogle Scholar
  24. Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883CrossRefPubMedGoogle Scholar
  25. Malison RL, Benjamin JR, Baxter CV (2010) Measuring adult insect emergence from streams: the influence of trap placement and a comparison with benthic sampling. J N Am Benthol Soc 29:647–656CrossRefGoogle Scholar
  26. Matthews WJ (1998) Patterns in freshwater fish ecology. Chapman and Hall, New YorkCrossRefGoogle Scholar
  27. Mazerolle M (2011) AICcmodavg: model selection and multimodel inference based on (Q) AIC (c). R package version 1Google Scholar
  28. McCauley SJ, Rowe L, Fortin M-J (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048CrossRefPubMedGoogle Scholar
  29. McCoy MW, Barfield M, Holt RD (2009) Predator shadows: complex life histories as generators of spatially patterned indirect interactions across ecosystems. Oikos 118:87–100CrossRefGoogle Scholar
  30. Meissner K, Muotka T (2006) The role of trout in stream food webs: integrating evidence from field surveys and experiments. J Anim Ecol 75:421–433CrossRefPubMedGoogle Scholar
  31. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166–170CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nakano S, Fausch KD, Kitano S (1999) Flexible niche partitioning via a foraging mode shift: a proposed mechanism for coexistence in stream-dwelling charrs. J Anim Ecol 68:1079–1092CrossRefGoogle Scholar
  33. Oliver D (1971) Life history of the Chironomidae. Annu Rev Entomol 16:211–230CrossRefGoogle Scholar
  34. Orrock JL et al (2010) Predator effects in predator-free space: the remote effects of predators on prey. Open Ecol J 3:22–30CrossRefGoogle Scholar
  35. Planes S, Lecaillon G (2001) Caging experiment to examine mortality during metamorphosis of coral reef fish larvae. Coral Reefs 20:211–218CrossRefGoogle Scholar
  36. Power ME (1990) Effects of fish in river food webs. Science 250:811–814CrossRefPubMedGoogle Scholar
  37. Power ME (1992) Habitat heterogeneity and the functional significance of fish in river food webs. Ecology 73:1675–1688CrossRefGoogle Scholar
  38. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  39. R Development Core Team (2007) R: a language and environment for statistical computing. R foundation for Statistical Computing, ViennaGoogle Scholar
  40. Rader RB (1997) A functional classification of the drift: traits that influence invertebrate availability to salmonids. Can J Fish Aquat Sci 54:1211–1234CrossRefGoogle Scholar
  41. Resetarits WJ, Binckley AA (2009) Spatial contagion of predation risk affects colonization dynamics in experimental aquatic landscapes. Ecology 90:869–876CrossRefPubMedGoogle Scholar
  42. Richardson JS, Zhang Y, Marczak LB (2010) Resource subsidies across the land–freshwater interface and responses in recipient communities. River Res Appl 26:55–66CrossRefGoogle Scholar
  43. Ross ST (2013) Ecology of North American freshwater fishes. University of California Press, BerkeleyGoogle Scholar
  44. Sabo JL, Power ME (2002) Numerical response of lizards to aquatic insects and short-term consequences for terrestrial prey. Ecology 83:3023–3036CrossRefGoogle Scholar
  45. Schreiber S, Rudolf VH (2008) Crossing habitat boundaries: coupling dynamics of ecosystems through complex life cycles. Ecol Lett 11:576–587CrossRefPubMedGoogle Scholar
  46. Soucek DJ, Dickinson A (2015) Full-life chronic toxicity of sodium salts to the mayfly Neocloeon triangulifer in tests with laboratory cultured food. Environ Toxicol Chem 34:2126–2137CrossRefPubMedGoogle Scholar
  47. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137CrossRefGoogle Scholar
  48. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48CrossRefGoogle Scholar
  49. Vonesh JR, Osenberg CW (2003) Multi-predator effects across life-history stages: non-additivity of egg-and larval-stage predation in an African treefrog. Ecol Lett 6:503–508CrossRefGoogle Scholar
  50. Wagner A, Volkmann S, Dettinger-Klemm P (2012) Benthic-pelagic coupling in lake ecosystems: the key role of chironomid pupae as prey of pelagic fish. Ecosphere 3:art14Google Scholar
  51. Werner E (1988) Size, scaling, and the evolution of complex life cycles. In: Ebenman B, Persson L (eds) Size structured populations: ecology and evolution. Springer, Berlin, pp 60–81Google Scholar
  52. Wesner JS (2010) Aquatic predation alters a terrestrial prey subsidy. Ecology 91:1435–1444CrossRefPubMedGoogle Scholar
  53. Wesner JS (2012) Predator diversity effects cascade across an ecosystem boundary. Oikos 121:53–60CrossRefGoogle Scholar
  54. Wesner JS, Kraus JM, Schmidt TS, Walters DM, Clements WH (2014) Metamorphosis enhances the effects of metal exposure on the mayfly, Centroptilum triangulifer. Environ Sci Technol 48:10415–10422CrossRefPubMedGoogle Scholar
  55. Winkelmann C, Hellmann C, Worischka S, Petzoldt T, Benndorf J (2011) Fish predation affects the structure of a benthic community. Freshw Biol 56:1030–1046CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of South DakotaVermillionUSA

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