Biological Invasions

, Volume 16, Issue 7, pp 1545–1555 | Cite as

Effects of crayfish on leaf litter breakdown and shredder prey: are native and introduced species functionally redundant?

  • L. Dunoyer
  • L. Dijoux
  • L. Bollache
  • C. Lagrue
Original Paper


Recent increases in biological invasions frequency may have important consequences on native communities. However, functional redundancy between invasive and native species could reduce non-native species effects on native ecosystems. Despite this, even small differences in functional traits between these species may still have unpredictable effects on colonized ecosystems. Invasive crayfish, as ecosystem engineers, potentially have wide and complex effects on recipient ecosystems, even when replacing a native counterpart. We used laboratory microcosms to test whether native (Astacus astacus) and invasive crayfish species (Orconectes limosus, Pacifastacus leniusculus and Procambarus clarkii) are actually functionally redundant in their effects on prey/shredder density and leaf litter breakdown. Results show that crayfish strongly influenced macroinvertebrate numbers and leaf litter breakdown and indicate that differences in direct (prey and leaf litter consumption) and indirect (prey habitat use and leaf litter breakdown) effects between crayfish species do exist. While the replacement of A. astacus by O. limosus may have induced only minor changes in freshwater ecosystems, invasions by the larger and more aggressive P. clarkii and P. leniusculus will likely have strong effects on invaded ecosystem. Overall, there seems to be no functional redundancy between these four species and outcomes of crayfish invasion will likely be species specific.


Astacus astacus Invasive species Pacifastacus leniusculus Orconectes limosus Procambarus clarkii Functional redundancy 



C. Lagrue was funded by a post-doctoral grant from the regional council of Burgundy. We thank S. Motreuil for help during experiments, A. Güvenatam and J. Turlin for comments on the manuscript and F.-X. Dechaume-Montcharmont and M. Gilingham for statistical advices.


  1. Bärlocher F, Kendrick B (1975) Leaf-conditioning by microorganisms. Oecologia 20:359–362CrossRefGoogle Scholar
  2. Boulton AJ, Boon PI (1991) A review of methodology used to measure leaf litter decomposition in lotic environments: time to turn over an old leaf? Aust J Mar Freshw Res 42:1–43CrossRefGoogle Scholar
  3. Byers JE, Reichard S, Randall JM, Parker IM, Smith CS, Lonsdale WM, Atkinson IAE, Seastedt TR, Williamson M, Chornesky E, Hayes D (2002) Directing research to reduce the impacts of nonindigenous species. Conserv Biol 16:630–640CrossRefGoogle Scholar
  4. Cerenius L, Söderhäll K, Persson M, Axajon R (1988) The crayfish plague fungus Aphanomyces astaci diagnosis, isolation, and pathobiology. Freshw Crayfish 7:131–144Google Scholar
  5. Cerenius L, Bangyeekhun E, Keyser P, Söderhäll I, Söderhäll K (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cell Microbiol 5:353–357PubMedCrossRefGoogle Scholar
  6. Charlebois PM, Lamberti GA (1996) Invading crayfish in a Michigan stream: direct and indirect effects on periphyton and macroinvertebrates. J N Am Benthol Soc 15:551–556CrossRefGoogle Scholar
  7. Cohen J (1988) Statistical power analysis for the behavioral sciences. Erlbaum, HillsdaleGoogle Scholar
  8. Crawford L, Yeomans WE, Adams CE (2006) The impact of introduced signal crayfish Pacifastacus leniusculus on stream invertebrate communities. Aquat Conserv Mar Freshw Ecosyst 16:611–621CrossRefGoogle Scholar
  9. Creed RP, Reed JM (2004) Ecosystem engineering by crayfish in a headwater stream community. J N Am Benthol Soc 23:224–236CrossRefGoogle Scholar
  10. Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80CrossRefGoogle Scholar
  11. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  12. Geiger W, Alcorlo P, Baltanas A, Montes C (2005) Impact of an introduced Crustacean on the trophic webs of Mediterranean wetlands. Biol Invasions 7:49–73CrossRefGoogle Scholar
  13. Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshw Behav Physiol 39:175–191CrossRefGoogle Scholar
  14. Gherardi F (2007) Understanding the impact of invasive crayfish. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. AA Dordrecht, The Netherlands, pp 507–542CrossRefGoogle Scholar
  15. Gherardi F, Aquiloni L, Dieguez-Uribeondo J, Tricarico E (2011) Managing invasive crayfish: is there a hope? Aquat Sci 73:185–200CrossRefGoogle Scholar
  16. Goddard JS (1988) Food and feeding. In: Holdich DM, Lowery RS (eds) Freshwater crayfish—biology, management and exploitation. Timber Press, Portland, pp 145–166Google Scholar
  17. Gurevitch J, Fox GA, Wardle GM, Taub D (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418PubMedCrossRefGoogle Scholar
  18. Haddaway NR, Wilcox RH, Heptonstall REA, Griffiths HM, Mortimer RJG, Christmas M, Dunn AM (2012) Predatory functional response and prey choice identify predation differences between native/invasive and parasitized/unparasitised crayfish. PLoS One 7:e32229PubMedCentralPubMedCrossRefGoogle Scholar
  19. Hart RC, Campbell LM, Hecky RE (2003) Stable isotope analyses and demographic responses counter prospects of planktivory by Caridina (Decapoda: Atyidae) in Lake Victoria. Oecologia 136:270–278PubMedCrossRefGoogle Scholar
  20. Harvey GL, Moorhouse TP, Clifford NJ, Henshaw AJ, Johnson MF, Macdonald DW, Reid I, Rice SP (2011) Evaluating the role of invasive aquatic species as drivers of fine sediment-related river management problems: the case of the signal crayfish (Pacifastacus leniusculus). Prog Phys Geogr 35:517–533CrossRefGoogle Scholar
  21. Hecky RE, Smith REH, Barton DR, Guildford SJ, Taylor WD, Charlton MN, Howell T (2004) The nearshore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can J Fish Aquat Sci 61:1285–1293CrossRefGoogle Scholar
  22. Hesselschwerdt J, Tscharner S, Necker J, Wantzen KM (2009) A local gammarid uses kairomones to avoid predation by the invasive crustaceans Dikerogammarus villosus and Orconectes limosus. Biol Invasions 11:2133–2140CrossRefGoogle Scholar
  23. Hobbs HH, Jass JP, Huner JV (1989) A review of global crayfish introductions with particular emphasis on two North American species (Decapoda, Cambaridae). Crustaceana 56:299–316CrossRefGoogle Scholar
  24. Hudina S, Hock K (2012) Behavioural determinants of agonistic success in invasive crayfish. Behav Process 91:77–81CrossRefGoogle Scholar
  25. Huner JV, Barr JE (1991) Red-swamp crawfish: biology and exploitation. Louisiana State University, Baton RougeGoogle Scholar
  26. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  27. Lawton JH, Brown VK (1993) Redundancy in ecosystems. In: Schulze ED, Mooney HA (eds) Biodiversity and ecosystem function. Springer, Berlin, pp 255–270Google Scholar
  28. Loreau M (2004) Does functional redundancy exist? Oikos 104:606–611CrossRefGoogle Scholar
  29. McCarthy JM, Hein CL, Olden JD, Vander Zander MJ (2006) Coupling long-term studies with meta-analysis to investigate impacts of non-native crayfish on zoobenthic communities. Freshw Biol 51:224–235CrossRefGoogle Scholar
  30. Miehls ALJ, Mason DM, Frank KA, Krause AE, Peacor SD, Taylor WW (2009a) Invasive species impacts on ecosystem structure and function: a comparison of Oneida Lake, New York, USA, before and after zebra mussel invasion. Ecol Model 220:3194–3209CrossRefGoogle Scholar
  31. Miehls ALJ, Mason DM, Frank KA, Krause AE, Peacor SD, Taylor WW (2009b) Invasive species impacts on ecosystem structure and function: a comparison of the Bay of Quinte, Canada, and Oneida Lake, USA, before and after zebra mussel invasion. Ecol Model 220:3182–3193CrossRefGoogle Scholar
  32. Momot WT (1984) Crayfish production: a reflection of community energetics. J Crustac Biol 4:35–54CrossRefGoogle Scholar
  33. Momot WT (1995) Redefining the role of crayfish in aquatic ecosystems. Rev Fish Sci 3:33–63CrossRefGoogle Scholar
  34. Moore JW, Carlson SM, Twardochleb LA, Hwan JL, Fox JM, Hayes SA (2012) Trophic tangles through time? Opposing direct and indirect effects of an invasive omnivore on stream ecosystem processes. PLoS One 7:e50687PubMedCentralPubMedCrossRefGoogle Scholar
  35. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605PubMedCrossRefGoogle Scholar
  36. Nyström P, Brönmark C, Granéli W (1996) Patterns in benthic food webs: a role for omnivorous crayfish? Freshw Biol 36:631–646CrossRefGoogle Scholar
  37. Nyström P, Svensson O, Lardner B, Brönmark C, Granéli W (2001) The influence of multiple introduced predators on a littoral pond community. Ecology 82:1023–1039CrossRefGoogle Scholar
  38. Olsson K, Stenroth P, Nystrom P, Graneli W (2009) Invasions and niche width: does niche width of an introduced crayfish differ from a native crayfish? Freshw Biol 54:1731–1740CrossRefGoogle Scholar
  39. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65CrossRefGoogle Scholar
  40. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
  41. Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol 33:291–315CrossRefGoogle Scholar
  42. Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162CrossRefGoogle Scholar
  43. Strauss SY (1991) Indirect effects in community ecology: their definition, study and importance. Trends Ecol Evol 6:206–210PubMedCrossRefGoogle Scholar
  44. Strayer DL (2009) Twenty years of zebra mussel: lessons from the mollusk that made headlines. Front Ecol Environ 7:135–141CrossRefGoogle Scholar
  45. Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw Biol 55:152–174CrossRefGoogle Scholar
  46. Strayer DL, Caraco NF, Cole JJ, Findlay S, Pace ML (1999) Transformation of freshwater ecosystems by bivalves—a case study of zebra mussels in the Hudson River. Bioscience 49:19–27CrossRefGoogle Scholar
  47. Tablado Z, Tella JL, Sanchez-Zapata JA, Hiraldo F (2010) The paradox of the long-term positive effects of a North American crayfish on a European community of predators. Conserv Biol 24:1230–1238PubMedCrossRefGoogle Scholar
  48. Tachet H, Bournaud M, Richoux P, Dessaix P, Pattee E (2009) Initiation aux invertébrés des eaux douces. Association Française de Limnologie, LyonGoogle Scholar
  49. Usio N (2000) Effects of crayfish on leaf processing and invertebrate colonization of leaves in a headwater stream: decoupling of a trophic cascade. Oecologia 124:608–614CrossRefGoogle Scholar
  50. Usio N, Townsend CR (2001) The significance of the crayfish Paranephrops zealandicus as shredders in a New Zealand headwater stream. J Crustac Biol 21:354–359CrossRefGoogle Scholar
  51. Usio N, Townsend CR (2004) Roles of crayfish: consequences of predation and bioturbation for stream invertebrates. Ecology 85:807–822CrossRefGoogle Scholar
  52. Usio N, Suzuki K, Konishi M, Nakano S (2006) Alien vs. endemic crayfish: roles of species identity in ecosystem functioning. Arch Hydrobiol 166:1–21CrossRefGoogle Scholar
  53. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  54. Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23CrossRefGoogle Scholar
  55. White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455CrossRefGoogle Scholar
  56. Whitledge GW, Rabeni CF (1997) Energy sources and ecological role of crayfishes in an Ozark stream: insights from stable isotopes and gut analysis. Can J Fish Aquat Sci 54:2555–2563CrossRefGoogle Scholar
  57. Williamson M (1996) Biological invasions. Chapman and Hull, LondonGoogle Scholar
  58. Witte F, Goldschmidt T, Goudswaard PC, Ligtvoet W, van Oijen MJP, Wanink JH (1992a) Species extinction and concomitant ecological changes in Lake Victoria. Neth J Zool 42:214–232CrossRefGoogle Scholar
  59. Witte F, Goldschmidt T, Goudswaard PC, Ligtvoet W, van Oijen MJP, Wanink JH (1992b) The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ Biol Fish 34:1–28CrossRefGoogle Scholar
  60. Zang Y, Richardson JS, Negishi JN (2004) Detritus processing, ecosystem engineering and benthic diversity: a test of predator–omnivore interference. J Anim Ecol 73:756–766CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • L. Dunoyer
    • 2
  • L. Dijoux
    • 2
  • L. Bollache
    • 2
    • 3
    • 4
  • C. Lagrue
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.UMR CNRS 6282 BiogéosciencesDijonFrance
  3. 3.INRA, UMR 1347 AgroécologieDijonFrance
  4. 4.Université de BourgogneDijonFrance

Personalised recommendations