Biodiversity and Conservation

, Volume 21, Issue 10, pp 2641–2651 | Cite as

Complex impact of an invasive crayfish on freshwater food webs

  • Gentile Francesco Ficetola
  • Matteo Elio Siesa
  • Fiorenza De Bernardi
  • Emilio Padoa-Schioppa
Original Paper


Invasive alien species can have complex effects on native ecosystems, and interact with multiple components of food webs, making it difficult a comprehensive quantification of their direct and indirect effects. We evaluated the relationships between the invasive crayfish, Procambarus clarkii, amphibian larvae and predatory insects, to quantify crayfish impacts on multiple levels of food webs, and to evaluate whether crayfish predation of aquatic insects has indirect consequences for their preys. We used pipe sampling to assess the abundance of crayfish, amphibian larvae and their major predators (Ditiscidae, Notonectidae and larvae of Anisoptera) in invaded and uninvaded ponds within a human dominated landscape. We disentangled the multivariate effects of P. clarkii on different components of food web through a series of constrained redundancy analyses. The crayfish had a negative, direct impact on both amphibian communities and their predators. Amphibian abundance was negatively related to both predators. However, the negative, direct effects of crayfish on amphibians were much stronger than predation by native insects. Our results suggest that this crayfish impacts multiple levels of food webs, disrupting natural prey-predator relationships.


Amphibian larvae Biological invasions Dragonfly Mesopredator release Native predators Redundancy analysis 



We thank S. Ravani, F. Rizzotti and P. Todeschini for help during fieldwork. The comments of three reviewers improved an early version of the manuscript. GFF was funded by a scholarship of the University of Milano-Bicocca. This study is part of the PhD work of MES.


  1. Alcorlo P, Geiger W, Otero M (2004) Feeding preferences and food selection of the red swamp crayfish, Procambarus clarkii, in habitats differing in food item diversity. Crustaceana 77:435–453CrossRefGoogle Scholar
  2. Borcard D, Gillet F, Legendre P (2011) Numerical ecology withy R. Springer, New YorkCrossRefGoogle Scholar
  3. Carchini G (1983) Odonata. CNR, VeronaGoogle Scholar
  4. Correia AM (2003) Food choice by the introduced crayfish Procambarus clarkii. Ann Zool Fenn 40:517–528Google Scholar
  5. Covich AP, Palmer MA, Crowl TA (1999) The role of benthic invertebrate species in freshwater ecosystems—Zoobenthic species influence energy flows and nutrient cycling. Bioscience 49:119–127CrossRefGoogle Scholar
  6. Crooks KR, Soule ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566CrossRefGoogle Scholar
  7. Cruz MJ, Pascoal S, Tejedo M, Rebelo R (2006) Predation by an exotic crayfish, Procambarus clarkii, on Natterjack Toad, Bufo calamita, embryos: its role on the exclusion of this amphibian from its breeding ponds. Copeia 2006:274–280CrossRefGoogle Scholar
  8. Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496PubMedCrossRefGoogle Scholar
  9. Dieguez-Uribeondo J, Aquiloni L, Martin MP, Gherardi F (2011) The North American crayfish Procambarus clarkii is the carrier of the oomycete Aphanomyces astaci in Italy. Biol Invasions 13:359–367CrossRefGoogle Scholar
  10. Digiovinazzo P, Ficetola GF, Bottoni L, Andreis C, Padoa-Schioppa E (2010) Ecological thresholds in herb communities for the management of suburban fragmented forests. For Ecol Manage 259:343–349CrossRefGoogle Scholar
  11. Dodd CKJ (ed) (2010) Amphibian ecology and conservation. A handbook of techniques. Oxford University Press, OxfordGoogle Scholar
  12. Fea G, Nardi PA, Ghia D, Spairani M, Manenti R, Rossi S, Moroni M, Bernini F (2006) Dati preliminari sulla distribuzione in Lombardia dei gamberi d’acqua dolce autoctoni e alloctoni. Atti Soc It Sci Nat Mus Civ St Nat Milano 147:201–210Google Scholar
  13. Ficetola GF, De Bernardi F (2004) Amphibians in an human-dominated landscape: the community structure is related to habitat features and isolation. Biol Conserv 119:219–230CrossRefGoogle Scholar
  14. Ficetola GF, Padoa-Schioppa E, De Bernardi F (2009) Influence of landscape elements in riparian buffers on the conservation of semiaquatic amphibians. Conserv Biol 23:114–123PubMedCrossRefGoogle Scholar
  15. Ficetola GF, Marziali L, Rossaro B, De Bernardi F, Padoa-Schioppa E (2011a) Landscape - stream interactions and habitat conservation for amphibians. Ecol Appl 21:1272–1282PubMedCrossRefGoogle Scholar
  16. Ficetola GF, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011b) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Divers Distrib 17:1141–1151CrossRefGoogle Scholar
  17. Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar FreshwBehav Phy 39:175–191CrossRefGoogle Scholar
  18. Gherardi F, Panov VE (2009). Procambarus clarkii (Girard), red swamp crayfish/crawfish (Cambaridae, Crustacea). In: Pages 316 in DAISIE. Handbook of alien species in Europe. Springer, DordrechtGoogle Scholar
  19. Gomez-Mestre I, Diaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defences in tadpoles. Proc R Soc B 278:3364–3370PubMedCrossRefGoogle Scholar
  20. Gutierrez-Yurrita PJ, Montes C (2001) Bioenergetics of juveniles of red swamp crayfish (Procambarus clarkii). Compar Biochem Physiol Mol Integr Physiol 130:29–38CrossRefGoogle Scholar
  21. Hamasaki K, Yamanaka T, Tanaka K, Nakatani Y, Iwasaki N, Sprague DS (2009) Relative importance of within-habitat environment, land use and spatial autocorrelations for determining odonate assemblages in rural reservoir ponds in Japan. Ecol Res 24:597–605Google Scholar
  22. Heidemann H, Seidenbusch R (2002) Larves et exuvies des libellules de France et d’Allemagne (sauf de Corse). Société Française d’OdonatologieGoogle Scholar
  23. Hobbs HH (1972) Biota of freshwater ecosystems, identification manual 9: Crayfishes (Astacidae) of North and Middle America. Water Pollution Control Research Series. US Environmental Protection Agency, Washington, DCGoogle Scholar
  24. Klose K, Cooper SD (2012) Contrasting effects of an invasive crayfish (Procambarus clarkii) on two temperate stream communities. Freshw Biol 57:526–540CrossRefGoogle Scholar
  25. Lanza B, Andreone F, Bologna MA, Corti C, Razzetti E (eds) (2007) Fauna d’Italia, vol XLII. Amphibia, Calderini, BolognaGoogle Scholar
  26. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  27. Legendre P, Oskanen J, ter Braak CJF (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277Google Scholar
  28. Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes Rusticus) on a fresh-water littoral food-web. Ecology 75:1265–1281CrossRefGoogle Scholar
  29. Matsuzaki SS, Usio N, Takamura N, Washitani I (2009) Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158:673–686PubMedCrossRefGoogle Scholar
  30. McCauley SJ, Davis CJ, Relyea RA, Yurewicz KL, Skelly DK, Werner EE (2008) Metacommunity patterns in larval odonates. Oecologia 158:329–342Google Scholar
  31. Miyake M, Miyashita T (2011) Identification of alien predators that should not be removed for controlling invasive crayfish threatening endangered odonates. Aquatic Conserv Mar FreshwEcosyst 21:292–298CrossRefGoogle Scholar
  32. Nentwig W (ed) (2007) Biological invasions. Springer, BerlinGoogle Scholar
  33. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H (2011) Vegan: community ecology package version 1.17–6.
  34. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Ruffo S, Stoch F (eds) (2005) Checklist e distribuzione della fauna italiana. Memorie del Museo Civico di Storia Naturale di Verona, 2a serie, sezione Scienze della Vita, VeronaGoogle Scholar
  36. Siesa ME, Manenti R, Padoa-Schioppa E, De Bernardi F, Ficetola GF (2011) Spatial autocorrelation and the analysis of invasion processes from distribution data: a study with the crayfish Procambarus clarkii. Biol Invasions 13:2147–2160CrossRefGoogle Scholar
  37. Strayer DL, Evinver VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651PubMedCrossRefGoogle Scholar
  38. Usio N, Townsend CR (2002) Functional significance of crayfish in stream food webs: roles of omnivory, substrate heterogeneity and sex. Oikos 98:512–522CrossRefGoogle Scholar
  39. Van Buskirk J (2003) Habitat partitioning in European and North American pond-breeding frogs and toads. Divers Distrib 9:399–410CrossRefGoogle Scholar
  40. Van Buskirk JV (2005) Local and landscape influence on amphibian occurrence and abundance. Ecology 86:1936–1947CrossRefGoogle Scholar
  41. Van Buskirk JV, Arioli M (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. J Evol Biol 18:596–608PubMedCrossRefGoogle Scholar
  42. Werner EE, Skelly DK, Relyea RA, Yurewicz KL (2007) Amphibian species richness across environmental gradients. Oikos 116:1697–1712CrossRefGoogle Scholar
  43. Werner EE, Relyea RA, Yurewicz KL, Skelly DK, Davis CJ (2009) Comparative landscape dynamics of two anuran species: climate-driven interaction of local and regional processes. Ecol Monogr 79:503–521CrossRefGoogle Scholar
  44. White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Gentile Francesco Ficetola
    • 1
  • Matteo Elio Siesa
    • 2
  • Fiorenza De Bernardi
    • 2
  • Emilio Padoa-Schioppa
    • 1
  1. 1.Department of Environmental SciencesUniversità degli Studi di Milano BicoccaMilanItaly
  2. 2.Department of Life SciencesUniversità degli Studi di MilanoMilanItaly

Personalised recommendations