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Complex impact of an invasive crayfish on freshwater food webs

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Abstract

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.

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References

  • 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 77:435–453

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology withy R. Springer, New York

    Book  Google Scholar 

  • Carchini G (1983) Odonata. CNR, Verona

    Google Scholar 

  • Correia AM (2003) Food choice by the introduced crayfish Procambarus clarkii. Ann Zool Fenn 40:517–528

    Google Scholar 

  • 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 49:119–127

    Article  Google Scholar 

  • Crooks KR, Soule ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566

    Article  CAS  Google Scholar 

  • 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 2006:274–280

    Article  Google Scholar 

  • 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 22:489–496

    Article  PubMed  Google Scholar 

  • 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 13:359–367

    Article  Google Scholar 

  • 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 259:343–349

    Article  Google Scholar 

  • Dodd CKJ (ed) (2010) Amphibian ecology and conservation. A handbook of techniques. Oxford University Press, Oxford

    Google Scholar 

  • 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 147:201–210

    Google Scholar 

  • Ficetola GF, De Bernardi F (2004) Amphibians in an human-dominated landscape: the community structure is related to habitat features and isolation. Biol Conserv 119:219–230

    Article  Google Scholar 

  • Ficetola GF, Padoa-Schioppa E, De Bernardi F (2009) Influence of landscape elements in riparian buffers on the conservation of semiaquatic amphibians. Conserv Biol 23:114–123

    Article  PubMed  Google Scholar 

  • Ficetola GF, Marziali L, Rossaro B, De Bernardi F, Padoa-Schioppa E (2011a) Landscape - stream interactions and habitat conservation for amphibians. Ecol Appl 21:1272–1282

    Article  PubMed  Google Scholar 

  • 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 17:1141–1151

    Article  Google Scholar 

  • Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar FreshwBehav Phy 39:175–191

    Article  Google Scholar 

  • 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, Dordrecht

  • Gomez-Mestre I, Diaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defences in tadpoles. Proc R Soc B 278:3364–3370

    Article  PubMed  Google Scholar 

  • Gutierrez-Yurrita PJ, Montes C (2001) Bioenergetics of juveniles of red swamp crayfish (Procambarus clarkii). Compar Biochem Physiol Mol Integr Physiol 130:29–38

    Article  CAS  Google Scholar 

  • 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 24:597–605

    Google Scholar 

  • Heidemann H, Seidenbusch R (2002) Larves et exuvies des libellules de France et d’Allemagne (sauf de Corse). Société Française d’Odonatologie

  • 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, DC

    Google Scholar 

  • Klose K, Cooper SD (2012) Contrasting effects of an invasive crayfish (Procambarus clarkii) on two temperate stream communities. Freshw Biol 57:526–540

    Article  Google Scholar 

  • Lanza B, Andreone F, Bologna MA, Corti C, Razzetti E (eds) (2007) Fauna d’Italia, vol XLII. Amphibia, Calderini, Bologna

    Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Legendre P, Oskanen J, ter Braak CJF (2011) Testing the significance of canonical axes in redundancy analysis. Methods Ecol Evol 2:269–277

    Google Scholar 

  • Lodge DM, Kershner MW, Aloi JE, Covich AP (1994) Effects of an omnivorous crayfish (Orconectes Rusticus) on a fresh-water littoral food-web. Ecology 75:1265–1281

    Article  Google Scholar 

  • Matsuzaki SS, Usio N, Takamura N, Washitani I (2009) Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158:673–686

    Article  PubMed  Google Scholar 

  • McCauley SJ, Davis CJ, Relyea RA, Yurewicz KL, Skelly DK, Werner EE (2008) Metacommunity patterns in larval odonates. Oecologia 158:329–342

    Google Scholar 

  • 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 21:292–298

    Article  Google Scholar 

  • Nentwig W (ed) (2007) Biological invasions. Springer, Berlin

    Google Scholar 

  • 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. www.r-project.org

  • R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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, Verona

  • 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 13:2147–2160

    Article  Google Scholar 

  • Strayer DL, Evinver VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651

    Article  PubMed  Google Scholar 

  • Usio N, Townsend CR (2002) Functional significance of crayfish in stream food webs: roles of omnivory, substrate heterogeneity and sex. Oikos 98:512–522

    Article  Google Scholar 

  • Van Buskirk J (2003) Habitat partitioning in European and North American pond-breeding frogs and toads. Divers Distrib 9:399–410

    Article  Google Scholar 

  • Van Buskirk JV (2005) Local and landscape influence on amphibian occurrence and abundance. Ecology 86:1936–1947

    Article  Google Scholar 

  • Van Buskirk JV, Arioli M (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. J Evol Biol 18:596–608

    Article  PubMed  Google Scholar 

  • Werner EE, Skelly DK, Relyea RA, Yurewicz KL (2007) Amphibian species richness across environmental gradients. Oikos 116:1697–1712

    Article  Google Scholar 

  • 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 79:503–521

    Article  Google Scholar 

  • White EM, Wilson JC, Clarke AR (2006) Biotic indirect effects: a neglected concept in invasion biology. Divers Distrib 12:443–455

    Article  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Environmental Sciences, Università degli Studi di Milano Bicocca, Piazza della Scienza 1, 20126, Milan, Italy

    Gentile Francesco Ficetola & Emilio Padoa-Schioppa

  2. Department of Life Sciences, Università degli Studi di Milano, Via Celoria 26, 2133, Milan, Italy

    Matteo Elio Siesa & Fiorenza De Bernardi

Authors
  1. Gentile Francesco Ficetola
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  2. Matteo Elio Siesa
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  3. Fiorenza De Bernardi
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  4. Emilio Padoa-Schioppa
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Correspondence to Gentile Francesco Ficetola.

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Ficetola, G.F., Siesa, M.E., De Bernardi, F. et al. Complex impact of an invasive crayfish on freshwater food webs. Biodivers Conserv 21, 2641–2651 (2012). https://doi.org/10.1007/s10531-012-0323-1

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  • DOI: https://doi.org/10.1007/s10531-012-0323-1

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