Abstract
The trade of live ornamental freshwater crayfish has grown rapidly in the last decade and has become the major pathway for new non-indigenous crayfish species (NICS) introductions into Europe. Here, I report on the German ornamental crayfish trade, the main importer of non-indigenous crayfish into Europe. In total, 120 NICS have been available as ornamental aquarium species. One hundred and five species originate from North or Central America and are, therefore, suspected to be crayfish plague vectors. The import rate since 2005 was estimated to be seven new species per year. Despite many species being imported, only eleven species were found to be very common in the trade. In 2009, 16 online shops offered at least 37 NICS. The availability, price, and size of the offered species were used to predict their introduction status. Multiple binary logistic regression analysis showed that species’ availability and size were the principal predictors of the likelihood of being recorded as introduced from aquaria. NICS introduced from aquaria were found to be more available and larger than those present only in aquaria, and their potential invasiveness was also higher. The findings are consistent with the propagule pressure hypothesis in that a greater availability is likely related to more release events, and large species may be released more frequently as a result of overpopulating or outgrowing their aquaria. Efforts to mitigate the risk of further harmful crayfish introductions from aquaria should aim to drastically reduce the availability of high-risk species.
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References
Adams SB (2008) Cambarellus shufeldtii. Version 1.0. USDA Forest Service, Crayfishes of Mississippi website, Oxford. http://maps.fs.fed.us/crayfish/factsheets/FS0056.pdf. Accessed 23 Aug 2009
Alderman DJ (1997) Crustaceans: bacterial and fungal diseases. OIE Sci Tech Rev 15
Bauer U (2011) Neocaridina in Deutschland aufgetaucht. http://www.crustahunter.com/de/node/1248. Accessed 22 Nov 2011
Beatty S, Morgan D, Gill H (2005) Role of life history strategy in the colonisation of Western Australian aquatic systems by the introduced crayfish Cherax destructor Clark, 1936. Hydrobiologia 549:219–237
Blankenhaus R (2010) CPO—Cambarellus patzcuarensis “Orange”. Amazonas 6:28–35
CBD (2000). Global strategy on invasive alien species. Convention on Biological Diversity, UNEP/CBD/SBTTA/6/INF/9: 1-52. UNEP, Montreal, Canada Publ Internet. http://www.cbd.int/programmes/cross-cutting/alien/documents.aspx Accessed 22 Dec 2008
CBD (2011) Aichi biodiversity targets, convention on biological diversity. http://www.cbd.int/sp/targets/. Accessed 19 Dec 2011
Chambers JM, Hastie TJ (1992) Statistical models in S. Wadsworth, Pacific Grove
Chucholl C (2011a) Der Handel mit exotischen Flusskrebsen. Forum Flusskrebse 15:33–39
Chucholl C (2011b) Population ecology of an alien “warm water” crayfish (Procambarus clarkii) in a new cold habitat. KMAE 401:29. doi:10.1051/kmae/2011053
Chucholl C, Daudey T (2008) First record of Orconectes juvenilis (Hagen, 1870) in eastern France: update to the species identity of a recently introduced orconectid crayfish (Crustacea: Astacida). Aquat Inv 3:105–107
Chucholl C, Dehus P (2011) Flusskrebse in Baden-Württemberg. Fischereiforschungsstelle Baden-Württemberg (FFS), Langenargen
Chucholl C, Pfeiffer M (2010) First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquat Inv 5:405–412
Courtenay WR Jr (1999) Aquariums and water gardens as vectors of introduction. In: Claudi R, Leach JH (eds) Nonindigenous freshwater organisms: vectors, biology, and impacts. Lewis Publishers, Boca Raton, pp 127–128
Crossman EJ, Cudmore BC (1999) Summary of North American fish introductions through the aquarium/horticulture trade. In: Claudi R, Leach JH (eds) Nonindigenous freshwater organisms: vectors, biology, and impacts. Lewis Publishers, Boca Raton, pp 129–134
Dehus P, Dussling U, Hoffmann C (1999a) Notes on the occurrence of the calico crayfish (Orconectes immunis) in Germany. Freshw Crayfish 12:786–790
Dehus P, Phillipson S, Bohl E, Oidtmann B, Keller M, Lechleiter S (1999b) German conservation strategies for native crayfish species with regard to alien species. Crustac Issues 11:149–159
Duggan I (2010) The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biol Inv. doi:10.1007/s10530-010-9768-x
Duggan I (2011) Aquaria. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkley, pp 32–35
Duggan I, Rixon CAM, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Inv 8:377–382
Dümpelmann C, Bonacker F, Häckl M (2009) Erstnachweis des Rotem Amerikanischen Sumpfkrebses Procambarus clarkii (Decapoda: Cambaridae) in Hessen. Lauterbornia 67:39–47
Faulkes Z (2010) The spread of the parthenogenetic marbled crayfish, Marmorkrebs (Procambarus sp.), in the North American pet trade. Aquat Inv 5:447–450
Gelmar CF, Pätzold F, Grabow K, Martens A (2006) Der Kalikokrebs Orconectes immunis am nördlichen Oberrhein: ein neuer amerikanischer Flusskrebs breitet sich schnell in Mitteleuropa aus (Crustacea: Cambaridae). Lauterbornia 56:15–25
Groß H (2011) Edelkrebsprojekt NRW. http://www.edelkrebsnrw.de/krebse_frame.htm. Accessed 12 Jan 2011
Henttonen P, Huner JV (1999) The Introduction of alien species of crayfish in Europe: a historical introduction. Crustac Issues 11:13–22
Hobbs HH (1974) A checklist of the North and Middle American crayfishes (Decapoda: Astacidae and Cambaridae). Smithson Contrib Zool 166
Hobbs HH (1989) An illustrated checklist of the American crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae). Smithson Contrib Zool 480
Hobbs HH, Jass JP, Huner JV (1989) A review of global crayfish introductions with particular emphasis on two North American species (Decapoda, Cambaridae). Crustaceana 56:299–316
Holdich DM (1999) The negative effects of established crayfish introductions. Crustac Issues 11:31–48
Holdich DM, Gheradi F (1999) Native and alien crayfish in Europe: an introduction. Crustac Issues 11:3–12
Holdich DM, Pöckl M (2005) Does legislation work in protecting vulnerable species? Bull Fr Peche Piscicult 376–377:809–827
Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. KMAE 11:394–395. doi:10.1051/kmae/2009025
Holthuis LB (1986) The freshwater Crayfish of New Guinea. Freshw Crayfish 6:48–58
Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Py P, Roques A, Sol D, Solarz W, Vilà M (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol. doi:10.1111/j.1365-2664.2007.01442.x
Hulme PE, Pysek P, Nentwig W, Vilà M (2009) Will threat of biological invasions unite the European Union? Science 324:40–41
Huner JV, Barr LE (1991) Red swamp crawfish: biology, culture, and exploitation. Louisiana State University Sea Grant College System, Louisiana State University, Baton Rouge
Jaklič M, Vrezec A (2011) The first tropical alien crayfish species in European waters: the redclaw Cherax quadricarinatus (Von Martens, 1868) (Decapoda, Parastacidae). Crustaceana 84:651–665
Janský V, Mutkovič A (2010) Rak Procambarus sp. (Crustacea: Decapoda: Cambaridae)—Prvŷ Nález na Slovensku. Acta Rer Natur Mus Nat Slov 56:64–67
Jimenez SA, Faulkes Z (2010) Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights? J Ethol. doi:10.1007/s10164-010-0232-2
Jones JPG, Rasamy JR, Harvey A, Toon A, Oidtmann B, Randrianarison MH, Raminosoa N, Ravoahangimalala OR (2009) The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol Inv 11:1475–1482
Justo-Hanani R, Dayan T, Tal A (2010) The role of regulatory decision-making on non-indigenous species introductions. Biol Inv 12:2815–2824. doi:10.1007/s10530-010-9687-x
Knuth D (1999) Erstnachweis des Roten Amerikanischen Sumpfkrebses Procambarus (Scapulicambarus) clarkii (GIRARD, 1852) für Brandenburg in der Havel bei Werder. Beitr Tierwelt Mark 14:117–118
Larson ER, Olden JD (2010) Latent extinction and invasion risk of crayfishes in the southeastern United States. Conserv Biol 24:1099–1110. doi:10.1111/j.1523-1739.2010.01462.x
Lindqvist OV, Huner JV (1999) Life history characteristics of crayfish: what makes them good colonizers? Crustac Issues 11:23–30
Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell publishing, Oxford
Lodge DM, Taylor CA, Holdich DM, Skurdal J (2000) Nonindigenous crayfishes threaten North American freshwater biodiversity. Fisheries 25:7–19
Lukhaup C (2004) Süßwasserkrebse aus aller Welt. Dähne Verlag, Ettlingen
Lukhaup C, Herbert B (2008) A new species of freshwater crayfish (Crustacea: Decapoda: Parastacidae) from the Fly River drainage, Western Province, Papua New Guinea. Mem Queensl Mus 52:213–219
Lukhaup C, Pekny R (2005) Krebse im aquarium. Dähne Verlag, Ettlingen
Lukhaup C, Pekny R (2006) Cherax (Cherax) holthuisi, a new species of crayfish (Crustacea: Decapoda: Parastacidae) from the centre of the Vogelkop Peninsula in Irian Jaya (West New Guinea), Indonesia. Zool Med Leiden 80–1:101–107
Lukhaup C, Pekny R (2008) Cherax (Astaconephrops) boesemani, a new species of crayfish (Crustacea: Decapoda: Parastacidae) from the centre of the Vogelkop Peninsula in Irian Jaya (West New Guinea), Indonesia. Zool Med Leiden 82:1–10
Lukhaup C, Pekny R (2009) Flusskrebse in der Aquaristik. In: Füreder L (ed) Flusskrebse: Biologie, Ökologie, Gefährdung. Veröffentlichungen des Naturmuseums Südtirol, vol 6. Folio Verlag, Bozen, pp 129–132
Marten M, Werth C, Marten D (2004) Der Marmorkrebs (Cambaridae, Decapoda) in Deutschland—ein weiteres Neozoon im Einzugsgebiet des Rheins. Lauterbornia 50:17–23
Martin P, Shen H, Füller G, Scholtz G (2010) The first record of the parthenogenetic Marmorkrebs (Decapoda, Astacida, Cambaridae) in the wild in Saxony (Germany) raises the question of its actual threat to European freshwater ecosystems. Aquat Inv 5:397–403
Marzano FN, Scalici M, Chiesa S, Gherardi F, Piccinini A, Gibertini G (2009) The first record of the marbled crayfish adds further threats to fresh waters in Italy. Aquat Inv 4. doi:10.3391/ai.2009.4.2
McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ, Symes A, Chanson J, Hoffmann M (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108
Muller KE, Peterson BL (1984) Practical methods for computing power in testing the multivariate general linear hypothesis. Comput Stat Data Anal 2:143–158
Nyström P (2002) Ecology. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Scientific Press, Oxford, pp 192–224
OIE (2009) Aquatic animal health code. Publ Internet. http://www.oie.int/eng/normes/fcode/en_sommaire.htm. Accessed 1 July 2010
Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138
Peay S (2009) Invasive non-indigenous crayfish species in Europe: recommendations on managing them. KMAE 394–395:03. doi:10.1051/kmae/2010009
Peay S, Holdich DM, Brickland J (2010) Risk assessments of non-indigenous crayfish in Great Britain. Freshw Crayfish 17 (in press)
Pekny R (2003) Flusskrebse aus aller Welt—Mögliche Invasoren in Europa. Internationales Flusskrebsforum Augsburg 2003, Tagungsband, 27–34
Pekny R, Lukhaup C (2005) Aquarienkrebse in Europa—eine rasante Entwicklung! 2. Internationale Flusskrebstagung, Baden 2005, Tagungsband, 78–94
Rabalais MR, Magoulick DD (2006) Is competition with the invasive crayfish Orconectes neglectus chaenodactylus responsible for the displacement of the native crayfish Orconectes eupunctus? Biol Inv 8:1039–1048
R Development Core Team (2011) R 2.14. http://www.r-project.org. Accessed 12 Nov 2011
Riley S (2005) Invasive alien species and the protection of biodiversity: the role of quarantine laws in resolving inadequacies in the international legal regime. J Environ Law 17:323–359
Rodríguez CF, Bécares E, Fernández-Aláez M, Fernández-Aláez C (2005) Loss of diversity and degradation of wetlands as a result of introducing exotic crayfish. Biol Inv 7:75–85
Royo F, Andersson G, Bangyeehkun E, Múzquiz JL, Söderhäll K, Cerenius L (2004) Physiological and genetic characterisation of some new Aphanomyces strains isolated from freshwater crayfish. Vet Microbiol 104:103–112
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sannwald E, Huenneke L, Jackson RB, Kinzig A, Leemanns R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes BH, Walker BH, Walker M, Wall DH (2000) Biodiversity scenario for the year 2100. Science 287:1770–1774
Sandodden R, Johnsen SI (2010) Eradication of introduced signal crayfish Pacifastacus leniusculus using the pharmaceutical BETAMAX VET. Aquat Inv 5. doi:10.3391/ai.2010.5.1
Schlüter M (1989) Flußkrebse aus Australien. Ritter in farbenfroher Rüstung. DATZ 42:526–528
Scholtz G, Bradand A, Tolley L, Reimann A, Mittmann B, Lukhaup C, Steuerwald F, Vogt G (2002) Parthenogenesis in an outsider crayfish. Nature 421:806
Schulz H, Groß H, Dümpelmann C, Schulz R (2009) Flusskrebse Deutschlands. In: Füreder L (ed) Flusskrebse: Biologie, Ökologie, Gefährdung. Veröffentlichungen des Naturmuseums Südtirol, vol 6. Folio-Verlag, Bozen, pp 71–81
Seitz R, Vilpoux K, Hopp U, Harzsch S, Maier G (2005) Ontogeny of the Marmorkrebs (Marbled Crayfish): a parthenogenetic crayfish with unknown origin and phylogenetic position. J Exp Zool 303:393–405
Shine C, Kettunen M, ten Brink P, Genovesi P, Gollasch S (2009) Technical support to EU strategy on invasive species (IAS)—recommendations on policy options to control the negative impacts of IAS on biodiversity in Europe and the EU. Final report for the European Commission. Institute for European Environmental Policy (IEEP), Brussels
Simons SA, De Poorter M (eds) (2009) Best practices in pre-import risk screening for species of live animals in international trade. In: Proceedings of an expert workshop on preventing biological invasions, University of Notre Dame, Indiana, USA, 9–11 April 2008. Global Invasive Species Programme, Nairobi, Kenya
Skelton CE (2010) History, status, and conservation of Georgia crayfishes. Southeast Nat 9(Special Issue 3):127–138
Soes M, Koese B (2010) Invasive crayfish in the Netherlands: a preliminary risk analysis. Interim report, Bureau Waardenburg bv, Stichting EIS-Nederland, Invasive Alien Species Team, Waardenburg
Soes M, van Eekelen R (2006) Rivierkrefeten, een oprukkend problem? De Levede Natuur 107:56–59
Soes M, Majoor GD, Keulen SMA (2011) Bellamya chinensis (Gray, 1834) (Gastropoda: Viviparidae), a new alien snail species for the European fauna. Aquat Inv 6:97–102
Souty-Grosset C, Reynolds JD (2009) Current ideas on methodological approaches in European crayfish conservation and restocking procedures. KMAE 394–395:01. doi:10.1051/kmae/2009021
Souty-Grosset C, Holdich DM, Noel PY, Reynolds JD, Haffner P (eds) (2006) Atlas of Crayfish in Europe. Museum national d’Histoire naturelle, Paris (Patrimoines naturels, 64)
Stucki T, Jean-Richard P (1999) Verbreitung der Flusskrebse in der Schweiz. Mitteilungen zur Fischerei 65. BUWAL, Bern
Taylor CA, Schuster GA (2004) Crayfishes of Kentucky. Illinois Natural History Survey, Special Publication 28
Thompson WL (ed) (2004) Sampling rare or elusive species: concepts, designs, and techniques for estimating population parameters. Island Press, Washington
Tricarico E, Vilizzi L, Gherardi F, Copp GH (2009) Calibration of FI-ISK, an Invasiveness screening tool for nonnative freshwater invertebrates. Risk Anal. doi:10.1111/j.1539-6924.2009.01255.x
UCLA/ATS (2011) Pseudo R-squareds. University of California: Academic Technology Services, Statistical Consulting Group. http://www.ats.ucla.edu/stat/mult_pkg/faq/general/psuedo_rsquareds.htm. Accessed 12 Nov 2011
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Wendt W (2011) Erstnachweis des invasiven Marmorkrebses, Procambarus fallax (HAGEN, 1870) f. virginalis, für Sachsen. Forum Flusskrebse 15:39–42
Werner U (1993) Ausgefallene Aquarienpfleglinge. Landbuch-Verlag, Hannover
Acknowledgments
I would like to thank R. Pekny and C. Lukhaup for their help with data collection and kind support. I am especially grateful to D.M. Holdich, P. Dehus, L. Johnson, and three anonymous reviewers for their helpful comments on the manuscript. A part of this study was funded by the scholarship programme of the German Federal Environmental Foundation (DBU).
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10530_2012_273_MOESM1_ESM.pdf
Online Resource 1. Year of import, general availability, and presumed introduction pathways of freshwater crayfish in the German pet trade. Introduction pathway abbreviations are as follows: C = consumption trade, FB = fishing bait, and S = deliberate stocking. Please note that the list includes probable synonyms and misidentified specimens: */# = presumably the same species; $ = status unsure, probably Ca. shufeldtii and Ca. schmitti; § = probably misidentified. The main references are as follows: 1 = Pekny and Lukhaup 2005, 2 = present study, 3 = Lukhaup and Pekny 2005, and 4 = Holdich et al. 2009. Supplementary material 1 (PDF 21 kb)
10530_2012_273_MOESM2_ESM.pdf
Online Resource 2. Mean price class, online availability, potential invasiveness (FI-ISK score), natural habitat, and native and introduced range of non-indigenous crayfish species offered by 16 online shops in 2009. N.A. means that the price was not depicted or no available information on the natural habitat. Supplementary material 2 (PDF 18 kb)
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Chucholl, C. Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15, 125–141 (2013). https://doi.org/10.1007/s10530-012-0273-2
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DOI: https://doi.org/10.1007/s10530-012-0273-2