[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Log in

Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

After interest in keeping crayfish (Crustacea, Decapoda, Astacida) in home aquaria peaked in the mid-2000s, the aquarium trade has become a novel introduction pathway for non-native crayfish species in Germany. Here, we provide an update on the ornamental crayfish trade approximately one decade after the ‘crayfish hype’ to explore the long-term implications in terms of bio-invasion risk. Specifically, species’ availability in e-commerce and potential invasiveness were assessed and compared to previous studies. Morphological and ecological traits of the offered species were compiled and related to their long-term availability (covering 2005–2015). In July 2015, a total of 31 online shops offered 28 crayfish species, which represents a decline of 24 % in species diversity compared to the late 2000s. The estimated rate of import of new species has considerably flattened and approaches pre-hype values (<1 species year−1). However, the risk associated with the offered species, as assessed by a risk screening tool, has not decreased compared to the late 2000s. Long-term availability in the trade was primarily determined by bright coloration, the ability to reproduce under warm aquarium conditions, and a preference for lentic habitats. Species featuring such traits are likely to persist in the aquarium trade and include four high-risk species, most notably invasive and crayfish plague-carrying red swamp crayfish (Procambarus clarkii) and Marmorkrebs (Procambarus fallax f. virginalis). Persistent propagule pressure from aquaria has substantially contributed to the establishment of both species in Germany, stressing the need for more effective pathway management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1

Data for 2009 were taken from Chucholl (2013)

Fig. 2
Fig. 3

Data for 2009 were taken from Chucholl (2013)

Fig. 4

Similar content being viewed by others

References

  • Adams SB (2008) Cambarellus shufeldtii. Version 1.0. USDA Forest Service, Crayfishes of Mississippi website, Oxford, MS. http://maps.fs.fed.us/crayfish/factsheets/FS0056.pdf. Accessed 23 Aug 2009

  • 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

    Article  Google Scholar 

  • Bitter F (ed) (2006) Wirbellose im Süßwasseraquarium—Garnelen, Krebse, Krabben & Co. Aquaristik Sonderheft 1, Dähne-Verlag, Ettlingen

  • Breiman L, Friedman J, Stone CJ, Olshen RA (1984) Classification and regression trees. CRC Press, Boca Raton

    Google Scholar 

  • Chucholl C (2011) Population ecology of an alien “warm water” crayfish (Procambarus clarkii) in a new cold habitat. Knowl Manag Aquat Ecosyst 401:29. doi:10.1051/kmae/2011053

    Article  Google Scholar 

  • Chucholl C (2013) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15:125–141. doi:10.1007/s10530-012-0273-2

    Article  Google Scholar 

  • Chucholl C (2015) Marbled crayfish gaining ground in Europe: the role of the pet trade as invasion pathway. In: Kawai T, Faulkes Z, Scholtz G (eds) Freshwater crayfish: a global overview. CRC Press, Boca Raton, pp 83–114

    Chapter  Google Scholar 

  • Chucholl C (2016) The bad and the super-bad: prioritising the threat of six invasive alien to three imperilled native crayfishes. Biol Invasions. doi:10.1007/s10530-016-1141-2

    Google Scholar 

  • Chucholl C, Morawetz K, Groß H (2012) The clones are coming-strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquat Invasions 7:511–519. doi:10.3391/ai.2012.7.4.008

    Article  Google Scholar 

  • Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20:37–46

    Article  Google Scholar 

  • Duggan IC, Rixon CAM, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Invasions 8:377–382. doi:10.1007/s10530-004-2310-2

    Article  Google Scholar 

  • European Commission (2016) Commission implementing regulation (EU) 2016/1141 of 13 July 2016 adopting a list of invasive alien species of union concern pursuant to regulation (EU) No 1143/2014 of the European parliament and of the council. Off J EU 59:4–8

    Google Scholar 

  • Faulkes Z (2015a) Marmorkrebs (Procambarus fallax f. virginalis) are the most popular crayfish in the North American pet trade. Knowl Manag Aquat Ecosyst 416:20. doi:10.1051/kmae/2015016

    Article  Google Scholar 

  • Faulkes Z (2015b) The global trade in crayfish as pets. Crustac Res 44:75–92. doi:10.18353/crustacea.44.0_75

    Article  Google Scholar 

  • Gonella H (1999) Krebse, Krabben und Garnelen im Süßwasseraquarium. Bede-Verlag, Ruhmannsfelden

    Google Scholar 

  • Gross H (2013) Blauer Floridakrebs (Procambarus alleni) im Rhein! Forum Flusskrebse 19:33–35

    Google Scholar 

  • Heip CH, Herman PM, Soetaert K (1998) Indices of diversity and evenness. Océanis, Paris

    Google Scholar 

  • Hobbs HH (1974) A checklist of the North and Middle American crayfishes (Decapoda: Astacidae and Cambaridae). Smithson Contrib Zool 166:161

    Google Scholar 

  • Hobbs HH (1989) An illustrated checklist of the American crayfishes (Decapoda: Astacidae, Cambaridae, and Parastacidae). Smithson Contrib Zool 480:236

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Holdich DM (ed) (2002) Biology of freshwater crayfish. Blackwell Science, London

    Google Scholar 

  • 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. Knowl Manag Aquat Ecosyst 394–395:11. doi:10.1051/kmae/2009025

    Article  Google Scholar 

  • Holthuis LB (1986) The freshwater Crayfish of New Guinea. Freshw Crayfish 6:48–58

    Google Scholar 

  • Jones JPG, Rasamy JR, Harvey A et al (2009) The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol Invasions 11:1475–1482. doi:10.1007/s10530-008-9334-y

    Article  Google Scholar 

  • Keller NS, Pfeiffer M, Roessink I et al (2014) First evidence of crayfish plague agent in populations of the marbled crayfish (Procambarus fallax forma virginalis). Knowl Manag Aquat Ecosyst 414:15. doi:10.1051/kmae/2014032

    Article  Google Scholar 

  • Kuhn M (2008) Building predictive models in R using the caret package. J Stat Softw 28:1–26

    Article  Google Scholar 

  • Laister G, Lehmann G, Martens A (2014) Exotic Odonata in Europe. Odonatologica 43:125–135

    Google Scholar 

  • Lietsch P (1984) Zur Pflege und Zucht des südamerikanischen Sumpfkrebses (Procambarus troglodytes). AT 31:313

    Google Scholar 

  • Lipták B, Vitázková B (2015) Beautiful, but also potentially invasive. Ekológia (Bratislava) 34:155–162

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi:10.1016/j.tree.2005.02.004

    Article  PubMed  Google Scholar 

  • Lukhaup C, Pekny R (2005) Krebse im Aquarium. Dähne Verlag, Ettlingen

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Lukhaup C, Pekny R (2008) Süßwasserkrebse aus aller Welt. Dähne Verlag, Ettlingen

    Google Scholar 

  • Lukhaup C, Panteleit J, Schrimpf A (2015) Cherax snowden, a new species of crayfish (Crustacea, Decapoda, Parastacidae) from the Kepala Burung (Vogelkop) Peninsula in Irian Jaya (West Papua), Indonesia. ZooKeys 518:1–14. doi:10.3897/zookeys.518.6127

    Article  Google Scholar 

  • Maceda-Veiga A, Domínguez-Domínguez O, Escribano-Alacid J, Lyons J (2016) The aquarium hobby: can sinners become saints in freshwater fish conservation? Fish Fish 17:860–874. doi:10.1111/faf.12097

    Article  Google Scholar 

  • Mengedoht O (2014) Hilft nur ein Selbstverzicht? DATZ 4:28–31

    Google Scholar 

  • Mrugała A, Kozubíková-Balcarová E, Chucholl C et al (2014) Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol Invasions. doi:10.1007/s10530-014-0795-x

    Google Scholar 

  • Nyström P (1999) Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. Crustac Issues 11:63–86

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Papavlasopoulou I, Perdikaris C, Vardakas L, Paschos I (2014) Enemy at the gates: introduction potential of non-indigenous freshwater crayfish in Greece via the aquarium trade. Cent Eur J Biol 9:11–18. doi:10.2478/s11535-013-0120-6

    Google Scholar 

  • Patoka J, Kalous L, Kopecký O (2014a) Risk assessment of the crayfish pet trade based on data from the Czech Republic. Biol Invasions 16:2489–2494. doi:10.1007/s10530-014-0682-5

    Article  Google Scholar 

  • Patoka J, Petrtýl M, Kalous L (2014b) Garden ponds as potential introduction pathway of ornamental crayfish. Knowl Manag Aquat Ecosyst 414:13

    Article  Google Scholar 

  • Patoka J, Bláha M, Devetter M et al (2015) Aquarium hitchhikers: attached commensals imported with freshwater shrimps via the pet trade. Biol Invasions. doi:10.1007/s10530-015-1018-9

    Google Scholar 

  • Peay S, Holdich D, Brickland J (2010) Risk assessments of non-indigenous crayfish in Great Britain. Freshw Crayfish 17:109–122

    Google Scholar 

  • Pekny R, Lukhaup C (2005) Aquarienkrebse in Europa—eine rasante Entwicklung! 2. Int Flusskrebstagung Baden 78–94

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rodríguez C, Bécares E, Fernández-Aláez M, Fernández-Aláez C (2005) Loss of diversity and degradation of wetlands as a result of introducing exotic crayfish. Biol Invasions 7:75–85

    Article  Google Scholar 

  • Schlüter M (1989) Flußkrebse aus Australien. Ritter in farbenfroher Rüstung. DATZ 42:526–528

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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)

  • Strobl C, Malley J, Tutz G (2009) An introduction to recursive partitioning: rationale, application, and characteristics of classification and regression trees, bagging, and random forests. Psychol Methods 14:323

    Article  PubMed  PubMed Central  Google Scholar 

  • Svoboda J, Mrugała A, Kozubíková-Balcarová E, Petrusek A (2016) Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. J Fish Dis. doi:10.1111/jfd.12472

    PubMed  Google Scholar 

  • Taylor CA, Schuster GA (2004) Crayfishes of Kentucky. Illinois natural history survey, Special Publication 28, Carbondale

    Google Scholar 

  • Therneau T, Atkinson B, Ripley B (2015) rpart: recursive Partitioning and Regression Trees. R package version 4.1–9.https://github.com/cran/rpart. Accessed 12 Aug 2015

  • Tricarico E, Vilizzi L, Gherardi F, Copp GH (2010) Calibration of FI-ISK, an Invasiveness Screening Tool for Nonnative Freshwater Invertebrates. Risk Anal 30:285–292. doi:10.1111/j.1539-6924.2009.01255.x

    Article  PubMed  Google Scholar 

  • Vaeßen S, Hollert H (2015) Impacts of the North American signal crayfish (Pacifastacus leniusculus) on European ecosystems. Environ Sci Eur. doi:10.1186/s12302-015-0065-2

    PubMed  PubMed Central  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth, Springer, New York

    Book  Google Scholar 

  • Veselý L, Buřič M, Kouba A (2015) Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? Sci Rep 5:16340. doi:10.1038/srep16340

    Article  PubMed  PubMed Central  Google Scholar 

  • Werner U (1993) Ausgefallene Aquarienpfleglinge. Landbuch-Verlag, Hannover

    Google Scholar 

  • Werner U (1998) Garnelen, Krebse und Krabben im Süßwasseraquarium. Aqualog Special, Verlag A.C.S., Mörfelden-Walldorf

    Google Scholar 

  • Zeng Y, Chong KY, Grey EK et al (2015) Disregarding human pre-introduction selection can confound invasive crayfish risk assessments. Biol Invasions. doi:10.1007/s10530-015-0881-8

    Google Scholar 

Download references

Acknowledgments

We are grateful to A. Martens, R. Wegner (both PH Karlsruhe), and S. Nehring (BfN) for kindly providing records of free-living Marmorkrebs. The helpful comments and suggestions made by I. Duggan (Editor) and two anonymous reviewers are also gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Chucholl.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1067 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chucholl, C., Wendler, F. Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade. Biol Invasions 19, 197–208 (2017). https://doi.org/10.1007/s10530-016-1272-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1272-5

Keywords

Navigation