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Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome

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Abstract

Rapidly growing trade of ornamental animals may represent an entry pathway for emerging pathogens; this may concern freshwater crayfish that are increasingly popular pets. Infected crayfish and contaminated water from aquaria may be released to open waters, thus endangering native crustacean fauna. We tested whether various non-European crayfish species available in the pet trade in Germany and the Czech Republic are carriers of two significant crustacean pathogens, the crayfish plague agent Aphanomyces astaci and the white spot syndrome virus (WSSV). The former infects primarily freshwater crayfish (causing substantial losses in native European species), the latter is particularly known for economic losses in shrimp aquacultures. We screened 242 individuals of 19 North American and Australasian crayfish taxa (the identity of which was validated by DNA barcoding) for these pathogens, using molecular methods recommended by the World Organisation for Animal Health. A. astaci DNA was detected in eight American and one Australian crayfish species, comprising in total 27 % of screened batches. Furthermore, viability of A. astaci was confirmed by its isolation to axenic cultures from three host taxa, including the parthenogenetic invader Marmorkrebs (Procambarus fallax f. virginalis). In contrast, WSSV was only confirmed in three individuals of Australian Cherax quadricarinatus. Despite modest prevalence of detected infections, our results demonstrate the potential of disease entry and spread through this pathway, and should be considered if any trade regulations are imposed. Our study highlights the need for screening for pathogens in the ornamental trade as one of the steps to prevent the transmission of emerging diseases to wildlife.

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References

  • Ahern D, England J, Ellis A (2008) The virile crayfish, Orconectes virilis (Hagen, 1870) (Crustacea: decapoda: cambaridae), identified in the UK. Aquat Invasions 3:102–104. doi:10.3391/ai.2008.3.1.18

    Article  Google Scholar 

  • Alderman DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Rev Sci Tech OIE 15:603–632

    CAS  Google Scholar 

  • Bartley DM, Subasinghe RP (1996) Historical aspects of international movement of living aquatic species. Rev Sci Tech OIE 15:387–400

    CAS  Google Scholar 

  • Bateman KS, Tew I, French C, Hicks RJ, Martin P, Munro J, Stentiford GD (2012) Susceptibility to infection and pathogenicity of white spot disease (WSD) in non-model crustacean host taxa from temperate regions. J Invertebr Pathol 110:340–351. doi:10.1016/j.jip.2012.03.022

    Article  CAS  PubMed  Google Scholar 

  • Baumgartner WA, Hawke JP, Bowles K, Varner PW, Hasson KW (2009) Primary diagnosis and surveillance of white spot syndrome virus in wild and farmed crawfish (Procambarus clarkii, P. zonangulus) in Louisiana. USA. Dis Aquat Org 85:15–22. doi:10.3354/dao02051

    Article  CAS  Google Scholar 

  • 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 5:353–357. doi:10.1046/j.1462-5822.2003.00282.x

    Article  CAS  PubMed  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, 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 

  • Culas A (2003) Entwicklung einer molekularbiologischen Methode zum Nachweis des Krebspesterregers Aphanomyces astaci SCHIKORA in nordamerikanischen Flusskrebsen (Pacifastacus leniusculus; Orconectes limosus; Procambarus clarkii). Dissertation, Ludwig-Maximilians-Universität München

  • Cunningham CO (2002) Molecular diagnosis of fish and shellfish diseases: present status and potential use in disease control. Aquaculture 206:19–55. doi:10.1016/S0044-8486(01)00864-X

    Article  CAS  Google Scholar 

  • DAISIE (2009) Handbook of alien species in Europe. Springer, Dordrecht

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449. doi:10.1126/science.287.5452.443

    Article  CAS  PubMed  Google Scholar 

  • Diéguez-Uribeondo J, Cerenius L, Söderhäll K (1995) Physiological adaptations in an Aphanomyces astaci strain from the warm-water crayfish Procambarus clarkii. Mycol Res 99:574–578. doi:10.1016/S0953-7562(09)80716-8

    Article  Google Scholar 

  • Dümpelmann C, Bonacker F, Häckl M (2009) Erstnachweis des Roten Amerikanischen Sumpfkrebses Procambarus clarkii (Decapoda: cambaridae) in Hessen. Lauterbornia 67:39–47

    Google Scholar 

  • Edgerton BF (2004) Susceptibility of the Australian freshwater crayfish Cherax destructor albidus to white spot syndrome virus (WSSV). Dis Aquat Org 59:187–193. doi:10.3354/dao059187

    Article  PubMed  Google Scholar 

  • Feria TP, Faulkes Z (2011) Forecasting the distribution of Marmorkrebs, a parthenogenetic crayfish with high invasive potential, in Madagascar, Europe, and North America. Aquat Invasions 6:55–67. doi:10.3391/ai.2011.6.1.07

    Article  Google Scholar 

  • Filipová L, Holdich DM, Lesobre J, Grandjean F, Petrusek A (2010) Cryptic diversity within the invasive virile crayfish Orconectes virilis (Hagen, 1870) species complex: new lineages recorded in both native and introduced ranges. Biol Invasions 12:983–989. doi:10.1007/s10530-009-9526-0

    Article  Google Scholar 

  • Filipová L, Petrusek A, Matasová K, Delaunay C, Grandjean F (2013) Prevalence of the crayfish plague pathogen Aphanomyces astaci in populations of the signal crayfish Pacifastacus leniusculus in France: evaluating the threat to native crayfish. PLoS ONE 8:e70157. doi:10.1371/journal.pone.0070157

    Article  PubMed Central  PubMed  Google Scholar 

  • Fisher MC, Garner TWJ (2007) The relationship between the emergence of Batrachochytrium dendrobatidis, the wildlife trade in amphibians and introduced amphibian species. Fungal Biol Rev 21:2–9. doi:10.1016/j.fbr.2007.02.002

    Article  Google Scholar 

  • Flegel TW (2009) Current status of viral diseases in Asian shrimp aquaculture. Isr J Aquacult Bamidgeh 61:229–239

    Google Scholar 

  • Gozlan RE, Peeler EJ, Longshaw M, St-Hilaire S, Feist SW (2006) Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes Infect 8:1358–1364. doi:10.1016/j.micinf.2005.12.010

    Article  PubMed  Google Scholar 

  • Gross H (2013) Blauer Floridakrebs (Procambraus alleni) im Rhein! Forum Flusskrebse 19:33–36

    Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–322. doi:10.1098/rspb.2002.2218

    Article  CAS  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 11:394–395. doi:10.1051/kmae/2009025

    Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18. doi:10.1111/j.1365-2664.2008.01600.x

    Article  Google Scholar 

  • Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J et al (2008) Grasping at the routes of biological invasions: framework for integrating pathways into policy. J Appl Ecol 45:403–414. doi:10.1111/j.1365-2664.2007.01442.x

    Article  Google Scholar 

  • Janský V, Mutkovič A (2010) Marbled crayfish —Procambarus sp. (Crustacea: decapoda: cambaridae)—first find in Slovakia. Acta Rer Natur Mus Nat Slov 56:64–67

    Google Scholar 

  • Jiravanichpaisal P, Söderhäll K, Söderhäll I (2004) Effect of water temperature on the immune response and infectivity pattern of white spot syndrome virus (WSSV) in freshwater crayfish. Fish Shellfish Immun 17:265–275. doi:10.1016/j.fsi.2004.03.010

    Article  CAS  Google Scholar 

  • Kim JH, Hayward CJ, Joh SJ, Heo GJ (2002) Parasitic infections in live freshwater tropical fishes imported to Korea. Dis Aquat Org 52:169–173. doi:10.3354/dao052169

    Article  CAS  PubMed  Google Scholar 

  • Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05. doi:10.1051/kmae/2014007

    Article  Google Scholar 

  • Kozubíková E, Vrålstad T, Filipová L, Petrusek A (2011) Re-examination of the prevalence of Aphanomyces astaci in North American crayfish populations in Central Europe by TaqMan MGB real-time PCR. Dis Aquat Org 97:113–125. doi:10.3354/dao02411

    Article  PubMed  Google Scholar 

  • Lightner DV (2011) Viral diseases of farmed shrimp in the Western Hemisphere (the Americas): a review. J Invertebr Pathol 106:110–130. doi:10.1016/j.jip.2010.09.012

    Article  CAS  PubMed  Google Scholar 

  • Lo CF, Leu JH, Ho CH, Chen CH, Peng SE, Chen YT, Chou CM, Yeh PY, Huang CJ, Chou HY et al (1996) Detection of baculovirus associated with white spot syndrome (WSBV) in penaeid shrimps using polymerase chain reaction. Dis Aquat Org 25:133–141. doi:10.3354/dao025133

    Article  CAS  Google Scholar 

  • Longshaw M, Bateman KS, Stebbing P, Stentiford GD, Hockley FA (2012) Disease risks associated with the importation and release of non-native crayfish species into mainland Britain. Aquat Biol 16:1–15. doi:10.3354/ab00417

    Article  Google Scholar 

  • Makkonen J, Kokko H, Vainikka A, Kortet R, Jussila J (2014) Dose-dependent mortality of the noble crayfish (Astacus astacus) to different strains of the crayfish plague (Aphanomyces astaci). J Invertebr Pathol 115:86–91. doi:10.1016/j.jip.2013.10.009

    Article  CAS  PubMed  Google Scholar 

  • McColl KA, Slater J, Jeyasken G, Hyatt AD, Crane MS (2004) Detection of white spot syndrome virus and yellowhead virus in prawns imported into Australia. Aust Vet J 82:69–74

    Article  CAS  PubMed  Google Scholar 

  • Oidtmann B (2012) Crayfish plague (Aphanomyces astaci). Manual of Diagnostic Tests for Aquatic Animals 2012. World Organization for Animal Health, Paris, pp 101–118

    Google Scholar 

  • Oidtmann B, Geiger S, Steinbauer P, Culas A, Hoffmann RW (2006) Detection of Aphanomyces astaci in North American crayfish by polymerase chain reaction. Dis Aquat Org 72:53–64. doi:10.3354/dao072053

    Article  CAS  PubMed  Google Scholar 

  • OIE (2012) Manual of Diagnostic Tests for Aquatic Animals 2012. OIE—World Organisation for Animal Health, Paris

  • Palumbi SR, Martin A, Romano S, MacMillan W, Stice L, Grabowski G (1991) The simple fool’s guide to PCR (Ver. 2). University of Hawaii Press, Honolulu

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

    Google Scholar 

  • Peay S (2009) Invasive non-indigenous crayfish species in Europe: recommendations on managing them. Knowl Manag Aquat Ecosyst 03:394–395. doi:10.1051/kmae/2010009

    Google Scholar 

  • Pedraza-Lara C, Doadrio I, Breinholt JW, Crandall KA (2012) Phylogeny and evolutionary patterns in the dwarf crayfish subfamily (Decapoda: cambarellinae). PLoS ONE 7:e48233. doi:10.1371/journal.pone.0048233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peeler EJ, Oidtmann BC, Midtlyng PM, Miossec L, Gozlan RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biol Invasions 13:1291–1303. doi:10.1007/s10530-010-9890-9

    Article  Google Scholar 

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

  • Reynolds J, Souty-Grosset C, Richardson A (2013) Ecological roles of crayfish in freshwater and terrestrial habitats. Freshw Crayfish 19:197–218. doi:10.5869/fc.2013.v19-2.197

    Google Scholar 

  • Rezinciuc S, Galindo J, Montserrat J, Diéguez-Uribeondo J (2014) AFLP-PCR and RAPD-PCR evidences of the transmission of the pathogen Aphanomyces astaci (Oomycetes) to wild populations of European crayfish from the invasive crayfish species, Procambarus clarkii. Fungal Biol 118:612–620. doi:10.1016/j.funbio.2013.10.007

    Article  CAS  PubMed  Google Scholar 

  • Rodgers CJ, Mohan CV, Peeler EJ (2011) The spread of pathogens through trade in aquatic animals and their products. Rev Sci Tech OIE 30:241–256

    CAS  Google Scholar 

  • Schrimpf A, Chucholl C, Schmidt T, Schulz R (2013) Crayfish plague agent detected in populations of the invasive North American crayfish Orconectes immunis (Hagen, 1870) in the Rhine River, Germany. Aquat Invasions 8:103–109. doi:10.3391/ai.2013.8.1.12

    Article  Google Scholar 

  • Schrimpf A, Schmidt T, Schulz R (2014) Invasive Chinese mitten crab (Eriocheir sinensis) transmits crayfish plague pathogen (Aphanomyces astaci). Aquat Invasions 9:203–209. doi:10.3391/ai.2014.9.2.09

    Article  Google Scholar 

  • Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357. doi:10.1111/j.1523-1739.2006.00524.x

    Article  PubMed  Google Scholar 

  • Smith KF, Behrens MD, Sax DF (2009) Local scale effects of disease on biodiversity. EcoHealth 6:287–295. doi:10.1007/s10393-009-0254-9

    Article  PubMed  Google Scholar 

  • Söderhäll K, Cerenius L (1999) The crayfish plague fungus: history and recent advances. Freshw Crayfish 12:11–35

    Google Scholar 

  • Stentiford GD, Bonami JR, Alday-Sanz V (2009) A critical review of susceptibility of crustaceans to Taura syndrome, yellowhead disease and white spot disease and implications of inclusion of these diseases in European legislation. Aquaculture 291:1–17. doi:10.1016/j.aquaculture.2009.02.042

    Article  Google Scholar 

  • Stentiford GD, Oidtmann B, Scott A, Peeler EJ (2010) Crustacean diseases in European legislation: implications for importing and exporting nations. Aquaculture 306:27–34. doi:10.1016/j.aquaculture.2010.06.004

    Article  Google Scholar 

  • Strand DA, Jussila J, Viljamaa-Dirks S, Kokko H, Makkonen J, Holst-Jensen A, Viljugrein H (2012) Vrålstad T (2012) Monitoring the spore dynamics of Aphanomyces astaci in the ambient water of latent carrier crayfish. Vet Microbiol 160:99–107. doi:10.1016/j.vetmic.05.008

    Article  PubMed  Google Scholar 

  • Svoboda J, Kozubíková-Balcarová E, Kouba A, Buřič M, Kozák P, Diéguez-Uribeondo J, Petrusek A (2013) Temporal dynamics of spore release of the crayfish plague pathogen from its natural host, American spiny-cheek crayfish (Orconectes limosus), evaluated by transmission experiments. Parasitology 140:792–801. doi:10.1017/S0031182012002223

    Article  CAS  PubMed  Google Scholar 

  • Svoboda J, Mrugała A, Kozubíková-Balcarová E, Kouba A, Diéguez-Uribeondo J, Petrusek A (2014a) Resistance to the crayfish plague pathogen, Aphanomyces astaci, in two freshwater shrimps. J Invertebr Pathol 121:97–104. doi:10.1016/j.jip.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  • Svoboda J, Strand DA, Vrålstad T, Grandjean F, Edsman L, Kozák P, Kouba A, Fristad RF, Bahadir Koca S, Petrusek A (2014b) The crayfish plague pathogen can infect freshwater-inhabiting crabs. Freshw Biol 59:918–929. doi:10.1111/fwb.12315

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Masatoshi N, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taylor CA, Knouft JH (2006) Historical influences on genital morphology among sympatric species: gonopod evolution and reproductive isolation in the crayfish genus Orconectes (Cambaridae). Biol J Linn Soc 89:1–12. doi:10.1111/j.1095-8312.2006.00637.x

    Article  Google Scholar 

  • Tilmans M, Mrugała A, Svoboda J, Engelsma MY, Petie M, Soes DM, Nutbeam-Tuffs S, Oidtmann B, Roessink I, Petrusek A (2014) Survey of the crayfish plague pathogen presence in the Netherlands reveals a new Aphanomyces astaci carrier. J Invertebr Pathol 120:74–79. doi:10.1016/j.jip.2014.06.002

    Article  CAS  PubMed  Google Scholar 

  • Tricarico E (2012) A review on pathways and drivers of use regarding non-native freshwater fish introductions in the Mediterranean region. Fish Manag Ecol 19:133–141. doi:10.1111/j.1365-2400.2011.00834.x

    Article  Google Scholar 

  • Unestam T (1975) Defence reactions in and susceptibility of Australian and New Guinea freshwater crayfish to European crayfish plague fungus. Aust J Exp Biol Med 53:349–359

    Article  Google Scholar 

  • Viljamaa-Dirks S, Heinikainen S (2006) Improved detection of crayfish plague with a modified isolation method. Freshw Crayfish 15:376–382

    Google Scholar 

  • Viljamaa-Dirks S, Heinikainen S, Torssonen H, Pursiainen M, Mattila J, Pelkonen S (2013) Distribution and epidemiology of the crayfish plague agent Aphanomyces astaci genotypes from noble crayfish Astacus astacus in Finland. Dis Aquat Org 103:199–208. doi:10.3354/dao02575

    Article  CAS  PubMed  Google Scholar 

  • Vrålstad T, Knutsen AK, Tengs T, Holst-Jensen A (2009) A quantitative TaqMan® MGB real-time polymerase chain reaction based assay for detection of the causative agent of crayfish plague Aphanomyces astaci. Vet Microbiol 137:146–155. doi:10.1016/j.vetmic.2008.12.022

    Article  PubMed  Google Scholar 

  • Wang CS, Tang KFJ, Kou GH, Chen SN (1997) Light and electron microscopic evidence of white spot disease in the giant tiger shrimp, Penaeus monodon (Fabricius), and the kuruma shrimp, Penaeus japonicus (Bate), cultured in Taiwan. J Fish Dis 20:323–331. doi:10.1046/j.1365-2761.1997.00301.x

    Article  Google Scholar 

  • Whittington RJ, Chong R (2007) Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 81:92–116. doi:10.1016/j.prevetmed.2007.04.007

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The study has been partially funded by the Czech Science Foundation (Project No. P505/12/0545). A.M. was supported by the Charles University in Prague (Project SVV 267204). E.K.-B. was supported by the Project No. CZ.1.07/2.3.00/30.0022 of the Education for Competitiveness Operational Programme (ECOP) co-financed by the European Social Fund and the State Budget of the Czech Republic. We thank Michelle Pond and Kelly Bateman for their support with the WSSV molecular detection, Jiří Patoka and Petr Difko for providing crayfish from some Czech sources, and Jiří Svoboda for technical support. Anonymous referees provided useful comments to previous versions of the manuscript.

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  1. Department of Ecology, Faculty of Science, Charles University in Prague, Viničná 7, Prague 2, 12844, Czech Republic

    A. Mrugała, E. Kozubíková-Balcarová, S. Cabanillas Resino, J. Vukić & A. Petrusek

  2. Fisheries Research Station Baden-Württemberg, Argenweg 50/1, 88085, Langenargen, Germany

    C. Chucholl

  3. OIE Reference Laboratory for Crayfish Plague, Finnish Food Safety Authority Evira, 70701, Kuopio, Finland

    S. Viljamaa-Dirks

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  1. A. Mrugała
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Mrugała, A., Kozubíková-Balcarová, E., Chucholl, C. et al. Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol Invasions 17, 1313–1326 (2015). https://doi.org/10.1007/s10530-014-0795-x

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