Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-13T01:45:53.215Z Has data issue: false hasContentIssue false
  • English
  • Français

The prevalence of Aphanomyces astaci in invasive signal crayfish from the UK and implications for native crayfish conservation

Published online by Cambridge University Press:  12 January 2017

J. JAMES ,
S. NUTBEAM-TUFFS ,
J. CABLE ,
A. MRUGAŁA ,
N. VIÑUELA-RODRIGUEZ ,
A. PETRUSEK  and
B. OIDTMANN
J. JAMES*
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
S. NUTBEAM-TUFFS
Affiliation:
The Roslin Institute, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK Centre for Environment, Fisheries and Aquaculture Science (Cefas), The Nothe, Weymouth, Dorset DT4 8UB, UK
J. CABLE
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
A. MRUGAŁA
Affiliation:
Department of Ecology, Faculty of Science, Charles University, Viničná 7, CZ-12844 Prague 2, Czech Republic
N. VIÑUELA-RODRIGUEZ
Affiliation:
Department of Ecology, Faculty of Science, Charles University, Viničná 7, CZ-12844 Prague 2, Czech Republic
A. PETRUSEK
Affiliation:
Department of Ecology, Faculty of Science, Charles University, Viničná 7, CZ-12844 Prague 2, Czech Republic
B. OIDTMANN
Affiliation:
Centre for Environment, Fisheries and Aquaculture Science (Cefas), The Nothe, Weymouth, Dorset DT4 8UB, UK
*
*Corresponding author: School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK. E-mail: jamesj12@cardiff.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The crayfish plague agent, Aphanomyces astaci, has spread throughout Europe, causing a significant decline in native European crayfish. The introduction and dissemination of this pathogen is attributed to the spread of invasive North American crayfish, which can act as carriers for A. astaci. As native European crayfish often succumb to infection with A. astaci, determining the prevalence of this pathogen in non-native crayfish is vital to prioritize native crayfish populations for managed translocation. In the current study, 23 populations of invasive signal crayfish (Pacifastacus leniusculus) from the UK were tested for A. astaci presence using quantitative PCR. Altogether, 13 out of 23 (56·5%) populations were found to be infected, and pathogen prevalence within infected sites varied from 3 to 80%. Microsatellite pathogen genotyping revealed that at least one UK signal crayfish population was infected with the A. astaci genotype group B, known to include virulent strains. Based on recent crayfish distribution records and the average rate of signal crayfish population dispersal, we identified one native white-clawed crayfish (Austropotamobius pallipes) population predicted to come into contact with infected signal crayfish within 5 years. This population should be considered as a priority for translocation.

Keywords

Pacifastacus leniusculuscrayfish plaguewhite-clawed crayfishAustropotamobius pallipesArk Sites
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 411 - 418
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Both authors contributed equally to this study.

References

REFERENCES

Alderman, D. J. (1996). Geographical spread of bacterial and fungal diseases of crustaceans. Scientific and Technical Review of the Office International des Epizooties 15, 603–632.Google Scholar
Alderman, D. J., Polglase, J. L., Frayling, M. and Hogger, J. (1984). Crayfish plague in Britain. Journal of Fish Diseases 7, 401–405.Google Scholar
Alderman, D. J., Holdich, D. and Reeve, I. (1990). Signal crayfish as vectors in crayfish plague in Britain. Aquaculture 86, 3–6.CrossRefGoogle Scholar
Becking, T., Mrugała, A., Delaunay, C., Svoboda, J., Raimond, M., Viljamaa-Dirks, S., Petrusek, A., Grandjean, F. and Braquart-Varnier, C. (2015). Effect of experimental exposure to differently virulent Aphanomyces astaci strains on the immune response of the noble crayfish Astacus astacus . Journal of Invertebrate Pathology 132, 115–124.CrossRefGoogle ScholarPubMed
Bohman, P., Nordwall, F. and Edsman, L. (2006). The effect of the large-scale introduction of signal crayfish on the spread of crayfish plague in Sweden. Bulletin Français de la Pêche et de la Pisciculture 380–381, 1291–1302.CrossRefGoogle Scholar
Bubb, D. H., Thom, T. J. and Lucas, M. C. (2004). Movement and dispersal of the invasive signal crayfish Pacifastacus leniusculus in upland rivers. Freshwater Biology 49, 357–368.Google Scholar
Cerenius, L., Bangyeekhun, E., Keyser, P., Söderhäll, I. and Söderhäll, K. (2003). Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci . Cellular Microbiology 5, 353–357.Google Scholar
DAISIE, 2009. Handbook of Alien Species in Europe. Springer, Dordrecht.Google Scholar
Diéguez-Uribeondo, J., Temiño, C. and Múzquiz, J. L. (1997). The crayfish plague fungus (Aphanomyces astaci) in Spain. Bulletin Français de la Pêche et de la Pisciculture 347, 753–763.Google Scholar
Dunn, J. C., McClymont, H. E., Christmas, M. and Dunn, A. M. (2009). Competition and parasitism in the native white clawed crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK. Biological Invasions 11, 315–324.Google Scholar
Filipová, L., Petrusek, A., Matasová, K., Delaunay, C. and Grandjean, F. (2013). Prevalence of the crayfish plague pathogen Aphanomyces astaci in population of the signal crayfish Pacifastacus leniusculus in France: evaluating the threat to native crayfish. PLoS ONE 8, e70157.Google Scholar
Grandjean, F., Vrålstad, T., Diéguez-Uribeondo, J., Jelić, M., Mangombi, J., Delaunay, C., Filipová, L., Rezinciuc, S., Kozubíková-Balcarová, E., Guyonnet, D., Viljamaa-Dirks, S. and Petrusek, A. et al. (2014). Microsatellite markers for direct genotyping of the crayfish plague pathogen Aphanomyces astaci (Oomycetes) from infected host tissues. Veterinary Microbiology 170, 317–324.Google Scholar
Holdich, D. M. (2003). Crayfish in Europe – an overview of the taxonomy, legislation, distribution, and crayfish plague outbreaks. In Management and Conservation of Crayfish, Conference Proceedings, Nottingham, UK, November 7th 2002 (ed. Holdich, D. M. and Sibley, P. J.), pp. 15–34. Environment Agency, Rio House, Bristol, UK.Google Scholar
Holdich, D. M. and Reeve, I. D. (1991). Distribution of freshwater crayfish in the British Isles, with particular reference to crayfish plague, alien introduction and water quality. Aquatic Conservation Marine and Freshwater Ecosystems 1, 139–158.Google Scholar
Holdich, D. M. and Sibley, P. J. (2009). ICS and NICS in Britain in the 2000s. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), March 25, 2009, Leeds, UK, pp. 13–33.Google Scholar
Holdich, D. M., Rogers, W. D. and Reynolds, J. D. (1999). Native and alien crayfish in the British Isles. In Crayfish in Europe as Alien Species: How to Make the Best of a Bad Situation? (ed. Gherardi, F. and Holdich, D. M.), Crustacean Issues 11, pp. 221–235. A. A. Balkema, Rotterdam.Google Scholar
Holdich, D. M., Palmer, M. and Sibley, P. J. (2009). The indigenous status of Austropotamobius pallipes (Lereboullet) in Britain. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), March 25, 2009, Leeds, UK, pp. 1–12.Google Scholar
Holdich, D. M., James, J., Jackson, C. and Peay, S. (2014). The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain. Ethology Ecology and Evolution 26, 232–262.Google Scholar
Huang, T., Cerenius, L. and Söderhall, K. (1994). Analysis of genetic diversity in the crayfish plague fungus, Aphanomyces astaci, by random amplification of polymorphic DNA. Aquaculture 126, 1–9.CrossRefGoogle Scholar
Hudina, S., Faller, M., Lucic, A., Klobucar, G. and Maguire, I. (2009). Distribution and dispersal of two invasive crayfish species in the Drava River basin, Croatia. Knowledge and Management of Aquatic Ecosystems 394–395, 9.Google Scholar
IUCN (2015). The IUCN red list of threatened species [online]. www.iucnredlist.org [accessed on 28.10.15].Google Scholar
James, J., Slater, F. and Cable, J. (2014). A.L.I.E.N. databases: addressing the lack in establishment of non-natives databases. Crustaceana 87, 1192–1199.Google Scholar
James, J., Thomas, J. R., Ellis, A., Young, K. A., England, J. and Cable, J. (2016). Over-invasion in a freshwater ecosystem: newly introduced virile crayfish (Orconectes virilis) outcompete established invasive signal crayfish (Pacifastacus leniusculus). Marine and Freshwater Behaviour and Physiology 49, 9–18.CrossRefGoogle Scholar
Jussila, J., Makkonen, J., Vainikka, A., Kortet, R. and Kokko, H. (2011). Latent crayfish plague (Aphanomyces astaci) infection in a robust wild noble crayfish (Astacus astacus) population. Aquaculture 321, 17–20.Google Scholar
Kokko, H., Koistinen, L., Harlioğlu, M. M., Makkonen, J., Aydin, H. and Jussila, J. (2012). Recovering Turkish narrow clawed crayfish (Astacus leptodactylus) populations carry Aphanomyces astaci . Knowledge and Management of Aquatic Ecosystems 404, 1–7.Google Scholar
Kozubíková, E., Petrusek, A., Ďuriš, Z., Martín, M. P., Diéguez-Uribeondo, J. and Oidtmann, B. (2008). The old menace is back: recent crayfish plague outbreaks in the Czech Republic. Aquaculture 274, 208–217.Google Scholar
Kozubíková, E., Filipová, L., Kozák, P., Ďuriš, Z., Diéguez-Uribeondo, J., Oidtmann, B. and Petrusek, A. (2009). Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conservation Biology 22, 1204–1213.Google Scholar
Kozubíková, E., Vrålstad, T., Filipová, L. and 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. Diseases of Aquatic Organisms 97, 113–125.Google Scholar
Kušar, D., Vrezec, A., Ocepek, M. and Jenčič, V. (2013). Aphanomyces astaci in wild crayfish populations in Slovenia: first report of persistent infection in a stone crayfish (Austropotamobius torrentium) population. Diseases of Aquatic Organisms 103, 157–169.Google Scholar
Lilley, J. H., Cerenius, L. and Söderhäll, K. (1997). RAPD evidence for the origin of crayfish plague outbreaks in Britain. Aquaculture 157, 181–185.CrossRefGoogle Scholar
Lowe, S., Browne, M., Boudjelas, S. and De Poorter, M. (2004). 100 of the World's Worst Invasive Alien Species. A selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the IUCN, Gland, Switzerland.Google Scholar
Maguire, I., Jelić, M., Klobučar, G., Delpy, M., Delaunay, C. and Grandjean, F. (2016). Prevalence of the pathogen Aphanomyces astaci in freshwater crayfish populations in Croatia. Diseases of Aquatic Organisms 118, 45–53.Google Scholar
Makkonen, J., Jussila, J., Kortet, R., Vainikka, A. and Kokko, H. (2012). Differing virulence of Aphanomyces astaci isolates and elevated resistance of noble crayfish Astacus astacus against crayfish plague. Diseases of Aquatic Organisms 102, 129–136.CrossRefGoogle ScholarPubMed
Mrugała, A., Kawai, T., Kozubíková-Balcarová, E. and Petrusek, A. (2016). Aphanomyces astaci presence in Japan: a threat to the endemic and endangered crayfish species Cambaroides japonicus? Aquatic Conservation: Marine and Freshwater Ecosystems, doi: 10.1002/aqc.2674.Google Scholar
Oidtmann, B. (2012). Crayfish plague (Aphanomyces astaci). In Manual of Diagnostic Tests for Aquatic Animals 2012. Chapter 2·2·1, pp. 101–118. World Organisation of Animal Health, Office international des epizooties, Chapter 2·2·1, pp. 101–118. Paris.Google Scholar
Oidtmann, B., Heitz, E., Rogers, D. and Hoffman, R. W. (2002). Transmission of crayfish plague. Diseases of Aquatic Organisms 52, 159–167.Google Scholar
Oidtmann, B., Geiger, S., Steinbauer, P., Culas, A. and Hoffmann, R. W. (2006). Detection of Aphanomyces astaci in North American crayfish by polymerase chain reaction. Diseases of Aquatic Organisms 72, 53–64.Google Scholar
Pârvulescu, L., Schrimpf, A., Kozubíková, E., Cabanillas Resino, S., Vrålstad, T., Petrusek, A. and Schulz, R. (2012). Invasive crayfish and crayfish plague on the move: first detection of the plague agent Aphanomyces astaci in the Romanian Danube. Diseases of Aquatic Organisms 98, 85–94.CrossRefGoogle ScholarPubMed
Peay, S. (2009). Selection criteria for “ark sites” for white-clawed crayfish. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), March 25, 2009, Leeds, UK, pp. 63–70.Google Scholar
R Core Team(2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Royo, F., Andersson, G., Bangyeekhun, E., Múzquiz, J. L., Söderhall, K. and Cerenius, L. (2004). Physiological and genetic characterisation of some new Aphanomyces strains isolated from freshwater crayfish. Veterinary Microbiology 104, 103–112.Google Scholar
Schrimpf, A., Pârvulescu, L., Copilaş Ciocianu, D., Petrusek, A. and Schulz, R. (2012). Crayfish plague in the Danube Delta – a potential threat to biodiversity in southeastern Europe. Aquatic Invasions 7, 503–510.CrossRefGoogle Scholar
Schrimpf, A., Maiwald, T., Vrålstad, T., Schulz, H. K., Śmietana, P. and Schulz, R. (2013). Absence of the crayfish plague pathogen (Aphanomyces astaci) facilitates coexistence of European and American crayfish in central Europe. Freshwater Biology 58, 1116–1125.Google Scholar
Schulz, H. K., Smietána, P., Maiwald, T., Oidtmann, B. and Schulz, R. (2006). Case studies on the co-occurrence of Astacus astacus (L.) and Orconectes limosus (Raf.): snapshots of a slow displacement. Freshwater Crayfish 15, 212–219.Google Scholar
Skov, C., Aarestup, K., Sivebaek, F., Pedersen, S., Vrålstad, T. and Berg, S. (2011). Non-indigenous signal crayfish Pacifastacus leniusculus are now common in Danish streams: preliminary status for national distribution and protective actions. Biological Invasions 13, 1269–1274.Google Scholar
Söderbäck, B. (1994). Interactions among juveniles of two freshwater crayfish species and a predatory fish. Oecologia 100, 229–235.Google Scholar
Stevenson, M., Nunes, T., Sanchez, J., Thornton, R., Reiczigel, J., Robison-Cox, J., Sebastiani, P., Solymos, P., Yoshida, K., Jones, G., Pirikahu, S., Firestone, S. and Kyle, R. (2013) epiR: An R package for the analysis of epidemiological data. R package version 0.9. Online. Available at: https://cran.r-project.org/web/packages/epiR/index.html.Google Scholar
Strand, D. A., Holst-Jensen, A., Viljugrein, H., Edvardsen, B., Klaveness, D., Jussila, J. and Vrålstad, T. (2011). Detection and quantification of the crayfish plague agent in natural waters: direct monitoring approach for aquatic environments. Diseases of Aquatic Organisms 95, 9–17.Google Scholar
Svoboda, J., Strand, D. A., Vrålstad, T., Grandjean, F., Edsman, L., Kozák, P., Kouba, A., Fristad, R. F., Koca, S. B. and Petrusek, A. (2014). The crayfish plague pathogen can infect freshwater-inhabiting crabs. Freshwater Biology 59, 918–929.Google Scholar
Svoboda, J., Mrugała, A., Kozubíková-Balcarová, E. and Petrusek, A. (2017). Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. Journal of Fish Diseases 40, 127–140.Google Scholar
Tilmans, M., Mrugala, A., Svoboda, J., Engelsma, M. Y., Petie, M., Soes, D. M., Nutbeam-Tuffs, S., Oidtmann, B., Rossink, I. and Petrusek, A. (2014). Survey of the crayfish plague pathogen presence in the Netherlands reveals a new Aphanomyces astaci carrier. Journal of Invertebrate Pathology 120, 74–79.Google Scholar
Tuffs, S. and Oidtmann, B. (2011). A comparative study of molecular diagnostic methods designed to detect the crayfish plague pathogen, Aphanomyces astaci . Veterinary Microbiology 153, 343–353.CrossRefGoogle ScholarPubMed
Unestam, T. and Weiss, D. W. (1970). The host-parasite relationship between freshwater crayfish and the crayfish disease fungus Aphanomyces astaci: responses to infection by a susceptible and a resistant species. Journal of General Microbiology 60, 77–90.CrossRefGoogle Scholar
Vennerström, P., Söderhäll, K. and Cerenius, L. (1998). The origin of two crayfish plague (Aphanomyces astaci) epizootics in Finland on noble crayfish, Astacus astacus . Annales Zoologici Fennici 35, 43–46.Google Scholar
Vrålstad, T., Knutsen, A. K., Tengs, T. and 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 . Veterinary Microbiology 137, 146–155.Google Scholar
Weinländer, M. and Füreder, L. (2009). The continuing spread of Pacifastacus leniusculus in Carinthia (Austria): potential reasons, invasiveness and ecological effects. In Proceedings of the Regional European Crayfish Workshop: Future of Native Crayfish in Europe, Písek, p. 53.Google Scholar
Westman, K., Savolainen, R. and Julkunen, M. (2002). Replacement of the native crayfish Astacus astacus by the introduced species Pacifastacus leniusculus in a small, enclosed Finnish lake: a 30-year study. Ecography 25, 53–73.CrossRefGoogle Scholar