Detection of crayfish plague spores in large freshwater systems

Journal of Applied Ecology

Volumn 51, Issue 2, 2014, Pages 544-553

  Strand, David A ^a,b   Jussila, Japo ^c   Johnsen, Stein I ^d   Viljamaa Dirks, Satu ^e   Edsman, Lennart ^f   Wiik Nielsen, Jannicke ^a   Viljugrein, Hildegunn ^a   Engdahl, Frederik ^f   Vrålstad, Trude ^a,b  

^a NORWEGIAN VETERINARY INSTITUTE   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d NORWEGIAN INSTITUTE FOR NATURE RESEARCH   (Norway)

^e NATL VET AND FOOD RES INSTITUTE   (Finland)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Alien species; Aphanomyces astaci; Dead end ultrafiltration; Depth filtration; Disease surveillance; Environmental DNA; Environmental monitoring; Glass fibre filter; Pacifastacus leniusculus; Signal crayfish

Indexed keywords

ABUNDANCE; AQUATIC ENVIRONMENT; CRAYFISH; DETECTION METHOD; DEVELOPMENTAL BIOLOGY; DISEASE TRANSMISSION; DNA; ENVIRONMENTAL MONITORING; FILTER; FILTRATION; FRESHWATER ECOSYSTEM; HOST-PATHOGEN INTERACTION; INVASIVE SPECIES; NUMERICAL MODEL; OPTIMIZATION; POLYMERASE CHAIN REACTION; RISK ASSESSMENT;

NORTH AMERICA; NORTHERN EUROPE;

APHANOMYCES; APHANOMYCES ASTACI; ASTACOIDEA; ASTACUS ASTACUS; BACTERIA (MICROORGANISMS); PACIFASTACUS LENIUSCULUS; PONTASTACUS LEPTODACTYLUS;

EID: 84896394346     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/1365-2664.12218     Document Type: Article

References (39)

1. Alderman, D.J. & Polglase, J.L. (1986) Aphanomyces astaci - Isolation and culture. Journal of Fish Diseases, 9, 367-379.
2. Aw, T.G. & Rose, J.B. (2012) Detection of pathogens in water: from phylochips to qPCR to pyrosequencing. Current Opinion in Biotechnology, 23, 422-430.
3. Bohman, P., Nordwall, F. & 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.
4. Darling, J.A. & Mahon, A.R. (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environmental Research, 111, 978-988.
5. Diéguez-Uribeondo, J. (2006) Pathogens, parasites and ectocommensals. Atlas of Crayfish in Europe (eds C. Souty-Grosset, D.M. Holdich, P.Y. Noël, J.D. Reynolds & P. Haffner ), pp. 133-149. Muséum national d'histoire naturelle, Paris.
6. Diéguez-Uribeondo, J., Huang, T.S., Cerenius, L. & Söderhäll, K. (1995) Physiological adaptation of an Aphanomyces astaci strain isolated from the freshwater crayfish Procambarus clarkii. Mycological Research, 99, 574-578.
7. Dolan, J.R. & Stoeck, T. (2011) Repeated sampling reveals differential variability in measures of species richness and community composition in planktonic protists. Environmental Microbiology Reports, 3, 661-666.
8. Edgerton, B.F., Henttonen, P., Jussila, J., Mannonen, A., Paasonen, P., Taugbol, T., Edsman, L. & Souty-Grosset, C. (2004) Understanding the causes of disease in European freshwater crayfish. Conservation Biology, 18, 1466-1474.
9. 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.
10. Gibson, K.E. & Schwab, K.J. (2011) Tangential-flow ultrafiltration with integrated inhibition detection for recovery of surrogates and human pathogens from large-volume source water and finished drinking water. Applied and Environmental Microbiology, 77, 385-391.
11. Guy, R.A., Payment, P., Krull, U.J. & Horgen, P.A. (2003) Real-time PCR for quantification of Giardia and Cryptosporidium in environmental water samples and sewage. Applied and Environmental Microbiology, 69, 5178-5185.
12. He, J.W. & Jiang, S. (2005) Quantification of enterococci and human adenoviruses in environmental samples by real-time PCR. Applied and Environmental Microbiology, 71, 2250-2255.
13. Holdich, D.M., Reynolds, J.D., Souty-Grosset, C. & Sibley, P.J. (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems, 394-395, 11.
14. 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. Diseases of Aquatic Organisms, 97, 113-125.
15. Lindquist, H.D.A., Harris, S., Lucas, S., Hartzel, M., Riner, D., Rochele, P. & DeLeon, R. (2007) Using ultrafiltration to consentrate and detect Bacillus anthracis, Bacillus atrophaeus subspecies globigii, and Cryptosporidium parvum in 100-liter water samples. Journal of Microbiological Methods, 70, 484-492.
16. Lodge, D.M., Turner, C.R., Jerde, C.L., Barnes, M.A., Chadderton, L., Egan, S.P., Feder, J.L., Mahon, A.R. & Pfrender, M.E. (2012) Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA. Molecular Ecology, 21, 2555-2558.
17. Makkonen, J., Strand, D.A., Kokko, H., Vrålstad, T. & Jussila, J. (2013) Timing and quantifying Aphanomyces astaci sporulation from the noble crayfish suffering from the crayfish plague. Veterinary Microbiology, 162, 750-755.
18. Mull, B. & Hill, V.R. (2012) Recovery of diverse microbes in high turbidity surface water samples using dead-end ultrafiltration. Journal of Microbiological Methods, 91, 429-433.
19. Oidtmann, B., Geiger, S., Steinbauer, P., Culas, A. & Hoffmann, R.W. (2006) Detection of Aphanomyces astaci in North American crayfish by polymerase chain reaction. Diseases of Aquatic Organisms, 72, 53-64.
20. OIE (Office international des e'pizooties) (2012) Crayfish plague (Aphanomyces astaci). Chapter 2.2.1. Manual of Diagnostic Tests for Aquatic Animals 2012 (Ed. World Organization for Animal Health), pp. 101-118. Office international des e'pizooties, Paris. http://www.oie.int/international-standard-setting/aquatic-manual/access-online/ (accessed 9 January 2013).
21. Pârvulescu, L., Schrimpf, A., Kozubíková, E., Cabanillas, R.S., Vrålstad, T., Petrusek, A. & 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.
22. Pratten, D.J. (1980) Growth in the crayfish Austropotamobius pallipes (Crustacea: Astacidae). Freshwater Biology, 10, 401-402.
23. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
24. Santo Domingo, J.W., Siefring, S.C. & Haugland, R.A. (2003) Real-time PCR method to detect Enterococcus faecalis in water. Biotechnology Letters, 25, 261-265.
25. Schrimpf, A., Chucholl, C., Schmidt, T. & Schulz, R. (2013a) Crayfish plague agent detected in populations of the invasive North American crayfish Orconectes immunis (Hagen, 1870) in the Rhine River, Germany. Aquatic Invasions, 8, 103-109.
26. Schrimpf, A., Mainwald, T., Vrålstad, T., Schulz, H.K., Śmietana, P. & Schultz, R. (2013b) Absence of the crayfish plague pathogen (Aphanomyces astaci) facilitates coexistence of European and American crayfish in central Europe. Freshwater Biology, 58, 1116-1125.
27. Smith, C.M. & Hill, V.R. (2009) Dead-end hollow-fiber ultrafiltration for recovery of diverse microbes from water. Applied and Environmental Microbiology, 75, 5284-5289.
28. Söderhäll, K. & Cerenius, L. (1999) The crayfish plague fungus: history and recent advances. Freshwater Crayfish, 12, 11-35.
29. Strand, D.A. (2013) Environmental DNA monitoring of the alien crayfish plague pathogen Aphanomyces astaci in freshwater systems - Sporulation dynamics, alternative hosts and improved management tools. PhD thesis, Department of Biosciences, University of Oslo, Oslo, Norway.
30. Strand, D.A., Holst-Jensen, A., Viljugrein, H., Edvardsen, B., Klaveness, D., Jussila, J. & 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.
31. Strand, D.A., Jussila, J., Viljamaa-Dirks, S., Kokko, H., Makkonen, J., Holst-Jensen, A., Viljugrein, H. & Vrålstad, T. (2012) Monitoring the spore dynamics of Aphanomyces astaci in the ambient water of latent carrier crayfish. Veterinary Microbiology, 160, 99-107.
32. Svoboda, J., Kozubíková-Balcarová, E., Kouba, A., Buřič, M., Kozák, P. & Diéguez-Uribeondo, J. (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.
33. Thomsen, P.F., Kielgast, J., Iversen, L.L., Wiuf, C., Rasmussen, M., Gilbert, M.T.P., Orlando, L. & Willerslev, E. (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565-2573.
34. Varma, M., Hester, J.D., Schaefer, F.W., Ware, M.W. & Lindquist, H.D.A. (2003) Detection of Cyclospora cayetanensis using a quantitative real-time PCR assay. Journal of Microbiological Methods, 53, 27-36.
35. Viljamaa-Dirks, S. & Heinikainen, S. (2006) Improved detection of crayfish plague with a modified isolation method. Freshwater Crayfish, 15, 376-382.
36. ® MGB real-time polymerase chain reaction based assay for detection of the causative agent of crayfish plague Aphanomyces astaci. Veterinary Microbiology, 137, 146-155.
37. Vrålstad, T., Johnsen, S.I., Fristad, R.F., Edsman, L. & Strand, D. (2011) Potent infection reservoir of crayfish plague now permanently established in Norway. Diseases of Aquatic Organisms, 97, 75-83.
38. Westman, K. & Nylund, V. (1978) Crayfish plague, Aphanomyces astaci, observed in the European crayfish, Astacus astacus, in Pihlajavesi Waterway in Finland. A case study on the spread of the plague fungus. Freshwater Crayfish, 4, 419-426.
39. Zinger, L., Gobet, A. & Pommier, T. (2012) Two decades of describing the unseen majority of aquatic microbial diversity. Molecular Ecology, 21, 1878-1896.