Academic Scientific JournalsFirst record of Astathelohania contejeani (Henneguy, 1892) in the narrow-clawed crayfish Pontastacus leptodactylus (Eschscholtz, 1823) from Belarus
DOI:
https://doi.org/10.26881/oahs-2024.1.04Keywords:
Porcelain disease, microsporidiosis, Astathelohania contejeani, narrow-clawed crayfish, Pontastacus leptodactylusAbstract
Porcelain disease, caused by the parasite Astathelohania contejeani, is a fatal disease for freshwater crayfish. Previously published data provide information on the occurrence of A. contejeani in various crayfish species. However, its prevalence in host populations remains largely undetermined. This issue is relevant to the narrow-clawed crayfish Pontastacus leptodactylus, a species of high commercial value in Eastern Europe. A single published report addressed a potential microsporidia infection in P. leptodactylus, but without specific data on geographical location and prevalence. We present the first detailed information on the prevalence of A. contejeani in the P. leptodactylus population from Lake Losvido, including an assessment of the infection rate through both visual and molecular assessment. Astathelohania contejeani was observed in 1.56% of 128 crayfish examined visually. Of the 37 asymptomatic crayfish samples analyzed, 29.7% were found to be carriers. This finding suggests that parasitism of A. contejeani occurs frequently in the P. leptodactylus population in Lake Losvido prior to the manifestation of observable disease symptoms.
Downloads
References
Alekhnovich, A. (2016). Crayfish of Belarus in modern conditions: Distribution, population dynamics, production and commercial potential. [In Russian]. Belaruskaya navuka, Minsk, Belarus.
Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2013). GenBank. Nucleic Acids Research, 41(D1), D36–D42. https://doi. org/10.1093/nar/gks1195 PMID:23193287.
Bojko, J., & Stentiford, G. D. (2022). Microsporidian Pathogens of Aquatic Animals. W L. M. Weiss & A. W. Reinke (Red.), Microsporidia (T. 114, pp. 247–283). Springer International Publishing. https://doi.org/10.1007/978-3-030-93306- 7_10.
Bojko, J., Behringer, D. C., Moler, P., & Reisinger, L. (2020a). Ovipleistophora diplostomuri, a parasite of fish and their trematodes, also infects the crayfish Procambarus bivittatus. Journal of Invertebrate Pathology, 169, 107306. https://doi.org/10.1016/j.jip.2019.107306 PMID:31836486.
Bojko, J., Behringer, D. C., Moler, P., Stratton, C. E. L., & Reisinger, L. (2020b). A new lineage of crayfish-infecting Microsporidia: The Cambaraspora floridanus n. gen. n. sp. (Glugeida: Glugeidae) complex from Floridian freshwaters (USA). Journal of Invertebrate Pathology, 171, 107345. https://doi.org/10.1016/j.jip.2020.107345 PMID:32067978.
Bojko, J., Reinke, A. W., Stentiford, G. D., Williams, B., Rogers, M. S. J., & Bass, D. (2022). Microsporidia: A new taxonomic, evolutionary, and ecological synthesis. Trends in Parasitology, 38(8), 642–659. https://doi.org/10.1016/j. pt.2022.05.007 PMID:35667993.
Brown, D., & Bowler, K. (1977). A population study of the British freshwater crayfish Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, 3(1), 33–49.
Cossins, A. R. (1973). Thelohania contejeani Henneguy, microsporidian parasite of Austropotamobius pallipes Lereboullet - an histological and ultrastructural study. Freshwater Crayfish, 1(1), 151–164.
Cossins, A. R., & Bowler, K. (1974). An histological and ultrastructural study of Thelohania contejeani Henneguy, 1892 (Nosematidae), Microsporidian parasite of the crayfish Austropotamobius pallipes Lereboullet. Parasitology, 68(1), 81–91. https://doi.org/10.1017/S003118200004539X.
Diéguez-Uribeondo, J., Pinedo-Ruiz, J., & Mùzquiz, J. L. (1997a). Thelohania contejeani in the province of Alava, Spain. Bulletin Francais de la Peche et de la Pisciculture, 347, 749– 752. https://doi.org/10.1051/kmae/1997057.
Diéguez-Uribeondo, J., Cerenius, L., Dyková, I., Gelder, S., Henntonen, P., Jiravanichpaisal, P., Lom, J., & Söderhäll, K. (1997b). Pathogens, parasites and ectocommensals. In C. Souty-Grosset, D.M. Holdich, P.Y. Noël, J.D. Reynolds, P. Haffner (Eds.), Atlas of Crayfish in Europe (pp. 135–155). Muséum national d’Histoire naturelle, Paris: Collection Patrimoines Naturels.
Dragičević, P., Bielen, A., Petrić, I., & Hudina, S. (2021). Microbial pathogens of freshwater crayfish: A critical review and systematization of the existing data with directions for future research. Journal of Fish Diseases, 44(3), 221–247. https://doi.org/10.1111/jfd.13314 PMID:3334533.7
Duffield, J. E. (1933). Fluctuations in Numbers among Freshwater Crayfish, Potamobius pallipes Lereboullet. Journal of Animal Ecology, 2(2), 184–196. https://doi.org/10.2307/956.
Dunn, J. C., McClymont, H. E., Christmas, M., & 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(2), 315–324. https://doi. org/10.1007/s10530-008-9249-7.
Edgerton, B. F., Evans, L. H., Stephens, F. J., & Overstreet, R. M. (2002). Synopsis of freshwater crayfish diseases and commensal organisms. Aquaculture (Amsterdam, Netherlands), 206(1–2), 57–135. https://doi.org/10.1016/ S0044-8486(01)00865-1.
Edgerton, B. F., & Jussila, J. (2004). Keynote presentation and roundtable session 4. Crayfish pathology in Europe: Past, present and a programme for the future. Bulletin Francais de la Peche et de la Pisciculture, 372–373, 473–482. https:// doi.org/10.1051/kmae:2004021.
El-Matbouli, M., & Soliman, H. (2006). Molecular diagnostic methods for detection of Thelohania contejeani (Microsporidia), the causative agent of porcelain disease in crayfish. Diseases of Aquatic Organisms, 69, 205–211. https://doi.org/10.3354/dao069205 PMID:16724564.
Evans, L., & Edgerton, B. (2002). Pathogens, parasites and commensals. In D. M. Holdich (Ed.), Biology of Freshwater Crayfish (pp. 377–438). Blackwell Science.
Feller, C., Rinder, H., El-Matbouli, M., & Hoffmann, R. W. (2000). A PCR method for the detection of Thelohania contejeani. Retrieved accessed March 13, 2023, from https://www. ncbi.nlm.nih.gov/nuccore/AF303105.
France, R. L., & Graham, L. (1985). Increased microsporidian parasitism of the crayfish Orconectes virilis in an experimentally acidified lake. Water, Air, and Soil Pollution, 26(2), 129–136. https://doi.org/10.1007/BF00292063.
Goodrich, H. P. (1956). Crayfish epidemics. Parasitology, 46(3- 4), 480–483. https://doi.org/10.1017/S0031182000026615 PMID:13378890.
Haddaway, N. R., Wilcox, R. H., Heptonstall, R. E. A., Griffiths, H. M., Mortimer, R. J. G., Christmas, M., & Dunn, A. M. (2012). Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS One, 7(2), e32229. https://doi.org/10.1371/journal.pone.0032229 PMID:22359673.
Hall, T. (1999). BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Imhoff, E., Mortimer, R., Christmas, M., & Dunn, A. (2009). Porcelain disease in white-clawed and signal crayfish in the UK. In Crayfish Conservation in the British Isles, Proceedings of a conference held on 25th March 2009 in Leeds (pp. 49–56). Leeds, Great Britan.
Imhoff, E., Mortimer, R., Christmas, M., & Dunn, A. (2010). Non-lethal tissue sampling allows molecular screening for microsporidian parasites in signal, Pacifasticus leniusculus (Dana), and vulnerable white-clawed crayfish, Austropotamobius pallipes (Lereboullet). Freshwater Crayfish, 17(1), 145–150.
Imhoff, E., Mortimer, R., Christmas, M., & Dunn, A. (2011). Invasion progress of the signal crayfish (Pacifastacus leniusculus (Dana)) and displacement of the native whiteclawed crayfish (Austropotamobius pallipes (Lereboullet)) in the River Wharfe, UK. Freshwater Crayfish, 18(1), 45–53. https://doi.org/10.5869/fc.2011.v18.45.
Krucińska, J., & Simon, E. (1968). On the parasites and epibionts of the branchial cavity in crayfish at Wrocław and vicinity. [In Polish]. Przegląd Zoologiczny, 7(3), 288–290.
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/ msy096 PMID:29722887.
Lom, J., Nilsen, F., & Dyková, I. (2001). Thelohania contejeani Henneguy, 1892: Dimorphic life cycle and taxonomic affinities, as indicated by ultrastructural and molecular study. Parasitology Research, 87(10), 860–872. https://doi. org/10.1007/s004360100436 PMID:11688894.
Longshaw, M. (2011). Diseases of crayfish: A review. Journal of Invertebrate Pathology, 106(1), 54–70. https://doi. org/10.1016/j.jip.2010.09.013 PMID:21215355.
Longshaw, M., Stebbing, P. D., Bateman, K. S., & Hockley, F. A. (2012). Histopathological survey of pathogens and commensals of white-clawed crayfish (Austropotamobius pallipes) in England and Wales. Journal of Invertebrate Pathology, 110(1), 54–59. https://doi.org/10.1016/j. jip.2012.02.005 PMID:22366663.
Mažylis, A. (1978). On Astacus astacus L. infected with Thelohania contejeani Henneguy. Freshwater Crayfish, 4(1), 471–473.
McGriff, D., & Modin, J. (1983). Thelohania contejeani parasitism of the crayfish, Pacifastacus leniusculus, in California. California Fish and Game, 69(3), 178–183.
Moodie, E. G., Le Jambre, L. F., & Katz, M. E. (2003a). Thelohania montirivulorum sp. nov. (Microspora: Thelohaniidae), a parasite of the Australian freshwater crayfish, Cherax destructor (Decapoda: Parastacidae): fine ultrastructure, molecular characteristics and phylogenetic relationships. Parasitology Research, 91(3), 215–228. https://doi. org/10.1007/s00436-003-0948-9 PMID:12923630.
Moodie, E. G., Le Jambre, L. F., & Katz, M. E. (2003b). Thelohania parastaci sp. nov. (Microspora: Thelohaniidae), a parasite of the Australian freshwater crayfish, Cherax destructor (Decapoda: Parastacidae). Parasitology Research, 91(2), 151–165. https://doi.org/10.1007/s00436-003-0941-3 PMID:12923627.
Moodie, E. G., Le Jambre, L. F., & Katz, M. E. (2003c). Ultrastructural characteristics and small subunit ribosomal DNA sequence of Vairimorpha cheracis sp. nov., (Microspora: Burenellidae), a parasite of the Australian yabby, Cherax destructor (Decapoda: Parastacidae). Journal of Invertebrate Pathology, 84(3), 198–213. https://doi.org/10.1016/j.jip.2003.11.004 PMID:14726242.
Mori, M., & Salvidio, S. (2000). The occurrence of Thelohania contejeani Henneguy, a microsporidian parasite of the crayfish Austropotamobius pallipes (Lereboullet), in Liguria Region (NW Italy). Journal of Limnology, 59(2), 167–169. https://doi.org/10.4081/jlimnol.2000.167.
Pretto, T., Montesi, F., Ghia, D., Berton, V., Abbadi, M., Gastaldelli, M., Manfrin, A., & Fea, G. (2018). Ultrastructural and molecular characterization of Vairimorpha austropotamobii sp. nov. (Microsporidia: Burenellidae) and Thelohania contejeani (Microsporidia: Thelohaniidae), two parasites of the white-clawed crayfish, Austropotamobius pallipes complex (Decapoda: Astacidae). Journal of Invertebrate Pathology, 151, 59–75. https://doi.org/10.1016/j. jip.2017.11.002 PMID:29122615.
Quaglio, F., Capovilla, P., Fioravanti, M. L., Marino, F., Gaglio, G., Florio, D., Fioretto, B., & Gustinelli, A. (2011). Histological analysis of thelohaniasis in white-clawed crayfish Austropotamobius pallipes complex. Knowledge and Management of Aquatic Ecosystems, 401, 27. https://doi.org/10.1051/kmae/2011045.
Quilter, C. G. (1976). Microsporidan parasite Thelohania contejeani Henneguy from New Zealand freshwater crayfish. New Zealand Journal of Marine and Freshwater Research, 10(1), 225–231. https://doi.org/10.1080/002883 30.1976.9515609.
Skurdal, J., Qvenild, T., Taugbol, T., & Fjeld, E. (1990). A 6-year study of Thelohania contejeani parasitism of the noble crayfish, Astacus astacus L., in Lake Steinsfjorden, S. E. Norway. Journal of Fish Diseases, 13(5), 411–415. https:// doi.org/10.1111/j.1365-2761.1990.tb00800.x.
Skurdal, J., Taugbol, T., Fjeld, E., Hessen, D. O., & Hastein, T. (1988). Thelohania contejeani Henneguy parasitizing the noble crayfish, Astacus astacus L., in Norway. Journal of Fish Diseases, 11(5), 433–435. https://doi. org/10.1111/j.1365-2761.1988.tb00739.x.
Sumari, O., & Westman, K. (1969). The crayfish parasite Thelohania contejeani Henneguy (Sporozoa, Microsporidia) found in Finland. Annales Zoologici Fennici, 7, 193–194.
Stratton, C. E., Kabalan, B. A., Bolds, S. A., Reisinger, L. S., Behringer, D. C., & Bojko, J. (2023a). Cambaraspora faxoni n. sp. (Microsporidia: Glugeida) from native and invasive crayfish in the USA and a novel host of Cambaraspora floridanus. Journal of Invertebrate Pathology, 199, 107949. https://doi.org/10.1016/j.jip.2023.107949 PMID:37276936.
Stratton, C. E., Moler, P., Allain, T. W., Reisinger, L. S., Behringer, D. C., & Bojko, J. (2022a). The plot thickens: Ovipleistophora diplostomuri infects two additional species of Florida crayfish. Journal of Invertebrate Pathology, 191, 107766. https://doi.org/10.1016/j.jip.2022.107766 PMID:35472375.
Stratton, C. E., Reisinger, L. S., Behringer, D. C., Reinke, A. W., & Bojko, J. (2023b). Alternosema astaquatica n. sp. (Microsporidia: Enterocytozoonida), a systemic parasite of the crayfish Faxonius virilis. Journal of Invertebrate Pathology, 199, 107948. https://doi.org/10.1016/j. jip.2023.107948 PMID:37276935.
Stratton, C. E., Reisinger, L. S., Behringer, D. C., & Bojko, J. (2022b). Revising the Freshwater Thelohania to Astathelohania gen. Et comb. Nov., and description of two new species. Microorganisms, 10(3), 636. https://doi. org/10.3390/microorganisms10030636 PMID:35336214.
Vey, A., & Vago, C. (1973). Protozoal and fungal diseases of Austropotamobius pallipes, Lereboullet in France. Freshwater Crayfish, 1(1), 165–179.
Voronin, V. (1971). New data on microsporidiosis of the crayfish, Astacus astacus (L. 1758). Parazitologiia, 5(2), 186–191.
Weiss, L. M., Zhu, X., Cali, A., Tanowitz, H. B., & Wittner, M. (1994). Utility of microsporidian rRNA in diagnosis and phylogeny: A review. Folia Parasitologica, 41(2), 81–90. PMID:7927064.
