Haplosporidium raabei n. sp. (Haplosporidia): A parasite of zebra mussels, Dreissena polymorpha (Pallas, 1771)

Parasitology

Volumn 139, Issue 4, 2012, Pages 463-477

  Molloy, D P ^a,f   GiambErini L ^b   Stokes, N A ^c   Burreson, E M ^c   Ovcharenko, M A ^d,e  

^a NEW YORK STATE MUSEUM   (United States)

^b UNIVERSITÉ DE LORRAINE   (France)

^c VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

^d W STEFA SKI INSTITUTE OF PARASITOLOGY   (Poland)

^e Pomeranian Akademy   (Poland)

^f STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Dreissena polymorpha; Haplosporidia; Haplosporidium raabei n. sp.; phylogeny; small subunit ribosomal DNA

Indexed keywords

ANIMAL TISSUE; ARTICLE; DNA EXTRACTION; DREISSENA; DREISSENA POLYMORPHA; FRESHWATER ENVIRONMENT; GENE SEQUENCE; GEOGRAPHIC DISTRIBUTION; HAPLOSPIRIDIAN INFECTION; HAPLOSPORIDIUM RAABEI; HISTOLOGY; MUSSEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; PARASITE EXAMINATION; PARASITE IDENTIFICATION; PARASITE PREVALENCE; PARASITE VIRULENCE; PARASITOSIS; PATHOGENICITY; PHYLOGENY; PLASMODIUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPOROCYST; SPOROGENESIS; TAXONOMY; WATER SAMPLING;

ANIMALS; DNA, PROTOZOAN; DNA, RIBOSOMAL; DREISSENA; EUROPE; HAPLOSPORIDA; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SPORES, PROTOZOAN; UNITED STATES;

BIVALVIA; DREISSENA POLYMORPHA; HAPLOSPORIDIA; HAPLOSPORIDIUM; INVERTEBRATA;

EID: 84858844856     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011002101     Document Type: Article

References (43)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller,W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402.
2. Andrews, J. D. (1984). Epizootiology of diseases of oysters (Crassostrea virginica), and parasites of associated organisms in eastern North America. Helgolander Meeresuntersuchungen 37, 149-166.
3. Azevedo, C., Balseiro, P., Casal, G., Gestal, C., Aranguren, R., Stokes, N. A., Carnegie, R. B., Novoa, B., Burreson, E. M. and Figueras, A. (2006). Ultrastructural and molecular characterization of Haplosporidium montforti n. sp., parasite of the European abalone Haliotis tuberculata. Journal of Invertebrate Pathology 92, 23-32.
4. Azevedo, C., Conchas, R. F. and Montes, J. (2003). Description of Haplosporidium edule n. sp. (Phylum Haplosporidia), a parasite of Cerastoderma edule (Mollusca, Bivalvia) with complex spore ornamentation. European Journal of Protistology 39, 161-168.
5. Barrow, J. H., Jr. (1961). Observations of a haplosporidian, Haplosporidium pickfordi sp. nov. in fresh water snails. Transactions of the American Microscopical Society 80, 319-329.
6. Barrow, J. H., Jr. (1965). Observations on Minchinia pickfordae (Barrow 1961) found in snails of the Great Lakes region. Transactions of the American Microscopical Society 84, 587-593.
7. Bearham, D., Spiers, Z., Raidal, S., Jones, J. B., Burreson, E. M. and Nicholls, P. K. (2008a). Spore ornamentation of Haplosporidium hinei n. sp. (Haplosporidia) in pearl oysters Pinctada maxima (Jameson, 1901). Parasitology 135, 521-527.
8. Bearham, D., Spiers, Z., Raidal, S., Jones, J. B. and Nicholls, P. K. (2008b). Spore ornamentation of Minchinia occulta n. sp. (Haplosporidia) in rock oysters Saccostrea cuccullata (Born, 1778). Parasitology 11, 1271-1280.
9. Bowmer, C. T. and van der Meer, M. (1991). Reproduction and Histopathological Condition in First Year Zebra Mussels (Dreissena polymorpha) from the Haringvliet, Volkerakmeer and Hollands Diep Basins. TNO Institute of Environmental Sciences Report R91/132, Delft, The Netherlands.
10. Burreson, E. M. (2001). Spore ornamentation of Haplosporidium pickfordi Barrow, 1961 (Haplosporidia), a parasite of freshwater snails in Michigan, USA. Journal of Eukaryotic Microbiology 48, 622-626.
11. Burreson, E. M. (2005). Haplosporidia (haplosporidians). In Marine Parasitology (ed. Rohde, K.), pp. 23-25. CABI Publishing, Oxon, UK.
12. Burreson, E. M. and Ford, S. E. (2004). A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17, 499-517.
13. Burreson, E. M. and Reece, K. S. (2006). Spore ornamentation of Haplosporidium nelsoni and Haplosporidium costale (Haplosporidia), and incongruence of molecular phylogeny and spore ornamentation in the Haplosporidia. Journal of Parasitology 92, 1295-1301.
14. Camp, J.W., Blaney, L. M. and Barnes, D. K. (1999). Helminths of the round goby, Neogobius melanostomus (Perciformes: Gobiidae), from southern Lake Michigan, Indiana. Journal of Helminthological Society of Washington 66, 70-72.
15. Carlton, J. T. (2008). The zebra mussel Dreissena polymorpha found in North America in 1986 and 1987. Journal of Great Lakes Research 34, 770-773.
16. Carnegie, R. B., Burreson, E. M., Hine, P. M., Stokes, N. A., Audemard, C., Bishop, M. J. and Peterson, C. H. (2006). Bonamia perspora n. sp. (Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. Journal of Eukaryotic Microbiology 53, 232-245.
17. Caullery, M. and Mesnil, F. (1905). Recherches sur les Haplosporidies. Archives de Zoologie Experimentale et Generale, IV Série 4, 101-181 + plates XI-XIII.
18. Farley, C. A. (1967). A proposed life cycle of Minchinia nelsoni (Haplosporida, Haplosporidiidae) in the American oyster Crassostrea virginica. Journal of Protozoology 14, 616-625.
19. Ford, S. E., Stokes, N. A., Burreson, E. M., Scarpa, E., Carnegie, R. B., Kraeuter, J. N. and Bushek, D. (2009). Minchinia mercenariae n. sp. (Haplosporidia) in the hard clam Mercenaria mercenaria: Implications of a rare parasite in a commercially important host. Journal of Eukaryotic Microbiology 56, 542-551.
20. Ford, S. E. and Tripp, M. R. (1996). Diseases and defense mechanisms. In The Eastern Oyster Crassostrea virginica (ed. Kennedy, V. S., Newell, R. I. E. and Eble, A. F.), pp. 581-660. Maryland Sea Grant, College Park, Maryland, USA.
21. Granata, L. (1913). Ciclo di sviluppo di Haplosporidium limnodrili n. sp. Rendiconti della Reale Accademia dei Lincei 22, 734-737.
22. Granata, L. (1914). Ricerche sul ciclo evolutivo di Haplosporidium limnodrili Granata. Archiv für Protistenkunde 35, 47-79 + 3 plates.
23. Hine, P. M., Carnegie, R. B., Burreson, E. M. and Engelsma, M. Y. (2009). Inter-relationships of haplosporidians deduced from ultrastructural studies. Diseases of Aquatic Organisms 83, 247-256.
24. Jírovic, O. (1936). Haplosporidium cernosvitovi n. sp., eine neue Haplosporidienart aus Opistocysta (Pristina) flagellum Leidy. Archiv für Protistenkunde 86, 500-508+plate.
25. Karatayev, A. Y., Burlakova, L. E. and Padilla, D. K. (2002). Impacts of zebra mussels on aquatic communities and their role as ecosystem engineers. In Invasive Aquatic Species of Europe: Distribution, Impacts and Management (ed. Leppäkoski, E., Gollasch, S. and Olenin, S.), pp. 433-446. Kluwer Academic Publishers, Boston, Massachusetts, USA.
26. Kim, Y. and Powell, E. N. (2007). Distribution of parasites and pathologies in sentinel bivalves: NOAA status and trends "mussel watch" program. Journal of Shellfish Research 26, 1115-1151.
27. Kinzelbach, R. (1992). The main features of the phylogeny and dispersal of the zebra mussel Dreissena polymorpha. In The Zebra Mussel Dreissena polymorpha: Ecology, Biological Monitoring and First Applications in the Water Quality Management (ed. Neumann, D. and Jenner, H. A.), pp. 5-17. Gustav Fischer, New York, USA.
28. Mastitsky, S. E., Karatayev, A. Y., Burlakova, L. E. and Molloy, D. P. (2010). Parasites of exotic species in invaded areas: Does lower diversity mean lower epizootic impact? Diversity and Distributions 16, 798-803.
29. Medlin, L., Elwood, H. J., Stickel, S. and Sogin, M. L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNAcoding regions. Gene 71, 491-499.
30. Messick, G. A. (2009). Haplosporidian parasite in Diporeia spp. amphipods from the Great Lakes region, USA. Diseases of Aquatic Organisms 83, 153-157.
31. Messick, G. A., Overstreet, R. M., Nalepa, T. F. and Tyler, S. (2004). Prevalence of parasites in amphipods Diporeia spp. from Lakes Michigan and Huron, USA. Diseases of Aquatic Organisms 59, 159-170.
32. Molloy, D. P. (1998). The potential for using biological control technologies in the management of Dreissena spp. Journal of Shellfish Research 17, 177-183.
33. Molloy, D. P., Giamberini, L., Burlakova, L. E., Karatayev, A. Y., Cryan, J. R., Trajanovski, S. L. and Trajanovska, S. P. (2010). Investigation of the endosymbionts of Dreissena stankovici with morphological and molecular confirmation of host species. In The Zebra Mussel in Europe (ed. Van der Velde, G., Rajagopal, S. and bij de Vaate, A.), pp. 227-238. Backhuys Publishers, Leiden, The Netherlands.
34. Molloy, D. P., Karatayev, A. Y., Burlakova, L. E., Kurandina, D. P. and Laruelle, F. (1997). Natural enemies of zebra mussels: Predators, parasites, and ecological competitors. Reviews in Fisheries Science 5, 27-97.
35. O'Neill, C. R., Jr. (2008). The Silent Invasion: Finding Solutions to Minimize the Impacts of Invasive Quagga Mussels on Water Rates, Water Infrastructure and the Environment. Hearing of the U.S. House of Representatives Committee on Natural Resources-Subcommittee on Water and Power, Washington, D.C. at: URL: http://naturalresources. house.gov/uploadedfiles/ oneilltestimony06.24.08.pdf. Accessed March 11, 2011.
36. Perkins, F. O. (1990). Phylum Haplosporidia. In Handbook of Protoctista (ed. Margulis, L., Corliss, J. O., Melkonian, M. and Chapman, D. J.), pp. 19-29. Jones and Bartlett, Boston, Massachusetts, USA.
37. Reece, K. S., Siddall, M. E., Stokes, N. A. and Burreson, E. M. (2004). Molecular phylogeny of the Haplosporidia based on two independent gene sequences. Journal of Parasitology 90, 1111-1122.
38. Renault, T., Stokes, N. A., Chollet, B., Cochennec, N., Berthe, F., Gérard, A. and Burreson, E. M. (2000). Haplosporidiosis in the Pacific oyster Crassostrea gigas from the French Atlantic coast. Diseases of Aquatic Organisms 42, 207-214.
39. Sunila, I., Stokes, N. A., Smolowitz, R., Karney, R. C. and Burreson, E. (2002). Haplosporidium costale (seaside organism), a parasite of the eastern oyster, is present in Long Island Sound. Journal of Shellfish Research 21, 113-118.
40. Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 10. Sinauer Associates, Sunderland, Massachusetts, USA.
41. Toews, S., Beverley-Burton, M. and Lawrimore, T. (1993). Helminth and protist parasites of zebra mussels, Dreissena polymorpha (Pallas, 1771), in the Great Lakes region of southwestern Ontario, with comments on associated bacteria. Canadian Journal of Zoology 71, 1763-1766.
42. Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. and Kuris, A. M. (2003). Introduced species and their missing parasites. Nature (London) 421, 628-630.
43. White, D. (2008). A Molecular Phylogeny of the Genus Bonamia Based on Sequence Data of the Ribosomal RNA (rRNA) Gene Complex. Master's thesis. College of William and Mary, Williamsburg, Virginia, USA.