Skip to main content
×
Home
    • Aa
    • Aa

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

  • D. P. MOLLOY (a1), L. GIAMBÉRINI (a2), N. A. STOKES (a3), E. M. BURRESON (a3) and M. A. OVCHARENKO (a4) (a5)...
Summary
SUMMARY

Extensive connective tissue lysis is a common outcome of haplosporidian infection. Although such infections in marine invertebrates are well documented, they are relatively rarely observed in freshwater invertebrates. Herein, we report a field study using a comprehensive series of methodologies (histology, dissection, electron microscopy, gene sequence analysis, and molecular phylogenetics) to investigate the morphology, taxonomy, systematics, geographical distribution, pathogenicity, and seasonal and annual prevalence of a haplosporidian observed in zebra mussels, Dreissena polymorpha. Based on its genetic sequence, morphology, and host, we describe Haplosporidium raabei n. sp. from D. polymorpha – the first haplosporidian species from a freshwater bivalve. Haplosporidium raabei is rare as we observed it in histological sections in only 0·7% of the zebra mussels collected from 43 water bodies across 11 European countries and in none that were collected from 10 water bodies in the United States. In contrast to its low prevalences, disease intensities were quite high with 79·5% of infections advanced to sporogenesis.

Copyright
Corresponding author
*Corresponding author: Present address: Department of Biological Sciences, State University of New York, 1400 Washington Avenue, Albany, NY 12222, USA. Tel: +1 518 677 8245. Fax: +1 518 677 5236. E-mail: dmolloy@albany.edu
References
Hide All
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, 33893402.
Andrews J. D. (1984). Epizootiology of diseases of oysters (Crassostrea virginica), and parasites of associated organisms in eastern North America. Helgolander Meeresuntersuchungen 37, 149166.
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, 2332.
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, 161168.
Barrow J. H. Jr. (1961). Observations of a haplosporidian, Haplosporidium pickfordi sp. nov. in fresh water snails. Transactions of the American Microscopical Society 80, 319329.
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, 587593.
Bearham D., Spiers Z., Raidal S., Jones J. B., Burreson E. M. and Nicholls P. K. (2008 a). Spore ornamentation of Haplosporidium hinei n. sp. (Haplosporidia) in pearl oysters Pinctada maxima (Jameson, 1901). Parasitology 135, 521527.
Bearham D., Spiers Z., Raidal S., Jones J. B. and Nicholls P. K. (2008 b). Spore ornamentation of Minchinia occulta n. sp. (Haplosporidia) in rock oysters Saccostrea cuccullata (Born, 1778). Parasitology 11, 12711280.
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.
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, 622626.
Burreson E. M. (2005). Haplosporidia (haplosporidians). In Marine Parasitology (ed. Rohde K.), pp. 2325. CABI Publishing, Oxon, UK.
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, 499517.
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, 12951301.
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, 7072.
Carlton J. T. (2008). The zebra mussel Dreissena polymorpha found in North America in 1986 and 1987. Journal of Great Lakes Research 34, 770773.
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, 232245.
Caullery M. and Mesnil F. (1905). Recherches sur les Haplosporidies. Archives de Zoologie Experimentale et Generale, IV Série 4, 101181 + plates XI–XIII.
Farley C. A. (1967). A proposed life cycle of Minchinia nelsoni (Haplosporida, Haplosporidiidae) in the American oyster Crassostrea virginica. Journal of Protozoology 14, 616625.
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, 542551.
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.
Granata L. (1913). Ciclo di sviluppo di Haplosporidium limnodrili n. sp. Rendiconti della Reale Accademia dei Lincei 22, 734737.
Granata L. (1914). Ricerche sul ciclo evolutivo di Haplosporidium limnodrili Granata. Archiv für Protistenkunde 35, 4779 + 3 plates.
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, 247256.
Jírovic O. (1936). Haplosporidium cernosvitovi n. sp., eine neue Haplosporidienart aus Opistocysta (Pristina) flagellum Leidy. Archiv für Protistenkunde 86, 500508+plate.
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. 433446. Kluwer Academic Publishers, Boston, Massachusetts, USA.
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, 11151151.
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. 517. Gustav Fischer, New York, USA.
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, 798803.
Medlin L., Elwood H. J., Stickel S. and Sogin M. L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491499.
Messick G. A. (2009). Haplosporidian parasite in Diporeia spp. amphipods from the Great Lakes region, USA. Diseases of Aquatic Organisms 83, 153157.
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, 159170.
Molloy D. P. (1998). The potential for using biological control technologies in the management of Dreissena spp. Journal of Shellfish Research 17, 177183.
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. 227238. Backhuys Publishers, Leiden, The Netherlands.
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, 2797.
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.
Perkins F. O. (1990). Phylum Haplosporidia. In Handbook of Protoctista (ed. Margulis L., Corliss J. O., Melkonian M. and Chapman D. J.), pp. 1929. Jones and Bartlett, Boston, Massachusetts, USA.
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, 11111122.
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, 207214.
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, 113118.
Swofford D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 10. Sinauer Associates, Sunderland, Massachusetts, USA.
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, 17631766.
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, 628630.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Type Description Title
PDF
Supplementary Data

Molloy Supplementary Data
Sample collection data for histological examination of zebra mussels for H. raabei

 PDF (46 KB)
46 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 3
Total number of PDF views: 3 *
Loading metrics...

Abstract views

Total abstract views: 167 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd October 2017. This data will be updated every 24 hours.