Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T05:31:06.812Z Has data issue: false hasContentIssue false
  • English
  • Français

A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease)

Published online by Cambridge University Press:  15 December 2004

Eugene M. Burreson  and
Susan E. Ford
Eugene M. Burreson
Affiliation:
Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, Virginia 23062, USA
Susan E. Ford
Affiliation:
Haskin Shellfish Research Laboratory, Rutgers University, Port Norris, New Jersey 08349, USA
Get access

Abstract

The current status of the Haplosporidia is reviewed as well as recent information on Haplosporidium nelsoni, the causative agent of MSX disease in oysters. Recent molecular phylogenetic analyses with greatly increased taxon sampling support monophyly of the Haplosporidia and hypothesize placement of the group as sister taxon to the phylum Cercozoa. Oyster pathogens in the genus Bonamia should be considered haplosporidians based on molecular sequence data. Thus, the group contains 4 genera: Uropsoridium, Haplosporidium, Bonamia and Minchinia. Molecular phylogenetic analyses support monophyly of Urosporidium, Bonamia and Minchinia, but Haplosporidium forms a paraphyletic clade. Reports of haplosporidia worldwide are reviewed. Molecular detection assays have greatly increased our ability to rapidly and specifically diagnose important pathogens in the phylum and have also improved our understanding of the distribution and biology of H. nelsoni and H. costale. Much of the data available for H. nelsoni has been integrated into a mathematical model of host/parasite/environment interactions. Model simulations support hypotheses that recent H. nelsoni outbreaks in the NE United States are related to increased winter temperatures, and that a host other than oysters is involved in the life cycle. Evidence is presented that natural resistance to H. nelsoni has developed in oysters in Delaware Bay, USA. However, in Chesapeake Bay, USA H. nelsoni has intensified in historically low salinity areas where salinities have increased because of recent drought conditions. Efforts to mitigate the impact of H. nelsoni involve selective breeding programs for disease resistance and the evaluation of disease resistant non-native oysters.

Keywords

PhylogenyDiagnosticsNumerical modelHaplosporidiaHaplosporidium nelsoni
Type
Research Article
Information
Aquatic Living Resources , Volume 17 , Issue 4: Bivalve Diseases , October 2004 , pp. 499 - 517
Copyright
© EDP Sciences, IFREMER, IRD, 2004

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.)

References

Anderson, T.J., Newman, L.J., Lester, R.J.G., 1993, Light and electron microscope study of Urosporidium cannoni n. sp., a haplosporidian parasite of the polyclad turbellarian Stylochus sp. J. Euk. Microbiol. 40, 162-168. CrossRef
Andrews, J.D., 1964, Oyster mortality studies in Virginia. IV. MSX in James River public seed beds. Proc. Nat. Shellfish Assoc. 53, 65-84.
Andrews, J.D., 1967, Interaction of two diseases of oysters in natural waters. Proc. Nat. Shellfish Assoc. 57, 38-48.
Andrews, J.D., 1968, Oyster mortality studies in Virginia. VII. Review of epizootiology and origin of Minchinia nelsoni. Proc. Nat. Shellfish Assoc. 58, 23-36.
Andrews, J.D., 1983, Minchinia nelsoni (MSX) infections in the James River seed-oyster area and their expulsion in spring. Estuar. Coast. Shelf Sci. 16, 255-269. CrossRef
Andrews, J.D., 1984, Epizootiology of diseases of oysters (Crassostrea virginica), and parasites of associated organisms in eastern North America. Helgol. Meer. 37, 149-166. CrossRef
Andrews, J.D., Castagna, M., 1978, Epizootiology of Minchinia costalis in susceptible oysters in seaside bays of Virginia's eastern shore, 1959-1976. J. Invertebr. Pathol. 32, 124-138. CrossRef
Andrews, J.D., Wood, J.L., 1967, Oyster mortality studies in Virginia. VI. History and distribution of Minchinia nelsoni, a pathogen of oysters, in Virginia. Ches. Sci. 8, 1-13. CrossRef
Armstrong, D.A., Armstrong, J.L., 1974, A haplosporidan infection in gaper clams, Tresus capax (Gould), from Yaquina Bay, Oregon. Proc. Natl Shellfish Assoc. 64, 68-72.
Arvy, , 1949, Présentation de documents relatifs à l'ovogenèse chez le Dentale et à deux parasites de ce Scaphopode: Cercaria prenanti n. sp. et Haplosporidium dentali. Bull. Soc. Zool. France 74, 292-294.
Azevedo, C., 1984, Ultrastructure of the spore of Haplosporidium lusitanicum sp. n. (Haplosporida, Haplosporidiidae), parasite of a marine mollusc. J. Parasitol. 70, 358-371. CrossRef
Azevedo, C., 2001, Ultrastructural description of the spore maturation stages of the clam parasite Minchinia tapetis (Vilela 1951) (Haplosporida: Haplosporidiidae). Syst. Parasitol. 49, 189-194. CrossRef
Azevedo, C., Conchas, R.F., Montes, C., 2003, Description of Haplosporidium edule n. sp. (Phylum Haplosporidia), a parasite of Cerastoderma edule (Mollulsca, Bivalvia) with complex spore ornamentation. Eur. J. Protistol. 39, 161-167. CrossRef
Azevedo, C., Montes, J., Corral, L., 1999, A revised description of Haplosporidium armoricanum, parasite of Ostrea edulis L. from Galicia, northwestern Spain, with special reference to the spore-wall filaments. Parasitol. Res. 85, 977-983. CrossRef
Bachere, E., Chagot, D., Tigé, G., Grizel, H., 1987, Study of a haplosporidian (Ascetospora), parasitizing the Australian flat oyster Ostrea angasi. Aquaculture 67, 266-268. CrossRef
Ball, S.J., 1980, Fine structure of the spores of Minchinia chitonis (Lankester 1885) Labbé, 1896 (Sporozoa: Haplosporida), a parasite of the chiton, Lepidochitona cinereus. Parasitology 81, 169-176. CrossRef
Barber, B.J., Langan, R., Howell, T.L., 1997, Haplosporidium nelsoni (MSX) epizootic in the Piscataqua river estuary (Maine New Hampshire, USA). J. Parasitol. 83, 148-150. CrossRef
Barber, R.D., Kanaley, S.A., Ford, S.E., 1991, Evidence for regular sporulation by Haplosporidium nelsoni (MSX) (Ascetospora: Haplosporidiidae) in spat of the American oyster, Crassostrea virginica. J. Protozool. 38, 305-306. CrossRef
Barrow, J.H Jr., 1961, Observations of a haplosporidian, Haplosporidium pickfordi sp. nov. in fresh water snails. Trans. Am. Microsc. Soc. 80, 319-329. CrossRef
Berthe, F.C.J., Le Roux, F., Peyretaillade, E., Peyret, P., Rodriguez, D., Gouy, M., Vivarés, C.P., 2000, Phylogenetic analysis of the small subunit ribosomal RNA of Marteilia refringens validates the existence of phylum Paramyxea (Desportes and Perkins, 1990). J. Euk. Microbiol. 47, 288-293. CrossRef
Bobo, M.Y., Richardson, D., Cheng, T.C., McGovern, E., Coen, L., 1996, Seasonal cycle of Haplosporidium nelsoni (MSX) in intertidal oysters, Crassostrea virginica, in South Carolina. J. Shellfish Res. 15, 525.
Burreson E.M., 1988, Use of immunoassays in haplosporidan life cycle studies. In: Fisher W.S. (Eds.). Disease Processes in Marine Bivalve Molluscs. Am. Fish. Soc., Bethesda, Maryland, pp. 298-303.
Burreson, E.M., 1991, Effects of Perkinsus marinus infection in the eastern oyster I: Susceptibility of native and MSX-resistant stocks. J. Shellfish Res. 10, 417-424.
Burreson, E.M., 1994, Further evidence of regular sporulation by Haplosporidium nelsoni in small oysters, Crassostrea virginica. J. Parasitol. 80, 1036-1038. CrossRef
Burreson, E.M., 2001, Spore ornamentation of Haplosporidium pickfordi Barrow, 1961 (Haplosporidia), a parasite of freshwater snails in Michigan, USA. J. Euk. Microbiol. 48, 622-626. CrossRef
Burreson E.M., Andrews J.D., 1988, Unusual intensification of Chesapeake Bay oyster diseases during recent drought conditions. Oceans '88 Proceedings, pp. 799-802.
Burreson, E.M., Ragone Calvo, L.M., 1996, Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. J. Shellfish Res. 15, 17-34.
Burreson, E.M., Robinson, M.E., Villalba, A., 1988, A comparison of paraffin histology and hemolymph analysis for the diagnosis of Haplosporidium nelsoni (MSX) in Crassostrea virginica (Gmelin). J. Shellfish Res. 7, 19-24.
Burreson, E.M., Stokes, N.A., Friedman, C.S., 2000, Increased virulence in an introduced pathogen: Haplosporidium nelsoni (MSX) in the eastern oyster Crassostrea virginica. J. Aquat. Anim. Health 12, 1-8. 2.0.CO;2>CrossRef
Bushek, D., Ford, S.E., Allen, J.S.K., 1994, Evaluation of methods using Ray's fluid thioglycollate medium for diagnosis of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica. Ann. Rev. Fish Dis. 4, 201-217. CrossRef
Calvo, G.W., Luckenbach, M.W., Allen, S.K., Burreson, E.M., 1999, Comparative field study of Crassostrea gigas (Thunberg, 1793) and Crassostrea virginica (Gmelin, 1791) in relation to salinity in Virginia. J. Shellfish Res. 18, 465-473.
Calvo, G.W., Luckenbach, M.W., Allen, S.K., Burreson, E.M., 2001, A comparative field study of Crassostrea ariakensis (Fujita 1913) and Crassostrea virginica (Gmelin 1791) in relation to salinity in Virginia. J. Shellfish Res. 20, 221-229.
Carballal, M.J., Iglesias, D., Santamarina, J., Ferro-Soto, B., Villalba, A., 2001, Parasites and pathologic conditions of the cockle Cerastoderma edule populations of the coast of Galicia (NW Spain). J. Invertebr. Pathol. 78, 87-97. CrossRef
Carnegie, R.G., Barber, B.J., Culloty, S.C., Figueras, A.J., Distel, D.L., 2000, Development of a PCR assay for detection of the oyster pathogen Bonamia ostreae and support for its inclusion in the Haplosporidia. Dis. Aquat. Org. 42, 199-206. CrossRef
Carnegie, R.G., Meyer, G.R., Blackbourn, J., Cochennec-Laureau, N., Berthe, F.C.J., Bower, S.M., 2003, Detection of the oyster parasite Mikrocytos mackini by PCR and fluorescent in situ hybridization, and a preliminary phylogenetic analysis. Dis. Aquat. Org. 54, 219-227. CrossRef
Caullery, M., Chappellier, A., 1906, Anurosporidium pelseneeri n.g., n. sp., Haplosporidie infectant les sporocysts d'un trematode parasite de Donax trunculus L. C. R. Soc. Biol. 60, 325-328.
Caullery, M., Mesnil, F., 1899, Sur le genre Aplosporidium (nov) et l'ordre nouveau des Aplosporidies. C. R. Soc. Biol. (Paris) 51, 789-791.
Caullery, M., Mesnil, F., 1905, Sur quelques nouvelles haplosporidies d'Annélide. C. R. Soc. Biol. (Paris) 58, 580-583.
Cavalier-Smith, T., 1993, Kingdom Protozoa and its 18 phyla. Microbiol. Rev. 57, 953-994.
Cavalier-Smith, T., Chao, E.E.-Y., 2003a, Phylogeny of Coanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. J. Mol. Evol. 56, 540-563. CrossRef
Cavalier-Smith, T., Chao, E.E.-Y., 2003b, Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154, 341-358. CrossRef
Chintala, M.M., Ford, S.E., Fisher, W.S., Ashton-Alcox, K.A., 1994, Oyster serum agglutinins and resistance to protozoan parasites. J. Shellfish Res. 13, 115-121.
Choi, K.-S., Wilson, E.A., Lewis, D.H., Powell, E.N., Ray, S.M., 1989, The energetic cost of Perkinsus marinus parasitism in oysters. Quantification of the thioglycollate method. J. Shellfish Res. 8, 117-125.
Chu, F.-L.E., Burreson, E.M., Zhang, F.S., Chew, K.K., 1996, An unidentified haplosporidian parasite of bay scallop Argopecten irradians cultured in the Shandong and Liaoning provinces of China. Dis. Aquat. Org. 42, 207-214.
Ciancio, A., Scippa, S., Izzo, C., 1999, Ultrastructure of vegetative and sporulation stages of Haplosporidium ascidiarum from the ascidian Ciona intestinalis L. Eur. J. Protistol. 35, 175-182. CrossRef
Cochennec-Laureau, N., Reece, K.S., Berthe, F.C.J., Hine, P.M., 2003, Mikrocytos roughleyi taxonomic affiliation leads to the genus Bonamia (Haplosporidia). Dis. Aquat. Org. 54, 209-217. CrossRef
Comps, M., Pichot, Y., 1991, Fine spore structure of a haplosporidan parasitizing Crassostrea gigas: taxonomic implications. Dis. Aquat. Org. 11, 73-77. CrossRef
Comps, M., Tigé, G., 1997, Fine structure of Minchinia sp., a haplosporidan infecting the mussel Mytilus galloprovincialis L. Syst. Parasitol. 38, 45-50. CrossRef
Cook, T., Folli, M., Klinck, J., Ford, S., Miller, J., 1998, The relationship between increasing sea surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar. Coast. Shelf Sci. 40, 587-597. CrossRef
Couch, J.A., Rosenfield, A., 1968, Epizootiology of Minchinia costalis and Minchina nelsoni in oysters introducted into Chincotaeague Bay. Proc. Natl. Shellfish Assoc. 58, 51-59.
Day, J.M., Franklin, M.E., Brown, B.L., 2000, Use of competitive PCR to detect and quantify Haplosporidium nelsoni infection (MSX disease) in the eastern oyster (Crassostrea virginica). Mar. Biotechnol. 1, 147-154.
Debaisieux, P., 1920, Haplosporidium (Minchinia) chitonis Lank., Haplosporidium nemertis, Nov. sp. La Cellule 30, 293-309.
DeBrosse, G.A., Allen, S.K., 1966, Cooperative regional oyster selective breeding (CROSBREED) project. J. Shellfish Res. 15, 514-515.
Desportes, I., Nashed, N.N., 1983, Ultrastructure of sporulation in Minchinia dentali (Arvy), an haplosporean parasite of Dentalium entale (Scaphopoda, Mollusca); taxonomic implications. Protistologica 19, 435-460.
Desportes I., Perkins F.O., 1990, Phylum Paramyxea. In: Margulis L., Corliss J.O., Melkonian M., Chapman D.J. (Eds.), Handbook of Protoctista, Jones and Bartlett Publishing, Boston, MA, pp. 30-35.
DeTurk, W.E., 1940, The occurrence and development of a hyperasite, Urosporidium crescens sp. nov. (Sporozoa, Haplosporidia), which infecsts the metacercariae of Spelotrema nicolli, parasitic in Callinectes sapidus. J. Elisha Mitchell Sci. Soc. 56, 231-232.
Diggles, B.K., Nichol, J., Hine, P.M., Wakefield, S., Cochennec-Laureau, N., Roberts, R.D., Friedman, C.S., 2002, Pathology of cultured paua Haliotis iris infected with a novel haplosporidian parasite, with some observations on the course of disease. Dis. Aquat. Org. 50, 219-231. CrossRef
Dollfus, R.Ph., 1925, Liste critique des cercaires marines à queue sétigère signalées jusqu'à présent. Trav. Station Zool. Wimereux 9, 3-65.
Duboscq, O., Harant, H., 1923, Sur les Sporozoaires des Tuniciers. C. R. Acad. Sci. Paris 177, 432-433.
Elston, R.A., Farley, C.A., Kent, M.L., 1986, Occurrence and significance of bonamiasis in European flat oysters Ostrea edulis in North America. Dis. Aquat. Org. 2, 49-54. CrossRef
Farley, C.A., 1975, Epizootic and enzootic aspects of Minchinia nelsoni (Haplosporida) disease in Maryland oysters. J. Protozool. 22, 418-427. CrossRef
Farley, C.A., Wolf, P.H., Elston, R.A., 1988, A long-term study of “microcell” disease in oysters with a description of a new genus, Mikrocytos (g. n.), and two new species, Mikrocytos mackini (sp. n.) and Mikrocytos roughleyi (sp. n.). Fish. Bull. 86, 581-593.
Figureras, A.J., Jardon, C.F., Caldas, J.R., 1991, Diseases and parsites of mussels (Mytilus edulis Linneaus, 1758) from two sites on the east coast of the United States. J. Shellfish Res. 10, 89-94.
Flores, B.S., Siddall, M.E., Burreson, E.M., 1996, Phylogeny of the Haplosporidia (Eukaryota: Alveolata) based on small subunit ribosomal RNA gene sequence. J. Parasitol. 82, 616-623. CrossRef
Fong, D., Chan, M.M.-Y., Rodriguez, R., Chen, C.-C., Liang, Y., Littlewood, D.T.J., Ford, S.E., 1993, Small subunit ribosomal RNA gene sequence of the parasitic protozoan Haplosporidium nelsoni provides a molecular probe for the oyster MSX disease. Mol. Biochem. Parasitol. 62, 139-143. CrossRef
Ford, S.E., 1996, Range extension by the oyster parasite Perkinsus marinus into the northeastern US: Response to climate change? J. Shellfish Res. 15, 45-56.
Ford, S.E., 2002, Development of high disease resistance in a wild oyster population. J. Shellfish Res. 21, 387.
Ford, S.E., Haskin, H.H., 1982, History and epizootiology of Haplosporidium nelsoni (MSX), an oyster pathogen, in Delaware Bay, 1957-1980. J. Invertebr. Pathol. 40, 118-141. CrossRef
Ford, S.E., Haskin, H.H., 1988, Comparison of in vitro salinity tolerance of the oyster parasite Haplosporidium nelsoni (MSX) and hemocytes from the host, Crassostrea virginica. Comp. Biochem. Physiol. 90A, 183-187. CrossRef
Ford, S.E., Kanaley, S.A., 1988, An evaluation of hemolymph diagnosis for detection of the oyster parasite Haplosporidium nelsoni (MSX). J. Shellfish Res. 7, 11-18.
Ford, S., Powell, E., Klinck, J., Hofmann, E., 1999a, Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. I. Model development, implementation, and verification. J. Shellfish Res. 18, 475-500.
Ford, S.E., Schotthoefer, A., Spruck, C., 1999b, In vivo dynamics of the microparasite Perkinsus marinus during progression and regression of infections in eastern oysters. J. Parasitol. 85, 273-282. CrossRef
Ford S.E., Tripp M.R., 1996, Diseases and defense mechanisms. In: Kennedy V.S., Newell R.I.E., Eble A.F. (Eds.), The eastern oyster Crassostrea virginica, Maryland Sea Grant, College Park, MD, pp. 581-660.
Granata, L., 1913, Ciclo de sviluppo di Haplosporidium limnodrili n. sp. Rend. R. Accad. Lincei 22, 734.
Guo, X., Ford, S., DeBrosse, G., 2003, Breeding and evaluation of eastern oyster strains selected for MSX, Dermo and JOD resistance. J. Shellfish Res. 22, 333.
Harvell, C.D.K.K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W., Vasta, G.R., 1999, Emerging marine disease - climate links and anthropogenic factors. Science 285, 1505-1510. CrossRef
Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S., Samuel, M.D., 2002, Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158-2162. CrossRef
Haskin, H.H., Andrews, J.D., 1988, Uncertainties and speculations about the life cycle of the eastern oyster pathogen Haplosporidium nelsoni (MSX). In: Fisher W.S. (Ed.), Disease Processes in Marine Bivalve Molluscs. Am. Fish. Soc. Spec. Publ. 18, 5-22.
Hervio, D., Bachère, E., Boulo, V., Cochennec, N., Vuillemin, V., Le Coguic, Y., Cailletaux, G., Mazurié, J., Mialhe, E., 1995, Establishment of an experimental infection protocol for the flat oyster, Ostrea edulis, with the intrahaemocytic protozoan parasite, Bonamia ostreae: application in the selection of parasite-resistant oysters. Aquaculture 132, 183-194. CrossRef
Haskin, H.H., Ford, S.E., 1979, Development of resistance to Minchinia nelsoni (MSX) mortality in laboratory-reared and native oyster stocks in Delaware Bay. Mar. Fish. Rev. 41, 54-63.
Haskin, H.H., Ford, S.E., 1982, Haplosporidium nelsoni (MSX) on Delaware Bay seed oyster beds: a host-parasite relationship along a salinity gradient. J. Invertebr. Pathol. 40, 388-405. CrossRef
Haskin H.H., Ford S.E., 1986, Report to the Bureau of Shellfisheries, NJ Department of Environmental Protection on the Delaware Bay Oyster Research Program 1984-1986. Rutgers University, Port Norris, New Jersey.
Haskin, H.H., Stauber, L.A., Mackin, J.A., 1966, Minchinia nelsoni n. sp. (Haplosporida, Haplosporidiidae): causative agent of the Delaware Bay oyster epizootic. Science 153, 1414-1416. CrossRef
Hillman, R.E., Boehm, P.D., Freitas, S.Y., 1988, A pathology potpourri from the NOAA mussel watch program. J. Shellfish Res. 7, 216.
Hillman, R.E., Ford, S.E., Haskin, H.H., 1990, Minchinia teredinis n. sp. (Balanosporida, Haplosporidiidae), a parasite of teredinid shipworms. J. Protozool. 37, 364-368. CrossRef
Hine, P.M., Thorne, T., 1998, Haplosporidium sp. (Haplosporidia) in hatchery-reared pearl oysters, Pinctada maxima (Jameson, 1901), in north western Australia. J. Invertebr. Pathol. 71, 48-52. CrossRef
Hine, P.M., Thorne, T., 2002, Haplosporidium sp. (Alveolata: Haplosporidia) associated with mortalities among rock oysters Saccostrea cuccullata in north Western Australia. Dis. Aquat. Org. 51, 123-133. CrossRef
Hine, P.M., Bower, S.M., Meyer, G.R., Cochennec-Laureau, N., Berthe, F.C.J., 2001a, Ultrastructure of Mikrocytos mackini, the cause of Denman Island disease in oysters Crassostrea spp. and Ostrea spp. in British Columbia, Canada. Dis. Aquat. Org. 45, 215-227. CrossRef
Hine, P.M., Cochennec-Laureau, N., Berthe, F.C.J., 2001b, Bonamia exitiosus n. sp. (Haplosporidia) infecting flat oysters Ostrea chilensis in New Zealand. Dis. Aquat. Org. 47, 63-72. CrossRef
Hine, P.M., Wakefield, S., Diggles, B.K., Webb, V.L., Maas, E.W., 2002, The ultrastructure of a haplosporidian containing Rickettsiae, associated with mortalities among cultured paua Haliotis iris. Dis. Aquat. Org. 49, 207-219. CrossRef
Hofmann, E., Ford, S., Powell, E., Klinck, J., 2001, Modeling studies of the effect of climate variability on MSX disease in eastern oyster (Crassostrea virginica) populations. Hydrobiologia 460, 195-212. CrossRef
Hofmann, E.E., Powell, E.N., Klinck, J.M., Saunders, G., 1995, Modelling diseased oyster populations I. Modelling Perkinsus marinus infections in oysters. J. Shellfish Res. 14, 121-151.
Howell, M., 1967, The trematode Bucephalus longicornutus (Manter, 1954) in the New Zealand Mud-oyster, Ostrea lutdaria. Trans. R. Soc. New Zealand 8, 221-237.
IPCC, 2001, Summary for Policy Makers. Report of Working Group I. Intergovernmental Panel on Climate Change. http://www.ipcc.ch/pub/pub.htm.
Jírovec, O., 1936, Haplosporidium cernosvitovi n. sp. eine neue Haplosporidienart aus Opistocysta (Pristina) flagellum Leidy. Arch. Protistenk. 86, 500-508.
Kamaishi, T., Yoshinaga, T., 2002, Detection of Haplosporidium nelsoni in Pacific oyster Crassostrea gigas in Japan. Fish Pathol. 37, 193-195. CrossRef
Kang, P.A., 1980, On the Minchinia sp. infection in the oysters from Chungmu area. Bull. Fish. Resour. Develop. Agency (Republic of Korea) 25, 25-28.
Karl, T.R., Knight, R.W., Easterling, D.R., Quayle, R.G., 1996, Indices of climate change for the United States. Bull. Am. Meteorol. Soc. 77, 279-291. 2.0.CO;2>CrossRef
Katkansky, S.C., Warner, R.W., 1970, Sporulation of a haplosporidian in a Pacific oyster (Crassostrea gigas) in Humboldt Bay, California. J. Fish. Res. Board Can. 27, 1320-1321. CrossRef
Kern, F.G., 1976, Sporulation of Minchinia sp. (Haplosporida, Haplosporidiidae) in the Pacific oyster Crassostrea gigas (Thunberg) from the republic of Korea. J. Protozool. 23, 498-500. CrossRef
Kern, F.G., 1988, Recent changes in the range of “MSX” Haplosporidium nelsoni. J. Shellfish Res. 7, 543.
Ko, Y.-T., Ford, S.E., Fong, D., 1995, Characterization of the small subunit RNA gene of the oyster parasite Haplosporidium costale. Mol. Mar. Biol. Biotechnol. 4, 236-240.
Krantz, E.L., Buchanan, L.R., Farley, C.A., Carr, A.H., 1972, Minchinia nelsoni in oysters from Massachusetts waters. Proc. Nat. Shellfish Assoc. 62, 83-88.
La Haye, C.A., Holland, N.D., McLean, N., 1984, Electron microscopic study of Haplosporidium comatulae n. sp. (Phylum Ascetospora: Class Stellatosporea), a haplosporidian endoparasite of an Australian crinoid, Oligometra serripinna (Phylum Echinodermata). Protistologica 20, 507-515.
Lankester E.R., 1885, Protozoa. In: Encyclopaedia Britannica, 9th edn. 19, 830-866.
Larsson, R., 1987, On Haplosporidium gammari, a parasite of the amphipod Rivulogamarus pulex, and it relationships with the phylum Ascetospora. J. Invertebr. Pathol. 49, 159-169. CrossRef
Lewis, E.J., Kern, F.G., Rosenfield, A., Stevens, S.A., Walker, R.L., Heffernan, P.B., 1992, Lethal parasites in oysters from coastal Georgia, with discussion of disease and management implications. Mar. Fish. Rev. 52, 1-6.
Marchand, J., Sprague, V., 1979, Ultrastructure de Minchinia cadomensis sp. n. (Haplosporida) parasite du Décapode Rhithropanopeus harrisii tridentatus Matiland dans le Canal de Caen à la Mer (Calvados, France). J. Protozool. 26, 179-185. CrossRef
Matthiessen, G.C., Feng, S.Y., Leibovitz, L., 1990, Patterns of MSX (Haplosporidium nelsoni) infection and subsequent mortality in resistant and susceptible strains of the eastern oyster Crassostrea virginica (Gmelin, 1791) in New England. J. Shellfish Res. 9, 359-366.
McGovern, E.R., Burreson, E.M., 1990, Ultrastructure of Minchinia sp. spores from shipworms (Teredo spp.) in the western North Atlantic, with a discussion of taxonomy of the Haplosporidiidae. J. Protozool. 37, 212-218. CrossRef
Mercier, L., Poisson, R., 1922, Une haplosporidie, Haplosporidium caulleryi nov. sp., parasite de Nereilepas fucata Sav. C.R. Acad. Sci. Paris 174, 1205-1207.
Messick, G.A., Nalepa, T.F., 2002, Parasites in Diporeia spp. amphipods from Lakes Michigan and Huron. J. Shellfish Res. 21, 391.
Mix, M.C., Sprague, V., 1974, Occurrence of a haplosporidian in native oysters (Ostrea lurida) from Yaquina Bay and Alsea Bay, Oregon. J. Invertebr. Pathol. 23, 2552-254. CrossRef
Morris, D.J., Adams, A., Richards, R.H., 2000, Observations on the electron-dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Dis. Aquat. Org. 39, 201-209. CrossRef
Newman, M.W., Johnson, C.A III, Pauley, G.B., 1976, A Minchinia-like haplosporidan parasitizing blue crabs, Callinectes sapidus. J. Invertebr. Pathol. 27, 311-315. CrossRef
Ormières, R., 1980, Haplosporidium parisi n. sp. Haplosporidie parasite de Serpula vermicularis L. étude ultrastructurale de la spore. Protistologica 16, 467-474.
Ormières, R., de Puytorac, P., 1968, Ultrastructure des spores de l'haplosporidie Haplosporidium ascidiarum endoparasite du tunicier Sydniuim elegans Giard. C. R. Acad. Sci. Paris 266, 1134-1136.
Ormières, R., Sprague, V., Bartoli, P., 1973, Light and electron microscope study of a new species of Urosporidium (Haplosporida), hyperparasite of trematode sporocysts in the clam Abra ovata. J. Invertebr. Pathol. 21, 71-86. CrossRef
Paraso, M.C., Ford, S.E., Powell, E.N., Hofmann, E.E., Klinck, J.M., 1999, Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. II. Salinity effects. J. Shellfish Res. 18, 501-516.
Penna, M.S., Khan, M., French, R.A., 2001, Development of a multiplex PCR for the detection of Haplosporidium nelsoni, Haplosporidium costale and Perkinsus marinus in the eastern oyster (Crassostrea virginica Gmelin, 1791). Mol. Cell. Probes 15, 385-390. CrossRef
Perkins, F.O., 1968, Fine structure of the oyster pathogen Minchinia nelsoni (Haplosporida, Haplosporidiidae). J. Invertebr. Pathol. 10, 287-305. CrossRef
Perkins, F.O., 1969, Electron microscope studies of sporulation in the oyster pathogen, Minchinia costalis (Sporozoa: Haplosporida). J. Parasitol. 55, 897-920. CrossRef
Perkins, F.O., 1971, Sporulation in the trematode hyperparasite Urosporidium crescens DeTurk, 1940 (Haplosporida: Haplosporidiidae) – an electron microscope study. J. Parasitol. 57, 9-23. CrossRef
Perkins, F.O., 1975, Fine structure of Minchinia sp. (Haplosporida) sporulation in the mud crab, Panopeus herbstii. Mar. Fish. Rev. 37, 46-60.
Perkins F.O., 1990, Phylum Haplosporidia. In: Margulis L., Corliss J.O., Melkonian M., Chapman D.J. (Eds.), Handbook of Protoctista, Jones and Bartlett Publishing, Boston, MA, pp. 19-29.
Perkins F.O., 1991, “Sporozoa”: Apicomplexa, Microsporidia, Haplosporidia, Paramyxea, Myxosporidia, and Actinosporidia. In: Harrison F.W., Corliss J.O. (Eds.), Microscopic anatomy of Invertebrates, Vol. 1, Wiley-Liss, NY, pp. 261-331.
Perkins F.O., 2000, Phylum Haplosporidia Caullery & Mesnil, 1899, In: Lee J.J., Leedale G.F., Bradbury P. (Eds.), An illustrated guide to the protozoa, 2nd edition, Vol. 2, Society of Protozoologists, Lawrence, KS, pp. 1328-1341.
Perkins, F.O., Madden, P.A., Sawyer, T.K., 1977, Ultrastructural study of the spore surface of the haplosporidian Urosporidium spisuli. Trans. Am. Micros. Soc. 96, 376-382. CrossRef
Perkins, F.O., Zwerner, D.E., Dias, R.K., 1975, The hyperparasite, Urosporidium spisuli sp. n. (Haplosporea), and its effects on the surf clam industry. J. Parasitol. 61, 944-949. CrossRef
Pichot, Y., Comps, M., Tigé, G., Grizel, H., Rabouin, M.A., 1979, Recherches sur Bonamia ostreae gen. n., sp. n., parasite nouveau de l'huître plate Ostrea edulis L. Trav. Inst. Pêches Marit. 443, 131-140.
Powell, E.N., Klinck, J.M., Ford, S.E., Hofmann, E.E., Jordan, S.J., 1999, Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. III. Regional application and the problem of transmission. J. Shellfish Res. 18, 517-537.
Ragone Calvo L.M., Burreson E.M., 2003, Status of the Major Oyster Diseases in Virginia 2002, A Summary of the Annual Monitoring Program. Marine Resource Report No. 03-02. Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, Virginia. March 2003.
Ragone Calvo, L.M., Calvo, G.W., Burreson, E.M., 2002, Dual disease resistance in a selectively bred eastern oyster, Crassostrea virginica, strain tested in Chesapeake Bay. Aquaculture 220, 69-87. CrossRef
Ragone Calvo, L.M., Dungan, C.F., Roberson, B.S., Burreson, E.M., 2003, Systematic evaluation of factors controlling Perkinsus marinus transmission dynamics in lower Chesapeake Bay. Dis. Aquat. Org. 56, 75-86. CrossRef
Reece, K.S., Siddall, M.E., Stokes, N.A., Burreson, E.M., 2004, Molecular phylogeny of the Haplosporidia based on two independent gene sequences. J. Parsitol. 90, 1111-1122. CrossRef
Reece, K.S., Stokes, N.A., 2003, Molecular analysis of a haplosporidian parasite from cultured New Zealand abalone Haliotis iris. Dis. Aquat. Org. 53, 61-66. CrossRef
Renault, T., Stokes, N.A., Chollet, B., Cochennec, N., Berthe, F., Burreson, E.M., 2000, Haplosporidiosis in the Pacific oyster, Crassostrea gigas, from the French Atlantic coast. Dis. Aquat. Org. 42, 207-214. CrossRef
Russell, S., Frasc, S. Jr., Sunila, I., French, R.A., 2004, Application of a multiplex PCR for the detection of protozoan parasites of the eastern oyster Crassostrea virginica in field samples. Dis. Aquat. Org. 59, 85-91 CrossRef
Saunders, G.L., Powell, E.N., Lewis, D.H., 1993, A determination of in vivo growth rates for Perkinsus marinus, a parasite of Crassostrea virginica. J. Shellfish Res. 12, 229-240.
Siddall, M.E., Stokes, N.A., Burreson, E.M., 1995, Molecular phylogenetic evidence that the phylum Haplosporidia has an alveolate ancestry. Mol. Biol. Evol. 12, 573-581.
Smith G., Jordan S., 1992, Monitoring Maryland's Chesapeake Bay Oysters. A comprehensive characterization of Modified Fall Survey Results 1990-1991. Maryland Department of Natural Resources, Chesapeake Bay Research and Monitoring Division Report No. CBRM-OX-93-3, Oxford, Maryland. September 1992.
Sprague, V., 1963, Minchinia louisiana n. sp. (Haplosporidia, hdaplosporidiidae), a parasite of Panopeus herbstii. J. Protozool. 10, 267-274. CrossRef
Sprague, V., 1979, Classification of the Haplosporidia. Mar. Fish. Rev. 41, 40-44.
Stephenson, M.F., McGladdery, S.E., Stokes, N.A., 2002, Detection of a previously undescribed haplosporidian-like infection of blue mussel (Mytilus edulis) in Atlantic Canada. J. Shellfish Res. 21, 389.
Stephenson, M.F., McGladdery, S.E., Maillet, M., Veniot, A., Meyer, G., 2003, First reported occurrence of MSX in Canada. J. Shellfish Res. 22, 355.
Stokes, N.A., Burreson, E.M., 1995, A sensitive and specific DNA probe for the oyster pathogen Haplosporidium nelsoni. J. Euk. Microbiol. 42, 350-357. CrossRef
Stokes, N.A., Burreson, E.M., 2001, Differential diagnosis of mixed Haplosporidium costale and Haplosporidium nelsoni infections in the eastern oyster, Crassostrea virginica, using DNA probes. J. Shellfish Res. 20, 207-213.
Stokes, N.A., Siddall, M.E., Burreson, E.M., 1995a, Detection of Haplosporidium nelsoni (Haplosporidia: Haplosporidiidae) in oysters by PCR amplification. Dis. Aquat. Org. 23, 145-152. CrossRef
Stokes, N.A., Siddall, M.E., Burreson, E.M., 1995b, Small subunit ribosomal RNA gene sequence of Minchinia teredinis (Haplosporidia: Haplosporidiidae) and a specific DNA probe and PCR primers for its detection. J. Invertebr. Pathol. 65, 300-308. CrossRef
Sunila, I., Karolus, J., Volk, J., 1999, A new epizootic of Haplosporidium nelsoni (MSX), a haplosporidian oyster parasite, in Long Island Sound, Connecticut. J. Shellfish Res. 18, 169-174.
Sunila, I., Stokes, N.A., Smolowitz, R., Karney, R.C., Burreson, E.M., 2002, Haplosporidium costale (Seaside Organism), a parasite of the eastern oyster, is present in Long Island sound. J. Shellfish Res. 21, 113-118.
Tarnowski M., 2002, Maryland Oyster Population Status Report: 2001 Fall Survey. Maryland Department of Natural Resources, Annapolis, Maryland. November, 2002.
Taylor, R.L., 1966, Haplosporidium tumefacientis sp. n., the etiologic agent of a disease of the California sea mussel, Mytilus californianus Conrad. J. Invertebr. Pathol. 8, 109-121. CrossRef
United States National Marine Fisheries Service, 2003, Annual Commercial Landings Statistics: http://www.st.nmfs.gov/st1/commercial/landings/ annual_landings.html.
van Banning, P., 1977, Minchinia armoricana sp. nov. (Haplosporida), a parasite of the European flat oyster, Ostrea edulis. J. Invertebr. Pathol. 30, 199-206. CrossRef
Vilela H., 1950, Sporozoaires parasites de la Palourde, Tapes decussatus (L.). Rev. Fac. Ciências, Lisboa, Sér. C, 1, 379-386.
Wood, J.L., Andrews, J.D., 1962, Haplosporidium costale (Sporozoa) associated with a disease of Virginia oysters. Science 136, 710-711. CrossRef
Zaika, V.E., Dolgikh, A.V., 1963, A rare case of haplosporidian hyperparasitism by Urosporidium tauricum sp. n. in partenites of trematodes of the family Hemiuridae Lühe from the mollusk Rissoa splendida Eichw. Zool. Zhur. 42, 1727-1729 (in Russian).