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Haplosporidium (=Minchinia) armoricanum of Flat Oysters

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Category

Category 1 (Not Reported in Canada)

Common, generally accepted names of the organism or disease agent

European oyster minchiniasis, Haplosporidian disease of flat oysters.

Scientific name or taxonomic affiliation

Haplosporidium armoricanum (=Minchinia armoricana), originally described by van Banning (1977) and taxonomy revised by Bachère and Grizel (1983) and Azevado et al. (1999), within the family Haplosporidiidae, order Haplosporida, class Haplosporea of the phylum Haplosporidia (Burreson and Ford 2004). However, the taxonomy of haplosporidians needs a thorough revision (Hine et al. 2009).

Geographic distribution

In Ostrea edulis, Haplosporidium armoricanum, H. armoricanum-like parasites and parasites reported as Haplosporidium sp. were detected in Atlantic (Brittany and Arcachon) and Meditteranean (Etang de Thau) coasts of France (Balouet 1978, Pichot et al. 1979, Cahour et al. 1980, Bachère and Grizel 1983, Bonami et al. 1985, Pichot 1986), Atlantic (Galicia) coast of Spain (Azevado et al. 1999, da Silva et al. 2005), the Netherlands (van Banning 1977, 1979; Hine et al. 2007) and Ireland (Lynch and Culloty 2011). The Haplosporidium detected in heart smears from one O. edulis in Ireland was most likely H. armoricanum based on PCR and DNA sequencing (Lynch et al. 2013). Haplosporidian plasmodia have also been reported in Ostrea conchaphila from Oregon, USA that were imported from California (Mix and Sprague 1974).

Host species

Ostrea edulis and Ostrea angasi. Possibly also in Olympia oysters, Ostrea conchaphila (=lurida).

Impact on the host

Comps (1976) reported plasmodia (4 to 8 µm in diameter) of an unidentified haplosporidian in a lesion of haemocytic infiltration (4 mm diameter) in the gills of O. edulis from a claire pond in La Tremblade, France. Oysters in late stages of the infection are often thin and watery in appearance and have a characteristic brownish colour caused by masses of spores in the connective tissue of all organs. Although the disease is fatal, the prevalence of infection to date has been low (less than 4%) with insignificant impact on the flat oyster culture industry in Europe (van Banning 1977, da Silva et al. 2005, Lynch et al. 2013). However, an acclimatization experiment with O. angasi in France indicated that this introduced species of oyster was exceptionally sensitive to infection with a haplosporidian similar to H. armoricanum and the Haplosporidium sp. reported by Bachère and Grizel (1983) (Bougrier et al. 1986, Bachère et al. 1987).

Diagnostic techniques

Gross Observations

Oysters in the terminal phase of the disease are usually thin and watery in appearance with a characteristic brownish colour caused by masses of spores in the connective tissues.

Wet Mounts

The ovoid spores (5.0-5.5 x 4.0-4.5 µm) are remarkably uniform in size in squash preparations of fresh material. At opposite ends of the spore are two characteristic long (70-100 µm) projections of the outer spore wall which are especially evident in interference light microscopy (van Banning 1977).

Smears

In order to screen heart tissue for parasites, open the oyster carefully to avoid disruption of the pericardial cavity, drain away excess seawater and other fluids, and blot the area around the pericardial cavity with clean tissue paper to remove any potential contaminants. Remove the heart using clean forceps. Make imprints of the heart on slides followed by air drying the slides and staining them with Wright, Wright-Giemsa, May-Grunwald-Giemsa or equivalent stain (e.g., Hemacolor, Merck; Diff-QuiK, Baxter). Examine for plasmodia (11 µm to 18 µm in diameter) containing 5 to 17 nuclei (1–2 µm in size) (Lynch et al. 2013).

Histology

The connective tissue of infected flat oysters contains plasmodia (17-25 µm in diameter), sporonts (early stages in sporulation 30-45 µm in diameter), and sporocysts (35-50 µm) containing 100-150 ellipsoid spores (4.0-4.5 × 3.0-4.5 µm) (van Banning 1977). In some infected oysters, there was no notable haemocyte infiltration nor evidence of important necrosis (Cahour et al. 1980). In heavy infections, plasmodia are rare indicating synchronized sporulation. The sporonts and sporocysts invade all of the connective tissue and are especially abundant in the visceral mass between the digestive gland tubules but were not observed in the epithelium of the tubules (van Banning 1977).

Electron Microscopy

Cahour et al. (1980) described the diplokaryon, process of formation of the sporoplasm and the episporoplasm, and the spore of H. armoricanum (=M. armoricana). Subsequently, Vivarès et al. (1982) described the vegetative stages (uni-nucleate and bi-nucleate plasmodia) of a haplosporidian from O. edulis from Saint-Philibert (near La Trinité-sur-Mer, Brittany), France, but in the absence of spores, did not attempt to name the parasite. In addition, Bachère and Grizel (1983) described uni-nucleate, diplokaryotic, early sporont and spore stages of H. armoricanum. Also, the ultrastructure of haplosporidian plasmodia described by Bonami et al. (1985) may have been of the prespore stages of H. armoricanum. The spores are ellipsoid (about 4 µm long and 3 µm wide) with an operculum over the orifice and ornamented with two long episomal cytoplasm extensions (70 to 130 µm long and 25 nm thick) attached eccentrically at opposite sides of the outer spore wall by a bundle of 9 to 13 cylindrical fibers (van Banning 1977, Pichot et al. 1979, Azevado et al. 1999). The spore wall consists of layers, the sporoplasm includes haplosporosomes (round, oval, or rod shaped, about 120 to 600 nm in size) and complex Golgi apparati situated near the orifice and the nucleus. The nature of the spore ornamentation indicated that this parasite belongs in the genus Haplosporidium and not Minchinia (Perkins and van Banning 1981, Bachère and Grizel 1983, Azevado et al. 1999). Further details on the ultrastructure of H. armoricanum including information on sporulation were presented by Hine et al. (2007).

DNA Probes

DNA was isolated from the ethanol fixed tissue of a heavily infected O. edulis, followed by polymerase chain reaction (PCR) and sequencing of the 18S ribosomal RNA (Hine et al. 2007). The partial sequence of the small subunit (SSU) ribosomal RNA gene was deposited in GenBank and identified as Haplosporidium sp. MYE-2005 (Accession # AY781176). Lynch et al. (2013) also deposited in GenBank the partial sequence of the SSU of a haplosporidian isolated from one O. edulis from Ireland that was identified as Haplosporidium sp. MYE-2005 isolate UCC3 (Accession # JX073257) and noted that it was possibly H. armoricanum.

Methods of control

No known methods of prevention or control.

References

Azevedo, C., J. Montes and L. Corral. 1999. A revised description of Haplosporidium armoricanum, parasite of Ostrea edulis L. from Galicia, northwestern Spain, with special reference to the spore-wall filaments. Parasitology Research 85: 977-983.

Bachère, E. and H. Grizel. 1983. Mise en évidence d'Haplosporidium sp. (Haplosporida - Haplosporidiidae) parasite de l'huître plate Ostrea edulis L. Revue des Travaux de l'Institut des Pêches Maritimes. 46: 226-232. (In French with English abstract).

Bachère, E., D. Chagot, G. Tigé and H. Grizel. 1987. Study of a haplosporidian (Acetospora), parasitizing the Australian flat oyster Ostrea angasi. Aquaculture 67: 266-268.

Balouet, G. 1978. Études sur la pathologie des huîtres. Contrat C.N.E.X.O. 78/1857. 47 pp (see pg. 18-19 for reference to haplosporidians). (In French with English abstract).

Bonami, J.R., C.P. Vivares and M. Brehelin. 1985. Étude d'une nouvelle haplosporidie parasite de l'huître plate Ostrea edulis L.: morphologie et cytologie de différents stades. Protistologica 21: 161-173. (In French, with English summary).

Bougrier, S., G. Tigé, E. Bachère and H. Grizel. 1986. Ostrea angasi acclimatization to French coasts. Aquaculture 58: 151-154.

Burreson, E.M. and S.E. Ford. 2004. A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17: 499-517.

Cahour, A., M. Poder and G. Balouet. 1980. Présence de Minchinia armoricana (Haplosporea, Haplosporida) chez Ostrea edulis d'origine française. Comptes Rendus des Seances de la Societe de Biologie et de ses Filiales 174: 359-364. (In French, with English summary).

Comps, M. 1976. Haplosporidie parasite des branchies de l'huître palte Ostrea edulis L. International Council for Exploration of the Sea C.M. 1976/K:22: 3 pp.(In French).

da Silva, P.M., J. Fuentes and A. Villalba. 2005. Growth, mortality and disease susceptibility of oyster Ostrea edulis families obtained from brood stocks of different geographical origins, through on-growing in the Ría de Arousa (Galicia, NW Spain). Marine Biology 147: 965-977.

Hine, P.M., M.Y. Engelsma and S.J. Wakefield. 2007. Ultrastructure of sporulation in Haplosporidium armoricanum. Diseases of Aquatic Organisms 77: 225-233.

Hine, P.M., R.B. Carnegie, E.M. Burreson and M.Y. Engelsma. 2009. Inter-relationships of haplosporidians deduced from ultrastructural studies. Diseases of Aquatic Organisms 83: 247-256.

Lynch, S.A. and S.C. Culloty. 2011. The incidence of haplosporidians, Haplosporidium nelsoni and Haplosporidium amoricanum, in the Pacific oyster, Crassostrea gigas, and the European flat oyster, Ostrea edulis, in Ireland. Journal of Shellfish Research 30: 528. (Abstract).

Lynch, S.A., A. Villalba, E. Abollo, M. Engelsma, N.A. Stokes and S.C. Culloty. 2013. The occurrence of haplosporidian parasites, Haplosporidium nelsoni and Haplosporidium sp., in oysters in Ireland. Journal of Invertebrate Pathology 112: 208-212.

Mix, M.C. and V. Sprague. 1974. Occurrence of a haplosporidian in native oysters (Ostrea lurida) from Yaquina Bay and Alsea Bay, Oregon. Journal of Invertebrate Pathology 23: 252-254.

Perkins, F.O. and P. van Banning. 1981. Surface ultrastructure of spores in three genera of Balanosporida, particularly in Minchinia armoricana van Banning, 1977 - the taxonomic significance of spore wall ornamentation in the Balanosporida. The Journal of Parasitology 67: 866-874.

Pichot, Y. 1986. Sporulation d'Haplosporidium sp. (Haplosporida, Haplosporidiidae) chez l'huître Ostrea edulis L. du bassin d'Arcachon (France). In: Vivarès C.P., J. R. Bonami, E. Jaspers (eds). Pathology in marine aquaculture. European Aquaculture Society, Special Publication 9: 119-126. (In French, with English abstract).

Pichot, Y., M. Comps and J.-P. Deltreil. 1979. Recherches sur Haplosporidium sp. (Haplosporida - haplosporidiidae) parasite de l'huitre plate Ostrea edulis L. Revue des Travaux de l'Institut des Pêches Maritimes. 43: 405-408. (In French).

Sparks, A.K. 1985. Synopsis of Invertebrate Pathology Exclusive of Insects. Elsevier Science Publishing Co., Amsterdam. p. 285-286.

van Banning, P. 1977. Minchinia armoricana sp. nov. (Haplosporida), a parasite of the European flat oyster, Ostrea edulis. Journal of Invertebrate Pathology 30: 199-206.

van Banning, P. 1979. Haplosporidian diseases of imported oysters, Ostrea edulis, in Dutch estuaries. Marine Fisheries Review 41: 8-18.

van Banning, P. 1985. Minchinia armoricana disease of the flat oyster. In: C.J. Sindermann (ed.) Fiches d'Identification des Maladies et Parasites des Poissons, Crustacés et Mollusques. No. 17. ICES, Copenhague 4 pp.

Vivarès, C.P., M. Brehélin, F. Cousserans and J.-R. Bonami. 1982. Mise en évidence d'une nouvelle haplosporidie parasite de l'huître plate Ostrea edulis L. Comptes Rendus Académie des Sciences Paris, Série III 295: 127-130. (In French with English abstract).

Citation Information

Bower, S.M. (2014): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Haplosporidium (=Minchinia) armoricana of Flat Oysters.

Date last revised: May 2014
Comments to Susan Bower

Date modified: