Gill Disease of Portuguese Oyster
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Category
Category 1 (Not Reported in Canada)
Common, generally accepted names of the organism or disease agent
Gill disease of Portuguese oysters, Gill necrosis virus disease (GNV), Maladie des branchies.
Scientific name or taxonomic affiliation
Gill disease (GNV) is associated with an icosahedral DNA virus thought to be an iridovirus and affiliations with the morphologically similar viruses that cause oyster velar virus disease (OVVD) and haemocyte infection virus disease (HIV) are unknown (Elston 1997). However, molecular characterization (currently not available) is required to assess their identity (Arzul et al. 2017). As indicated by Renault (2016) the presumptive link to the Iridoviridae is substantial, but definitive demonstration of viral etiology of the diseases must be accomplished by experimental transmission. Because the exact identification of these viruses has not been carried out, the term irido-like viruses needs to be used until their affiliations are established (Renault 2016). A protistan, Thanatostrea polymorpha belonging to the Phyla Sarcomastigophora or Labyrinthomorpha, has also been associated with gill disease (Franc et al. 1969, Comps and Duthoit 1976).
Geographic distribution
Atlantic coast of Europe (France, Portugal (Ferreira and Dias 1973), Spain), and in Great Britain in Crassostrea angulata imported from Portugal (Alderman and Gras 1969, Comps 1985, Renault 2016). Comps (1969a, 1970) reported that the gill abnormalities that were observed in C. gigas from Japan, Korea and British Columbia, Canada were different from maladie des branchies observed in C. angulata.
Host species
Crassostrea angulata (Comps 1980) and Crassostrea gigas (cultured in France, Comps and Bonami 1977) which is less sensitive to the disease (Comps 1970, 1985; Renault 2016). Similar clinical signs were reported in Ostrea edulis but not identified as the same disease which afflicts C. angulata.
Impact on the host
Extensive gill erosion corresponding with high mortalities occurred in C. angulata between 1966 to 1973 and the cause attributed to a viral infection (Comps and Duthoit 1976, 1977(1979); Comps 1978; Comps 1988; Renault and Novoa 2004). In Great Britain, mortalities exceeded 90% in some cases of C. angulata imported from Portugal (Alderman and Gras 1969). Although mortalities among C. angulata from important culture areas in France reached 70% in certain years, C. gigas cultivated in France appeared to have acquired complete resistance to gill disease, as no gill-diseased individuals of this species were found between 1969 and 1971 (Renault and Novoa 2004, Renault 2016).
In C. angulata, initial clinical signs of yellow spots on the gills progress to brown discolouration with associated necrosis and degeneration leaving a perforation or V-shaped indentation if the lesion occurred on the edge of the gill (Alderman and Gras 1969). Yellow or green pustules may also occur on the mantle or adductor muscle (Comps 1969b, 1970; Renault 1996, Renault and Novoa 2004). In advanced stages of the disease, infection might lead to degeneration of the entire gill structure (Alderman and Gras 1969, Renault 2016, Arzul et al. 2017). Similar but less extensive lesions could be observed in infected C. gigas (Renault and Novoa 2004, Arzul et al. 2017).
Oysters with non-proliferating infections, or in a state of recovery (healing or cicatrization (Comps 1970)), may show gill lesions but no tissue necrosis. Gill disease (GNV) is regarded as one factor in the elimination of C. angulata from important culture areas on the Atlantic coast of France (Comps 1970, Comps and Duthoit 1976). Also, in addition to HIV, GNV is associated with the almost total extermination of C. angulata, in European Atlantic waters in the early 1970's (Arzul et al. 2017). Although active disease has not been reported since 1969, mortalities and associated irido-like virus (possibly HIV) was detected in experimental C. angulata in 1983-1984 (Bougrier et al. 1986). Renault (2016) indicated that the pathogenicity of GNV was not demonstrated, nevertheless, GNV and HIV have been identified as the most probable cause of recurrent mass mortalities of C. angulata observed in Europe since 1966.
Diagnostic techniques
Gross observations
Preliminary diagnosis can be made on the visible signs as described above. With a dissecting microscope (macroscopy), localized degeneration of gill filaments and the formation of small excavations are evident (Comps 1985).
Histology
Examine for necrosis of gill or labial palp epithelial tissue, cellular hypertrophy and massive haemocytic cellular infiltration around the lesions (Comps 1988). In most lesions, polymorphic hypertrophic cells and hypertrophic globular cells with basophilic, cytoplasmic inclusions (5 to 15 μm in diameter), numerous vacuoles and fine granules were observed (Comps 1970, Renault 2016). Also, giant polymorphic cells (about 30 μm in size) were observed with a hypertrophied nucleus (Comps, 1988). The cytoplasmic inclusions tend to be Feulgen positive (Comps and Duthoit 1976) and show a yellow-green fluorescence with acridine orange stain (Comps 1985). Because the virus was not isolated from oysters nor characterized chemically, the presence of deoxyribonucleic acid (DNA) from the virus was demonstrated by histochemical techniques (Comps 1988). Comps (1988) speculated that the initial difficulties in isolation and analysis of these viruses stemmed partly from the relative scarcity of the virions: very few cells were infected, and the number of virions is usually light.
Electron microscopy
Cytoplasm of hypertrophied haemocytes or connective tissue cells in the gills containing virogenic stroma and icosahedral enveloped viral particles (350 to 380 nm in diameter) with an electron-opaque/dense core (190-200 nm in diameter) surrounded by an electron-lucent zone and another dense layer about 45 nm in thickness (Comps and Bonami 1977). The viral particles are enclosed within two membranes separated by a clear zone (Renault and Novoa 2004, Arzul et al. 2017). Renault and Novoa (2004) and Renault (2016) depict a typical irido-like virus particle from C. angulata. The virons are assembled in cytoplasmic inclusions by budding through de novo membrane at the edge of virogenic stroma (Comps and Duthoit 1976, 1977 (1979); Comps 1978; Elston 1997). Other cytopathological changes include the enlargement of the nucleus combined with a disappearance of the chromatin and nucleolus (Comps 1988).
Methods of control
No known methods of prevention or control. Because of the severity of the disease C. angulata is no longer cultured commercially and has been replaced by C. gigas which is more resistant to the disease (Renault and Novoa 2004). Renault (2016) indicated that in addition to standard techniques such as histopathology and ultrastructure examination, new tools such as those incorporating molecular assays (i.e., DNA detection and analysis) are required in order to obtain new insights into the management and control of viral diseases in aquaculture. Another important strategy is not to move oysters from areas with the disease (currently or historically) to areas where the disease has not been observed. For example, Renault (1996) speculated that both GNV and HIV could have spread throughout Europe as a result of international trade.
References
Alderman, D.J. and P. Gras. 1969. "Gill Disease" of Portuguese oysters. Nature 224: 616-617.
Arzul, I., S. Corbeil, B. Morga and T. Renault. 2017. Viruses infecting marine molluscs. Journal of Invertebrate Pathology 147: 118-135.
Bougrier, S., G. Raguenes, E. Bachere, G. Tige and H. Grizel. 1986. Essai de réimplantation de Crassostrea angulata en France. Résistance au chambrage et comportement des hybrides C. angulata - C. gigas. Conseil International pour l'Exploitation de la Mer (CIEM), Comité de la Mariculture C.M. 1986/F: 38, 10 pp. (in French only)
Comps, M. 1969a. Anomalies branchiales chez Crassostrea gigas (Thunberg). Conseil International pour l'Exploration de la Mer C.M.1969/K2: 4 pp. (in French only)
Comps, M. 1969b. Observations relatives à l'affection branchiale des huîtres portugaises (Crassostrea angulata Lmk). Revue des Travaux de l'Institut des Pêches Maritimes 33: 151-160. (in French only)
Comps, M. 1970. La maladie des branchies chez les huitres du genre Crassostrea caracteristiques et evolution des alterations processus de cicatrisation. Revue des Travaux de l'Institut des Pêches Maritimes 34: 23-43. (in French only)
Comps, M. 1978. Évolution des recherches et études récentes en pathologie des huîtres. Oceanologica Acta 1: 255-262. (in French only)
Comps, M. 1980. Mise en évidence par fluorescence du virus de la maladie des branchies de l'huître portugaise Crassostrea angulata Lmk. Sciences et Pêches, Bulletin de l'Institut des Pêches Maritimes 301: 17-18.
Comps, M. 1985. Maladie des branchies (Gill disease). In: Sindermann, C.J. (ed.) Identification Leaflets for Diseases and Parasites of Fish and Shellfish, No. 23. ICES, Copenhagen, 4 p. (in French only)
Comps, M. 1988. Epizootic diseases of oysters associated with viral infections. In: Fisher W.S. (ed.) Disease Processes in Marine Bivalve Molluscs. American Fisheries Society Special Publication 18: 23-37.
Comps, M. and J.-R. Bonami. 1977. Infection virale associée à des mortalités chez l'huître Crassostrea gigas Thunberg. Comptes Rendus Académie des Sciences de Paris, Série D285: 1139-1140. (in French only)
Comps, M. and J.-L. Duthoit. 1976. Infection virale associée à la "maladie des branchies" de l'huître portugaise Crassostrea angulata LmK. Comptes Rendus Académie des Sciences de Paris, Série D 283: 1595-1597. (in French only)
Comps, M. and J.-L. Duthoit. 1977 (1979). Infections virales chez les huîtres Crassostrea angulata Lmk. et Crassostrea gigas Th. Haliotis 8: 301-307. (in French only)
Elston, R. 1997. Special topic review: bivalve mollusc viruses. World Journal of Microbiology and Biotechnology 13: 393-403.
Farley, C.A. 1978. Viruses and viruslike lesions in marine mollusks. Marine Fisheries Review 40:18-20.
Ferreira, P.S. and A.A. Dias. 1973. Sur la répartition et l'évolution de l'altération des branchies de Crassostrea angulata dans le Tage, Le Sado et l'Algarve. Conseil Internaticnal pour l'Exploitation de la Mer, Comité des mollusques, coquillages et benthos, C.M. 1973/K:6, 19 pp. (in French only)
Franc, A., M. Arvy and P.P. Gras. 1969. Biologie: sur Thanatostrea polymorpha n.g., n.sp., agent de destruction des branchies et des palpes de l'huître portugaise. Comptes rendus de l'Académie des Sciences de Paris, Série D 268: 3189-3190.
Marteil, L. 1969. La maladie des branchies des huîtres portugaises des côtes françaises de l'Atlantique. Revue des Travaux de l'Institut des Pêches Maritimes 33: 145-150.
Marteil, L. 1976. La conchyliculture française, 2 partie: biologie de l'huitre et de la moule. Chapitre VI: maladies et mortalites. Revue des Travaux de l'Institut des Pêches Maritimes. 40: 285-313.
Renault, T. 1996. Appearance and spread of disease among bivalve molluscs in the northern hemishpere in relation to international trade. Revue Scientifique et Technique de l'Office International des Epizooties 15: 551-561. (in French only)
Renault, T. 2016. Chapter 36 - Iridolike viruses of mollusks, In: Kibenge, F.S.B., M.G. Godoy (eds.) Aquaculture Virology. Academic Press, San Diego, pp. 507-512.
Renault, T. and B. Novoa. 2004. Viruses infecting bivalve molluscs. Aquatic Living Resources 17: 397-409.
Citation information
Bower, S.M. (2022): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Gill Disease of Portuguese Oysters.
Date last revised: October 2022
Comments to Susan Bower
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