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Viral infections of clams and cockles

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Category

Category 1 (Not Reported in Canada)

Common, generally accepted names of the organism or disease agent

Viruses and virus-like infections of clams.

Scientific name or taxonomic affiliation

Viruses have been reported from various species of clams and cockles (Lopez et al. 2012). In some cases, the etiological agent of the disease has not be identified (for example see Shen et al. (2016) where the pathogen was described as a "spherical virus" in Meretrix meretrix from China). Following is a list of these reports, including more recent information, clustered according to similarity of disease aetiology. Available information pertaining to each cluster of reports has the same letter code in subsequent subject headings presented below.

  1. Virus-like particles with characteristics of the family Papillomaviridae (referred to as Papovaviridae prior to 1999) and with resemblance to Polyomavirus (Farley 1976, 1978; Harshbarger et al. 1977 (1979)). In addition, Montes et al. (2001) and Ruiz et al. (2011) reported unenveloped virus particles of similar size and symmetry to those in the families Papillomaviridae and Polyomaviridae. Both of these families were included in the class Papovaviricetes which was established in 2019 (Koonin et al. 2019).
  2. Virus with characteristics of the family Reoviridae especially with strong morphological resemblance to the fish pathogen, infectious pancreatic necrosis virus (IPN) (Hill 1976). Meyer and Burton (2009) reported the isolation of Aquareovirus genotype A.
  3. Herpes-like virus infection in European clams was first detected in France by Renault et al. (2001a, b). The virus was identified as Ostreid herpesvirus 1 (OsHV-1) in the genus Ostreavirus, and family Malacoherpesvividae (Davison et al. 2009, Burge et al. 2011, Arzul et al. 2017, Renault 2021) and was also reported in cockles from Australia (Evans et al. 2017). A herpesvirus-like agent was also observed in clams from Alaska (Meyers et al. 2009, Meyers and Burton 2009) and California, USA (Burge et al. 2011). In China, Bai et al. (2015, 2016) reported new variants of OsHV-1 allocated to a separate subclade and described as OsHV-1-SB by Xia et al. (2015) from the blood (ark shell) clam.
  4. Birnavirus with serological and biochemical properties similar to infectious pancreatic necrosis virus (AB IPNV) in fish (Lo et al. 1988, Chou et al. 1994). This virus was called marine birnaviruses (MABV) and was detected by the polymerase chain reaction (PCR) technique in many species of molluscs around Japan (Suzuki and Nojima 1999). MABV were defined as a group within the genus Aquabirnavirus in the family Birnaviridae (Renault 2008, Arzul et al. 2017). Members of the Birnaviridae are non-enveloped, bi-segmented, double-stranded RNA viruses (Lopez et al. 2012, McGladdery 2011).
  5. Virus-like particles associated with cytological changes in digestive and secretory (= basophil) cells in clams and morphology reminiscent of enteroviruses (Picornaviridae) and caliciviruses (Caliciviridae) (Hine and Wesney 1997, Carballal et al. 2003). Also, RNA-type viruses with characteristics suggestive of viruses in the Picornaviridae and Parvoviridae families were detected in connective tissue cell of clams (Novoa and Figueras, 2000, Dang et al. 2009, Bateman et al. 2012, Renault 2016). Similar viral infections have been reported from mussels and scallop .

Geographic distribution

  1. Initially reported from the north eastern coast of the United States (Farley 1976, 1978) including Chesapeake Bay (Harshbarger et al. 1977 (1979)). Subsequently, similar viruses were detected in clams from the northern Mediterranean coast of Spain (Montes et al. 2001) and from Galicia, north west Spain (Ruiz et al. 2011).
  2. Coast of Great Britain (Hill 1976), and Vallenar Bay on the north end of Gravina Island in southeastern Alaska, USA (Meyer and Burton 2009).
  3. Normandy coast of France (Renault et al. 2001a, b), Annette Island, Alaska and a bivalve hatchery in Seward, Alaska, USA (Meyers et al. 2009, Meyer and Burton 2009), Tomales Bay, California, USA (Burge et al. 2011), from bivalve hatcheries on the north coast of China (Bai et al. 2015, 2016; Xia et al. 2015) and in wild stocks of Sydney cockles from the Georges River, New South Wales, Australia (Evans et al. 2017).
  4. Taiwan (Lo et al. 1988, Chou et al. 1994, Renault 2008) and Alaska, USA (Meyers and Burton 2009). Suzuki and Nojima (1999) detected MABV by PCR in 4 coastal prefectures (Mie, Hiroshima, Kochi and Saga) around the southern end of Japan, including the Ariake Sea and in shell samples from Korea (Suzuki et al. 1997). McGladdery (2011) reported birnavirus-like viruses in clams from the coast of Scotland.
  5. New Zealand (Hine and Wesney 1997), intertidal beds in Ría do Barqueiro, Galicia, NW Spain (Carballal et al. 2003) and in two batches of clams farmed in Galicia, NW Spain (Novoa and Figueras 2000). Virus-like particles with morphological characteristics of both the Picornaviridae and Parvoviridae were detected in clams from France (Dang et al. 2009) and the south coast of England (Bateman et al. 2012).

Host species

  1. Mya arenaria on the north eastern coast of the United States (Farley 1976, 1978; Harshbarger et al. 1977 (1979)); Ruditapes philippinarum(=Tapes semidecussatus) on the Mediterranean coast of Spain (Montes et al. 2001); and Ensis arcuatus (Ruiz et al. 2011) and Ensis siliqua (López et al. 2011, 2012) on the coast of Galicia, Spain.
  2. Macomangulus (=Angulus, =Tellina) tenuis  and experimentally infective to Crassostrea gigas in Great Britain (Hill 1976). Panopea generosa (=abrupta) in Alaska (Meyers et al. 2009, Meyers and Burton 2009).
  3. Larvae of Ruditapes (=Venerupis ,=Tapes) philippinarum and Ruditapes decussatus in France (Renault et al. 2001a, b; Renault and Arzul 2001, Renault 2021). Initially recognized as a herpes-like virus, further research including molecular assays (Renault and Arzul 2001) and interspecies transmission studies (Arzul et al. 2001a) revealed that the virus (OsHV) was the same as that associated with mortalities of larval and spat oysters in France (Arzul et al. 2001b, Renault 2021). In Alaska, adult Protothaca staminea had Cowdry Type A intranuclear inclusion bodies containing arrays of virus-like particles resembling herpesvirus nucleocapsids. In California, OsHV DNA was detected in adult Ruditapes(=Venerupis) philippinarum (Burge et al. 2011). In China, broodstock of blood clams Anadara (=Scapharca) broughtonii experienced mass mortalities associated with variants of OsHV-1 (Bai et al. 2015, 2016; Xia et al. 2015). Bai et al. (2015) also reported detecting OsHV-1 DNA in Meretrix meretrix and R. philippinarum on the north coast of China. Low levels of OsHV-1 DNA was detected in wild stocks of Sydney cockles Anadara trapezia on the east coast of Australia from an area where the virus was also detected in oysters (Evans et al. 2017). Note that the virus known as OsHV-1 has a wide host range that, in addition to clams/cockles (species in the genus Anadara have common names of either clam or cockle) and oysters, also includes scallops (Renault 2008, Guo and Ford 2016). Mussels were reported to be less susceptible than Crassostrea gigas to OsHV-1 (Novoa et al. 2016) and the herpesvirus in abalone is a closely related species (Crane et al. 2016).
  4. Meretrix lusoria (Lo et al. 1988, Chou et al. 1994) and the Agemaki or jack knife clam Sinonovacula (=Sinonovacura) constricta (Renault 2008) from coastal areas of Taiwan. Protothaca staminea from the coast of Alaska (Meyers and Burton 2009). In samples of S. constricta from Japan and Korea, 2 strains of birnavirus were isolated and characterized by Suzuki et al. (1997). Also in Japan, Ruditapes philppinarum (=Tapes japonica), S. constricta, the ark shell Anadara subcrenata, and cockle Anadara granasa bisenensis were PCR-positive for MABV (Suizuki and Nojima 1999). In Scotland, birnavirus-like viruses were isolated from the tellin clam Macomangulus(=Tellina) tenuis on fish cell lines (McGladdery 2011).
  5. Toheroa, Paphies ventricosum, a large clam collected recreationally in New Zealand (Hine and Wesney 1997), cockles Cerastoderma edule commercially harvested in Galicia, Spain (Carballal et al. 2003), carpet-shell clams Ruditapes decussatus farmed in Galicia, Spain (Novoa and Figueras 2000) and possibly Manila clams Ruditapes philippinarum experiencing mortalities in Arcachon Bay, France (Dang et al. 2009) and in the same species of clam experiencing mortalities on the south coast of England (Bateman et al. 2012).

Impact on the host

For many of the viral infections in clams and cockles, the impact on hosts have not been specifically described. However, available information is as follows:

  1. In a sample of 50 M. arenaria from an area in Massachusetts, U.S. where paralytic shellfish poisoning had occurred, 20% of the clams had histological characteristics typical of papova-like viral infection in gill epithelial cells, and 10% of the clams had gill hyperplasia (Farley 1976). Montes et al. (2001) identified severe alterations in virus-infected cells but determined that infection was opportunistic in R. philippinarum (=T. semidecussatus) that were heavily infected by the protistan parasite Perkinsus olseni (=atlanticus). During a histological survey of E. arcuatus from Galicia, Spain, basophilic inclusion bodies were observed in epithelial cells of the digestive gland. The prevalence and intensity of these inclusions were usually low, and no adverse effects were reported in E. arcuatus (Ruiz et al. 2011).
  2. In Alaska, both adult and juvenile P. generosa had no microscopic cytopathology suggestive of any virus infections but some samples, tested on monolayers of fish cell cultures (bluegill fry cells – BF-2), showed cytopathic effects (CPE) (Meyers et al. 2009). Meyers and Burton (2009) indicated that bivalve molluscs are asymptomatic vectors of Aquareovirus and isolates from bivalves likely represent bioaccumulation by filter feeding after the virus was shed from a nearby fish host.
  3. In France, the herpes-like viral infection in larval R. philippinarum was associated with sporadic high mortalities in a commercial hatchery (Renault et al. 2001a, b). In Alaska, no overt disease nor mortality of wild or cultured bivalve molluscs was associated with a herpes-like virus infection (Meyers et al. 2009, Meyers and Burton 2009). However, from 1994 to 2002 the prevalence of infection ranged from 3.4 to 44.2% (Meyers et al. 2009). The absence of vertical transmission in the hatchery lead to the speculation that the Alaskan herpes-like virus may be less pathogenic in natural bivalve populations possibly due to consistently low seawater temperatures (rarely reaching 20°C) in Alaska (Meyers et al. 2009, Meyers and Burton 2009). In California, no histological abnormalities were found and OsHV DNA was detected in apparently healthy, commercially cultured R. philippinarum using conventional polymerase chain reaction assays designed to detect OsHV (Burge et al. 2011). However, in China, mass mortalities of A. broughtonii broodstock in several hatcheries were associated with variants of OsHV-1 (Xia et al. 2015; Bai et al. 2015, 2016). The mortalities were associated with a water temperature increase to 18°C (Bai et al. 2016). The variant OsHV-1-SB was infectious to A. broughtonii by intramuscular injection with mortality curves, histological lesions, abundance of herpesvirus-like particles seen by electron microscopy, and quantities of OsHV-1-SB detected by molecular assays in the challenged group, similar to those observed in diseased blood clams at affected hatcheries (Bai et al. 2017). Arzul et al. (2017) indicated that the OsHV-1 variants found in China exhibit different host stage preference (i.e., mortalities in adult clams) compared with those found in the other countries (where this virus generally induces mortality in young bivalve stages with adult bivalves apparently resistant to disease and possibly acting as reservoirs).
  4. The birnavirus was associated with mass mortalities among farmed M. lusoria and high mortalities could be replicated in the laboratory in small M. lusoria (4 months old with a mean weight of 1.2 grams) especially when the temperature was increased by 8°C (from 25 to 33°C) after viral infection (Chou et al. 1994). Birnavirus was also associated with mass mortalities of S. constricta in the Ariake Sea, Japan (Suzuki et al. 1997). Kitamura et al. (2000), Renault (2008) and Arzul et al. (2017) speculated that marine birnaviruses may be opportunistic pathogens which persistently infects marine organisms and becomes pathogenic under stressful condition, such as changes in temperature, spawning and exposure to heavy metals (Chou et al. 1998), resulting in mortality by increasing host susceptibility. Meyer and Burton (2009) indicated that bivalve molluscs are generally asymptomatic carriers and/or vectors of Aquabirnavirus. Suzuki and Nojima (1999) came to a similar conclusions and suggested that marine birnavirus in most wild shellfish is a persistent but not latent infection.
  5. Sporadic population crashes of P. ventricosum in New Zealand (Hine and Wesney 1997) and high mortalities of C. edule (Carballal et al. 2003) and R. decussatus (Novoa and Figueras 2000, Renault and Novoa 2004) in Galicia, Spain. The heavy mortalities of R. decussatus  from 2 culture locations in Galicia occurred during the late summer and early fall of 1997 and 1998 (Novoa and Figueras 2000). In France, virus-like particles possibly belonging to the Picornaviridae were associated with extensive adductor muscle lesions (brown muscle disease) in R. philippinarum experiencing mortalities (Dang et al. 2009). In southern England, a picorna-like virus was implicated in the 2008 mortality event in farmed and wild R. philippinarum (Bateman et al. 2012). Bateman et al. (2012) suggested that the stress of the viral infection may leave the clams more susceptible to other opportunistic pathogens.

Diagnostic techniques

Gross observations

  1. In China, broodstock of diseased blood clams (Anadara  broughtonii) from populations experiencing mass mortalities showed clinical signs that included slow response, gaping valves and pale visceral mass (Bai et al. 2016).
  2. The gills of diseased M. lusoria were described as being abnormally dark grey (usually white) in colour (Chou et al. 1994).

Histology

  1. Finely granular, Feulgen-positive, intranuclear inclusions in the connective tissue cells, haemocytes and gill and/or digestive gland epithelium. In M. arenaria, affected cells may have some hypertrophy and marginated chromatin in the particle-filled nucleus (Farley 1976, Harshbarger et al. 1977(1979), Elston 1997). In E. arcuatus, the unidentified basophilic inclusions caused high hypertrophy of infected epithelial cells of the digestive gland which had chromophilic margins (using light microscopy and haematoxylin and eosin stain), and showed a Feulgen-positive reaction, indicating the presence of DNA (Ruiz et al. 2011).
  2. Inclusion bodies in the cells of the digestive gland of Macomangulus tenuis (Hill 1976).
  3. Presence of abnormal nuclei (condensed or with chromatin margination) in fibroblast-like cells and/or haemocytes throughout the connective tissue and possibly in a few epithelial cells of moribund larvae of R. philippinarum in France (Renault et al. 2001a). In Alaska, adult P. staminea had Cowdry Type A intranuclear inclusion bodies within digestive gland epithelial cells (Meyers et al. 2009, Meyers and Burton 2009). In California, no histological abnormalities were found in commercially cultured R. philippinarum (Burge et al. 2011). In China, microscopic changes in diseased broodstock of A.  broughtonii included lysed connective tissue with cells showing nuclear chromatin margination and pyknosis, and dilation of the digestive gland tubules with some epithelial cells containing eosinophilic inclusion bodies (Bai et al. 2016)
  4. Not reported.
  5. Histopathology consisted of minimal digestive gland tubules (=diverticular) lesions, similar to those reported as part of the normal cycle of degeneration and renewal of diverticular epithelium in P. ventricosum (Hine and Westney 1997). In C. edule, infection was characterised by the occurrence of large foci of heavy haemocytic infiltration in different organs (Carballal et al. 2003). Carballal et al. (2003) indicated that histological sections of the haemocyte foci stained with methyl green-pyronin showed red deposits and had strong positive staining with lead citrate, both characteristic of RNA reactions and suggesting the presence of RNA viruses. The infection in R. decussatus was not reported from samples examined by routine histology (Novoa and Figueras 2000). In R. philippinarum, histological lesions consisted of haemocyte infiltration mainly associated with areas surrounding the digestive gland where hypertrophied cells with no nuclear changes were primarily observed in the connective tissues and striated muscle fibers (Bateman et al. 2012).

Electron microscopy

  1. Icosahedral (6- and 5-sided) non-enveloped virons, 40 to 55 nm in diameter, in the nucleus of affected cells in M. arenaria (Farley 1976). The virus detected in R. philippinarum was the same shape and size with several similarities in cell specificity as described by Farley (1976) for the virus in M. arenaria (Montes et al. 2001). In E. arcuatus, ultrastructural examination indicated the intranuclear position of the basophilic inclusions, the peripherally displaced chromatin and the presence of viral particles (38.27 ± 3.93 nm in diameter) inside the inclusions. The virions were unenveloped, with a rounded appearance suggesting icosahedral symmetry and both empty and full capsids were observed. Based on these characteristics, Ruiz et al. (2011) suggest similarities to the families Papillomaviridae and Polyomaviridae.
  2. Para-crystalline arrays of virus particles, of hexagonal profile and 50 to 60 nm in diameter, in the cytoplasm of cells of the digestive gland (Hill 1976). Meyers et al. (2009) and Meyers and Burton (2009) published transmission electron micrographs of a cytoplasmic arrays of Aquareovirus particles from P. generosa in cultured bluegill fry cells and negative stain of virus particles showing double capsid morphology.
  3. In R. philippinarum larvae from France, the virus appears to induce apoptosis characterised as nuclear changes of chromatin condensation to form dense crescent-shaped aggregates lining the nuclear membrane followed by nuclear collapse. Concurrently, the cell cytoplasm condenses and the cell rounds up but the morphology of the mitochondria and ribosomes is preserved. Nuclei of infected fibroblast-like cells and rarely haemocytes usually contain circular to polygonal empty capsids (82 ± 4 nm in diameter) and nucleocapsids (74 ± 4 nm in diameter). Extracellular viruses were usually enveloped (111 ± 5 nm in diameter) and a tail was rarely observed (Renault et al. 2001a, b). In P. staminea from Alaska, viral particles in the nucleus of digestive gland epithelial cells were circular or polygonal and approximately 83 nm in diameter with occasional empty capsids (Meyers et al. 2009, Meyers and Burton 2009). In broodstock of A. broughtonii from China, enveloped herpesvirus-like particles (intranuclear empty capsids, capsids with pleomorphic cores and nucleocapsids (109.92 ± 1.55 nm in diameter)) were found within the nucleus of connective tissue cells of the mantle of moribund clams. Also, enveloped extracellular viral particles (151.16 ± 1.24 nm in diameter) were frequently visualized in the intercellular space under the epithelial cells of the mantle (Bai et al. 2016). The sizes of these viral particles were slightly bigger than particles reported in oysters (Arzul et al. 2017).
  4. Virus-like particles in membrane-bound structures (1.0 to 1.5 µm in diameter) in the cytoplasm of necrotic gill cells. The unenveloped, hexagonal virus particles (average diameter of 62 nm) were uniform electron dense without cores (Lo et al. 1988). Meyers and Burton (2009) published a transmission electron micrograph of a cytoplasmic aggregate of hexagonal-shaped "aquabirna-like" virus particles from P. staminea cultured in bluegill fry cells. The intracellular virus particles were about 63 nm in diameter, but were slightly larger (70 nm) with no apparent envelope in negative staining preparations (Meyers et al. 2009).
  5. In P. ventricosum, the virus-like particles (22 to 36 nm in diameter) were arrayed along the outer membrane of the nucleus and dilated cisternae in the endoplasmic reticulum of digestive gland epithelial cells. After lysis of infected cells, large numbers of ovoid membranes remained bearing smaller virus-like particles from 20 to 24 nm in diameter (Hine and Wesney 1997). In C. edule, virus-like particles in paracrystalline arrays were seen within electron dense deposits in the cytoplasm of some haemocytes, phagocytosed host cells and in the phagocytic vacuoles. The unenveloped icosahedral virus-like particles were 19 to 21 nm in diameter. No virus-like particles were observed inside nuclei (Carballal et al. 2003). In R. decussatus, virus-like particles (unenveloped, icosahedrical-spherical in shape and 27 to 35 nm in diameter) were observed free in the cytoplasm of connective tissue cells that had enlarged nuclei with dispersed chromatin which sometimes condensed near the nuclear membrane (Novoa and Figueras 2000, Renault and Novoa 2004, Renault 2016). The cytoplasmic content of infected cells was reduced in comparison to uninfected cells and the replication of the viral particles occurred in the cytoplasm in association with the endoplasmic reticulum and cytoplasmic vesicles (Novoa and Figueras 2000). In R. philippinarum in France, the unenveloped virus-like particles exhibited an icosahedral structure (diameter of 25 to 35 nm) and were widespread in the tissues including the cytoplasm of muscle and epithelial cells and nucleoplasm of granulocytes (Dang et al. 2009). In England, the unenveloped and icosahedral-spherical virus-like particles (25 to 30 nm in diameter) appeared to be free within the cytoplasm or associated within cytoplasmic vesicles in affected cells of the connective tissue of the gills and surrounding the tubules in the digestive gland (Bateman et al. 2012, Renault 2016).

Molecular characteristics

  1. Not reported.
  2. Not reported.
  3. Renault et al. (2001b) and Renault and Arzul (2001) described polymerase chain (PCR) reaction procedures. Renault and Arzul (2001) determined that the primer pair that they described as C2/C6 appeared well adapted for oyster herpes-like virus (now known as OsHV-1) DNA detection because of processing ease and great sensitivity. This PCR assay was also confirmed to be a powerful technique for detecting viral DNA in various species of bivalve larvae (Arzul et al. 2001a, b). Burge et al. (2011) developed an OsHV-specific qPCR based on the A-region of the OsHV-1 genome to detect and quantify this virus in R. philippinarum and other bivalves from Tomales Bay, California, USA. Xia et al. (2015) and Bai et al. (2016) used quantitative PCR (adapted from published protocols) to detect OsHV-1 DNA in samples of moribund A. broughtonii and genome sequence analysis to identify new variants of OsHV-1. They determined that these variants were most closely related to Acute viral necrosis virus (AVNV) described from scallops. Bai et al. (2016) allocated the variants to a separate subclade of OsHV-1. Arzul et al. (2017) indicated that phylogenetic analysis of these virus variants identified 2 main phylogenetic groups which grouped with the reference type of OsHV-1 and AVNV.
  4. Suzuki et al. (1997) used a 2-step PCR to assay samples of S. constricta, and Suzuki and Nojima (1999) used reverse transcription (RT) PCR to assay samples of various shellfish with nested PCR performed on samples that tested negative by RT-PCR and identified the nucleotide sequence of 19 randomly chosen PCR products.
  5. Not reported.

Culture

  1. Not reported.
  2. The virus grew best in a bluegill fibroblast cell line but also produced cytopathic effect in Atlantic salmon embryo, fathead minnow and grunt fin cell lines. For details on culture procedures see Hill (1976). Meyers and Burton (2009) illustrated the unique cytopathic effect characterized by focal areas of cellular fusion (Syncytia) and cytoplasmic destruction creating a vacuolated or foamy appearance in the bluegill fry cell line.
  3. Not reported.
  4. The birnavirus was isolated from diseased clams using the tilapia ovary cell line (To-2) and also replicated in chinook salmon embryo (CHSE-214), rainbow trout gonad (RTG-2) and eel ovary (EO) cell lines at 20°C (Lo et al. 1988, Chou et al. 1994). The birnavirus isolated from S. constricta on CHSE-214 was weakly pathogenic to S. constricta when injected into the mid-gut and may have increased clam mortality after spawning (Suzuki et al. 1997). Meyers et al. (2009) reported that an Aquabirnavirus was isolated and cultured from asymptomatic adult P. staminae in at least 7 fish cell lines but not in epithelioma papulosum cyprini cells. Suzuki and Nojima (1999) isolated marine birnivirus from R. philippinarum, A. subcrenata and A. g. bisenensis on cultured cells from the kidney of red sea bream (RSBK-2). McGladdery (2011) reported that the birnavirus-like virus from the digestive gland of M. tenuis was isolated on bluegill fibroblast cell lines.
  5. Not reported.

Methods of control

Control and management of viral diseases in molluscs mainly involves active surveillance, implementation of effective biosecurity protocols and other innovations such as mollusc breeding programs targeting production of resistant animals (Arzul et al. 2017). Although these strategies were clearly explained by Arzul et al. (2017), no examples were presented that specifically address viral diseases of clams and cockles. Potential interspecies transmission (between larvae of R. philippinarum, Crassostrea gigas, and Ostrea edulis) of OsHV-1 within a commercial hatchery indicates that precautions should be taken to avoid the spread of the virus between batches of bivalve larvae (Renault et al. 2001a, b; Arzul et al. 2001b). Arzul et al. (2017) suggested that viruses may be attached or even may infect planktonic organisms. However, herpesviruses are assumed to be fragile outside their hosts. The transfer through planktonic organisms might thus protect viruses during their life outside their mollusc hosts (Arzul et al. 2017).

References

Arzul, I., T. Renault and C. Lipart. 2001a. Experimental herpes-like viral infections in marine bivalves: demonstration of interspecies transmission. Diseases of Aquatic Organisms 46: 1-6.

Arzul, I., T. Renault, C. Lipart and A.J. Davison. 2001b. Evidence for interspecies transmission of oyster herpesvirus in marine bivalves. Journal of General Virology 82: 865-870.

Arzul, I., S. Corbeil, B. Morga and T. Renault. 2017. Viruses infecting marine molluscs. Journal of Invertebrate Pathology 147: 118-135.

Bai, C., C. Wang, J. Xia, H. Sun, S. Zhang and J. Huang. 2015. Emerging and endemic types of Ostreid herpesvirus 1 were detected in bivalves in China. Journal of Invertebrate Pathology 124: 98-106.

Bai, C., W. Gao, C. Wang, T. Yu, T. Zhang, Z. Qiu, Q. Wang and J. Huang. 2016. Identification and characterization of ostreid herpesvirus 1 associated with massive mortalities of Scapharca broughtonii broodstocks in China. Diseases of Aquatic Organisms 118: 65-75.

Bai, C.-M., Q.-C. Wang, B. Morga, J. Shi and C.-M. Wang. 2017. Experimental infection of adult Scapharca broughtonii with Ostreid herpesvirus SB strain. Journal of Invertebrate Pathology 143: 79-82.

Bateman, K.S., P. White and M. Longshaw. 2012. Virus-like particles associated with mortalities of the Manila clam Ruditapes philippinarum in England. Diseases of Aquatic Organisms 99: 163-167.

Burge, C.A., R.E. Strenge and C.S. Friedman. 2011. Detection of the oyster herpesvirus in commercial bivalves in northern California, USA: conventional and quantitative PCR. Diseases of Aquatic Organisms 94: 107-116.

Carballal, M.J., A. Villalba, D. Iglesias and P.M. Hine. 2003. Virus-like particles associated with large foci of heavy hemocytic infiltration in cockles Cerastoderma edule from Galicia (NW Spain). Journal of Invertebrate Pathology 84: 234-237.

Crane, M.S.J., K.A. McColl, J.A. Cowley, K. Ellard, K.W. Savin, S. Corbeil, N.J.G. Moody, M. Fegan and S. Warner. 2016. Abalone herpesvirus, In: Liu, D. (ed.) Molecular Detection of Animal Viral Pathogens. CRC Press, pp. 807-815.

Chou, H.Y., H.J. Li and C.F. Lo. 1994. Pathogenicity of a birnavirus to hard clam (Meretrix lusoria) and effect of temperature stress on its virulence. Fish Pathology (Tokyo) 29: 171-175.

Chou, H.-Y., S.-J. Chang, H.-Y. Lee and Y.-C. Chiou. 1998. Preliminary evidence for the effect of heavy metal cations on the susceptibility of hard clam (Meretrix lusoria) to clam birnavirus infection. Fish Pathology 33: 213-219.

Dang, C., P. Gonzalez, N. Mesmer-Dudons, J.-R. Bonami, N. Caill-Milly and X. de Montaudouin. 2009. Virus-like particles associated with brown muscle disease in Manila clam, Ruditapes philippinarum, in Arcachon Bay (France). Journal of Fish Diseases 32: 577-584.

Elston, R. 1997. Special topic review: bivalve mollusc viruses. World Journal of Microbiology and Biotechnology 13: 393-403.

Evans, O., I. Paul-Pont and R.J. Whittington. 2017. Detection of ostreid herpesvirus 1 microvariant DNA in aquatic invertebrate species, sediment and other samples collected from the Georges River estuary, New South Wales, Australia. Diseases of Aquatic Organisms 122: 247-255.

Farley, C.A. 1976. Proliferative disorders in bivalve mollusks. Marine Fisheries Review 38 (10): 30-33.

Farley, C.A. 1978. Viruses and viruslike lesions in marine molluscs. Marine Fisheries Review 40 (10): 18-20.

Guo, X. and S.E. Ford. 2016. Infectious diseases of marine molluscs and host responses as revealed by genomic tools. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150206.

Harshbarger, J.C., S.V. Otto and S.C. Chang 1977 (1979). Proliferative disorders in Crassostrea virginica and Mya arenaria from the Chesapeake Bay and intranuclear virus-like inclusions in Mya arenaria with germinomas from a Maine oil spill site. Haliotis 8: 243-248.

Hill, B.J. 1976. Properties of a virus isolated from the bivalve mollusc Tellina tenuis (da Costa). In: Page, L.A. (ed.), Wildlife Diseases. Plenum Press, New York and London, pp. 445-452.

Hine, P.M. and B. Wesney. 1997. Virus-like particles associated with cytopathology in the digestive gland epithelium of scallops Pecten novaezelandiae and toheroa Paphies ventricosum. Diseases of Aquatic Organisms 29: 197-204.

Kitamura, S.-I., S.J. Jung and S. Suzuki. 2000. Seasonal change of infective state of marine birnavirus in Japanese pearl oyster Pincada fucata. Archives of Virology 145: 2003-2014.

Koonin, E.V., V.V. Dolja, M. Krupovic, A. Varsani, Y.I. Wolf, N. Yutin, M. Zerbini and J.H. Kuhn. 2019. "Create a megataxonomic framework, filling all principal taxonomic ranks, for ssDNA viruses" (docx). International Committee on Taxonomy of Viruses. Retrieved 2 July 2020. Reference from Wikipedia accessed September 2022.

Lo, C.F., Y.W. Hong, S.Y. Huang and C.H. Wang. 1988. The characteristics of the virus isolated from the gill of clam Meretrix lusoria. Fish Pathology (Tokyo) 23: 147-154.

López, C., S. Darriba, D. Iglesias, M. Ruiz and R. Rodríguez. 2011. Chapter 7. Pathology of sword razor shell (Ensis arcuatus) and grooved razor shell (Solen marginatus), In: Guerra, A., C. Lodeiros, M. Gaspar, F. da Costa (eds.) Razor clams: Biology, Aquaculture and Fisheries. Xunta de Galicia, Consellería do Mar., pp. 131-168.

López, C., S. Darriba and J.I. Navas. 2012. Clam symbionts, In: da Costa González, F. (ed.) Clam Fisheries and Aquaculture. Nova Sciences Publishers, Inc., New York, pp. 107-148.

McGladdery, S.E. 2011. Shellfish diseases (viral, bacterial and fungal), In: Woo, P.T.K., D.W. Bruno (eds.) Fish diseases and disorders. Volume 3: viral bacterial and fungal infections. CABI, pp. 748-854.

Meyers, T. and T. Burton. 2009. Diseases of wild and cultured shellfish in Alaska. Fish Pathology Laboratories, Alaska Department of Fish and Game, Anchorage, Alaska, USA.

Meyers, T.R., T. Burton, W. Evans and N. Starkey. 2009. Detection of viruses and virus-like particles in four species of wild and farmed bivalve molluscs in Alaska, USA, from 1987 to 2009. Diseases of Aquatic Organisms 88: 1-12.

Montes, J.F., M. Durfort and J. García-Valero. 2001. Parasitism by the protozoan Perkinsus atlanticus favours the development of opportunistic infections. Diseases of Aquatic Organisms 46: 57–66.

Novoa, B. and A. Figueras. 2000. Virus-like particles associated with mortalities of the carpet-shell clam Ruditapes decussatus. Diseases of Aquatic Organisms 39: 147-149.

Novoa, B., A. Romero, Á.L. Álvarez, R. Moreira, P. Pereiro, M.M. Costa, S. Dios, A. Estepa, F. Parra and A. Figueras. 2016. Antiviral activity of myticin C peptide from mussel: an ancient defense against herpesviruses. Journal of Virology 90: 7692-7702.

Renault, T. 2008. Shellfish viruses. In: Mahy, B.W.J., M.H.V.V. Regenmortel (eds.) Encyclopedia of Virology (Third Edition). Academic Press, Oxford, pp. 560-567.

Renault, T. 2016. Chapter 39. Picornalike viruses of mollusks. In: Kibenge, F.S.B., M.G. Godoy (eds.) Aquaculture Virology. Academic Press, San Diego, pp. 529-531.

Renault, T. 2021. Chapter 8. Viruses infecting marine mollusks. In: Hurst, J.C. (ed.) Studies in Viral Ecology, second edition. Wiley Online Library, pp. 275-303.

Renault, T. and I. Arzul. 2001. Herpes-like virus infections in hatchery-reared bivalve larvae in Europe: specific viral DNA detection by PCR. Journal of Fish Diseases 24: 161-167.

Renault, T. and B. Novoa. 2004. Viruses infecting bivalve molluscs. Aquatic Living Resources 17: 397-409.

Renault, T., C. Lipart and I. Arzul. 2001a. A herpes-like virus infects a non-ostreid bivalve species: virus replication in Ruditapes philippinarum larvae. Diseases of Aquatic Organisms 45: 1-7.

Renault, T., C. Lipart and I. Arzul. 2001b. A herpes-like virus infecting Crassostrea gigas and Ruditapes philippinarum larvae in France. Journal of Fish Diseases 24: 369-376.

Ruiz, M., S. Darriba, R. Rodríguez, D. Iglesias, R. Lee and C. López. 2011. Viral basophilic inclusions in the digestive gland of razor clams Ensis arcuatus (Pharidae) in Galicia (NW Spain). Diseases of Aquatic Organisms 94: 239-241.

Shen, H., X.-h. Wan, P.-m. He, G.-x. Yao and A.-h. Chen. 2016. Purification and ultrastructure of a spherical virus in the cultured hard clam Meretrix meretrix Linnaeus. Marine Sciences 40: 46-53.

Suzuki, S. and M. Nojima. 1999. Detection of a marine birnavirus in wild molluscan shellfish species from Japan. Fish Pathology 34: 121-125.

Suzuki, S., T. Nakata, M. Kamakura, M. Yoshimoto, Y. Furukawa, Y. Yamashita and R. Kusuda. 1997. Isolation of birnavirus from Agemaki (jack knife clam) Sinonovacura constricta and survey of the virus using PCR technique. Fisheries Science 63: 563-566.

Xia, J., C. Bai, C. Wang, X. Song and J. Huang. 2015. Complete genome sequence of Ostreid herpesvirus-1 associated with mortalities of Scapharca broughtonii broodstocks. Virology Journal 12: 110, 9 pp.

Citation Information

Bower, S.M. (2022): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Virus Infection of Clams.

Date last revised: September 2022
Comments to Susan Bower

Date modified: