Marteilia refringens/maurini of Mussels
Category 1 (Not Reported in Canada)
Common, generally accepted names of the organism or disease agent
Marteiliasis of mussels.
Scientific name or taxonomic affiliation
Marteilia refringens and Marteilia maurini, in the phylum Paramyxea (Berthe et al. 2000). Unfortunately no morphological features are available to differentiate between M. refringens and M. maurini. However, Le Roux et al. (2001) identified genetic dimorphism in the internal transcribed spacer region of the ribosomal RNA genes and the apparent link of the two genetic types to host species, indicating that two species of Marteilia existed in Europe; M. refringens in oysters (O. edulis) and M. maurini in mussels (M. edulis and M. galloprovincialis). Nevertheless, co-infections of oysters and mussels by both genetic types occurred but were rare in some areas (Tige and Rabouin 1976, Le Roux et al. 2001) and common in others (Balseiro et al. 2007). From the results of molecular assays, López-Flores et al. (2004) and Balseiro et al. (2004) suggested that the Marteilia from oysters and mussels may be two different strains of the same species that appear to readily infect both hosts. The pathogenicity of each of the two species (if indeed both species are valid) is also unclear (Berthe et al. 2004). Balseiro et al. (2007) indicated that more research is required (e.g., into the molecular identity of new genes especially the coding genes, the relationship between the parasite and its different hosts, ecological studies to complete the life cycle, etc.) before the synonymy of the two species can be confirmed. The World Organisation for Animal Health (Office international des épizooties, OIE) Reference Laboratory for Infection with Marteilia refringens recognises two types of Marteilia refringens, types O and M (for oysters and mussels, respectively) as defined by Le Roux et al. (2001) (OIE 2009).
Atlantic coast of Europe from southern United Kingdom to Portugal, Mediterranean Sea including the northern Adriatic Sea, Persian Gulf and the Gulf of Thermaikos in northern Greece; and maybe the east coast of Florida in the scallop Argopecten gibbus (possibly another marteiliad).
Mytilus edulis, and Mytilus galloprovincialis, as well as oysters, possibly clams and cockles, scallops and other bivalves (Berthe et al. 2004). Recently reported in the black pigmy mussel, Xenostrobus securis, a non-indigenous invasive species in the Ria de Vigo, Galicia, Spain where it cohabits with infected M. galloprovincialis (Pascual et al. 2010). Unpublished report in the horse mussel Modiolus modiolus (see Auffret and Poder 1983).
Impact on the host
This parasite is considered to be a potentially lethal pathogen. Mussels are usually not adversely affected by marteilioisis. However, in some areas, mortality attributed to this parasite is significant for the mussel farming industry. Berth (2002) indicated that mussels (M. edulis and M. galloprovincialis) from enzootic areas were susceptible to infection but not affected by (tolerant to) M. maurini, but naive M. edulis originating from an area free of Marteilia spp. experienced mass mortalities when transferred to the enzootic area. For example, mussel mortalities (up to 100%) associated with heavy infection by Marteilia maurini were reported in the past in France in Mytilus edulis bought in from Northern European countries for relaying in France. These mussels had no previous contact with M. refringens or M. maurini and were possibly highly susceptibility to the disease (Arzul and Joly 2011). Also, Fuentes et al. (2002) reported that hybrid crosses between M. edulis and M. galloprovincialis were more heavily parasitised than three M. galloprovincialis stocks cultured for one year under a commercial raft in northwest Spain. The average prevalence of infection in M. galloprovincialis from five rías in Galicia, NW Spain ranged up to 35% between 1985 and 1989 (Figueras et al. 1991, Villalba et al. 1997).
Figueras et al. (1991), Villalba et al. (1997) and Rayyan et al. (2006) noted that infection of M. refringens/maurini in mussels was associated with haemocyte infiltration of the digestive gland (connective tissue and epithelia) and extensive destruction of the digestive gland occurred in heavy infections. Pathologic disruption of the digestive gland tubule epithelia was most severe at the time of spore release from the sporangia. Heavy infections also caused reduction of absorption efficiency resulting in an inhibition of gonad and storage tissue development and thus a significant loss in condition of infected mussels (Robledo et al. 1995a). Infected M. galloprovincialis also had lower total carbohydrate concentrations in the haemolymph (Robledo et al. 1995a) and a significant increase in circulating haemocytes, especially hyalinocytes, (Carballal et al.1998) than uninfected mussels . The infection usually triggers a haemocytic reaction that may slow or even stop the infection at times. Association between mussel mortality and this parasite has been suggested (Villalba et al. 1993).
The complete life cycle of Marteilia refringens/maurini has not been fully described. Although Comps and Joly (1980) were able to infect mussels (Mytilus galloprovincialis) with M. refringens extracted from oysters (Ostrea edulis), Berthe et al. (1998, 2004) supported the hypothesis that intermediate or alternate hosts (unknown) or free-living stages (also unknown) were essential in the life cycle of this parasite. Research into potential intermediate hosts in French shallow-water oyster ponds (‘claires’), where species diversity is relatively limited, detected M. refringens DNA in various invertebrates with the most promising possibility being the Calanoida copepod Acartia (=Paracartia) grani (Audemard et al. 2001, 2002). Although A. grani could be infected with M. refringens/maurini from both oysters (O. edulis) and (M. galloprovincialis), attempts to transmit M. refringens from A. grani to O. edulis and mussels (Mytilus edulis) were unsuccessful (Audemard et al. 2002, Carrasco et al. 2008a). Also, Carrasco et al. (2008a) reported that the infection patterns of M. refringens/maurini in A. grani were different for copepods infected via M. galloprovincialis or via O. edulis with only early stages of infection found in the intestinal tract of A. grani infected from mussels compared to higher prevalence and intensity of infections in the intestinal tract and gonad of A. grani infected from oysters. Subsequently, Carrasco et al. (2007a and b, 2008b) detected M. refringens DNA in other copepods (3 Calanoida, Acartia discaudata, A. clausi and A. italica; 1 Cyclopoida, Oithona sp.; and at least 1 Harpacticoida, Euterpina acutifrons and an unidentified Harpaticoida species) and in larval stages of decapod crustaceans (zoea larvae of Brachyura, probably Portumnus sp.) from the natural bays of the Ebro (Ebre) Delta (NW Mediterranean Sea, Spain) where mussels are the predominate farmed mollusc. The involvement of these organisms in the life cycle of M. refringens/maurini remains unknown.
The developmental stages of Marteilia spp. in bivalves were described by Grizel et al. (1974), Perkins (1976), and Kleeman et al. (2002a), and summarized by Bower (2006) as follows. Infections by all Marteilia spp. are presumably initiated by a primary cell or stem cell (5 to 8 μm in diameter) in the epithelial cells of the gut or gills. Carrasco et al. (2008c) detected initial (early) infections in the gill and mantle epithelium of M. galloprovincialis using the in situ hybridisation technique. The primary uninucleate cell develops a secondary uninucleate daughter cell in a vacuole within its cytoplasm. The daughter cell divides by binary fission to produce four daughter cells within the enlarged primary (stem) cell and within each daughter cell a uninucleate cell develops by internal cleavage. The primary cell degenerates to release the daughter cells, which become new primary cells. In the gut, the parasite penetrates the basal membrane of the digestive gland tubules and becomes established as nurse cells at the base of the epithelial cells. Nurse cells containing daughter cells proliferated and eventually degraded. Daughter cells in the digestive gland tubules become sporangiosori called “primary cells” by Perkins and Wolf (1976) and pansporoblasts by Mialhe et al. (1985). Sporulation occurs within the sporangiosorus via a unique process of internal cleavages (endosporulation) to produce cells within cells (Fig. 1). At the initiation of sporulation, uninucleate segments become delimited within the cytoplasm of the sporangiosorus to form the sporangial primordia (secondary cells). Eventually, 8 to 16 sporangial primordia (each about 12 μm in diameter at maturity) form within the sporangiosorus that retains its nucleus and enlarges to about 30 μm in diameter. Each sporangial primordium matures into a sporont containing 2 to 4 spore primordia (tertiary cells) that mature into spores (Fig. 1). Each spore contains 3 uninucleate sporoplasms of graded sizes, with each of the smaller sporoplasms being enclosed within the cytoplasm of the next largest one (i.e., consecutive internal cleavage of two sporoplasms within the spore primordium) (Perkins, 1976). A continuous spore wall with no operculum occurs around each spheroid mature spore that measures 3.5 to 4.5 μm in diameter. As the spore matures, light refractile inclusion bodies appear in the sporont cytoplasm surrounding the spores. The specific name of M. refringens was derived from these 'refringent' inclusion bodies. Mature spores are shed into the tubule lumen for evacuation from the mussel and infected mussels may shed large numbers of spores before death.
Gross Observations: Clinical signs include dead or gaping molluscs (2 or more years old), especially when temperature is at a maximum for mussels (Carrasco et al. 2007b, OIE 2009). Reduced growth rate and inhibition of gonad development were reported for infected mussels (Villalba 1993). However, these clinical signs are not specific to infection with M. refringens/maurini and could be indicative of other infections (Berthe et al. 2004).
Wet mounts: In advanced infection, mature sporangia with refringent granules can be observed in wet mounts from gaping mussels, freshly dead mussels or faeces of live diseased mussels. Squash a piece of digestive gland or faeces from suspect mussels on a glass slide. Observations are then made at ×400 magnification and can potentially show refringent granules in mature sporangia. A positive result is the presence of large (20–30 μm) spherical bodies containing spherical thick walled structures (spores). In susceptible species, within the known geographic range of infection with M. refringens/maurini, a positive result is indicative of infection with this parasite. In other species, or outside the known geographic range of infection with M. refringens/maurini, a positive result is indicative of infection with a Marteilia species that needs to be confirmed by the OIE Reference Laboratory (OIE 2009).
Smears/Tissue Imprints: In advanced infection, parasites ranging in size up to 30–40 μm can be observed in digestive gland imprints from gaping mussels or freshly dead mussels. Prepare digestive gland imprints of suspect mussels by drying excised tissues on absorbent paper and make several imprints on a glass slide. Air-dried slides are then fixed in methanol or in absolute ethanol and stained using a commercially available blood-staining kit, in accordance with the manufacturer’s instructions (e.g., Hemacolor, Merck; Diff-QuiK, Baxter). After rinsing in tap water and drying, the slides are mounted with a cover-slip using an appropriate synthetic resin. Slides are observed first at ×200 magnification and then under oil immersion at ×1000 magnification. Note that because infections may be focal and because the early and late stages of infection targets different tissues, imprints might miss early and low levels of infection. A positive result is the observation of cells ranging in size up to 30–40 μm in diameter with basophilic cytoplasm, eosinophilic nucleus, pale halos around large, strongly stained (refringent) granules and, in larger cells, cell within cell arrangements may be evident (Grizel et al.1974, Berthe et al. 2000, Berthe et al. 2004, for colour image see Arzul and Joly 2011). In susceptible species, within the known geographic range of infection with M. refringens/maurini, a positive result is strongly indicative of infection with this parasite. In other species, or outside the known geographic range of infection with M. refringens/maurini, a positive result is indicative of infection with a Marteilia species that needs to be confirmed by the OIE Reference Laboratory (OIE 2009).
Histology: Various stages of the parasite (as described above) can be observed in the epithelial cells of the digestive gland ducts (basophilic stages, mainly nurse cells (plasmodia)) and the epithelial cells of the digestive tubules (acidophilic stages, mainly sporangiosori at various stages of development). Parasites in the primary and secondary digestive tubules are slightly smaller (mean 8.4 µm in diameter) than those in the major ducts and stomach (mean 9.9 µm in diameter with internal primary cells about 4.1 µm in longest axis). The sporangiosori, containing eight sporangial primordia (sporont), enlarge up to 19.6 µm in diameter and each sporangial primordia eventually contains 3-4 spores (mean 2.6 µm in diameter). Refringent granules appear during the course of sporulation and can range from deep orange to deep red in colour in tissues stained with haematoxylin and eosin stain.
Electron Microscopy: Only the outer sporoplasm of the spore contains haplosporosomes (130-400 × 130-200 nm). Comps et al. (1981) indicated that M. refringens could be differentiated from Marteilia maurini in Mytilus galloprovincialis by subtle differences in haplosporosome shape and the 'existance of a multimembraneous envelope next to the spore wall'. However, Auffret and Poder (1983) and Longshaw et al. (2001) concluded that these criteria are invalid. Haplosporosomes in mature Marteilia from oysters and mussels were similar in shape (sphaeroid and oblate), although those from mussels were marginally smaller in size, and spore wall morphology was found to vary depending on the state of maturity of the parasite. Nevertheless, ultrastructural criteria are not sufficient to discriminate between Marteilia refringens and M. maurini (Arzul and Joly 2011).
Isolation and Purification: Mialhe et al. (1985) described a procedure for the isolation and purification of Marteilia sp. from oysters and mussels by the application of density gradients to a homogenate of heavily infected digestive gland. Further details on the isolation of various developmental stages from the digestive gland of M. galloprovincialis are detailed by Robledo et al. (1995b).
Immunological Assay: Tiscar et al.(1993) prepared polyclonal antibodies to Marteilia sp. isolated from Mytilus galloprovincialis from southern Italy that was used to clearly mark the parasite by direct immunoperoxidase staining in smears of the digestive gland of infected mussels. Monoclonal antibodies from six clones obtained from mice (Balb/c) against Marteilia sp. from Mytilus edulis in Brittany, France were specific for Marteilia spp. and cross reacted with Marteilia refirngens from Mytilus galloprovincialis in Ria de Vigo, Spain. Four of the monoclonal antibodies reacted with the spore wall and two with the spore cytoplasm (Robledo et al. 1994a). These monoclonal antibodies were found to produce various results when used in different immunological tests (Pernas et al. 2000).
DNA Probes: The nucleotide sequence of the small subunit ribosomal RNA (SSU rDNA or 18S rDNA) gene was compared with that of various eukaryotic organisms and polymerase chain reaction (PCR) primers were designed (Le Roux et al. 1999). The specificity of the amplified fragment for Marteilia sp. was confirmed by Southern blotting with an oligoprobe. Berthe et al. (2000) reported that the SSU rDNA gene sequence of Marteilia sp. that they isolated from O. edulis and M. edulis collected in different location in France were identical. Therefore, the World Organisation for Animal Health recommends PCR primers that target the internal transcribed spacer 1 (ITS1) region described by Le Roux et al. (2001) to amplify M. refringens (OIE 2009). Balseiro et al. (2007) analysed the ITS1 region subjected to restriction fragment length polymorphism (RFLP) with the endonuclease HhaI of Marteilia spp. from oysters and mussels from various locations in Europe to support the synonymy of M. maurini with M. refringens. In addition to ITS1 region analysis, a nested PCR assay, that has been tested only with M. refringens from O. edulis from Huelva, SW Spain and M. galloprovincialis also from Huelva, SW Spain and two locations in NW Italy, was developed using primers targeting the rDNA intergene spacer (López-Flores et al. 2004). This assay was demonstrated to be more sensitive than ITS1 PCR assay but needs to be tested more thoroughly for specificity (OIE 2009). As infection may be focal and also because infection targets different tissues in the early and late stages, the sensitivity of PCR detection may be lower than the expected theoretical PCR performance. A nested PCR reaction was developed for the diagnosis of M. refringens in Mytilus galloprovincialis from Galicia, Spain (Pernas et al. 2001).Sequences that targete regions of the SSU rDNA, ITS1 and intergene spacer (IGS) are available in the public gene banks.
In situ hybridisation (ISH) protocols have been developed and published (Le Roux et al. 1999, Berthe et al. 2000). Probes that targets the SSU of the rRNA gene complex and have been validated against histology (Le Roux et al. 1999, Thébault et al. 2005) are recommended by the World Organisation for Animal Health (OIE 2009). However, the probe, named Smart 2, was shown to cross react with Marteilia sydneyi and Marteilioïdes chungmuensis (Kleeman et al. 2002b). Nevertheless, Zrnčić et al. (2001) used this probe to detect Marteillia sp. in Mytilus galloprovincialis in Croatia and Carrasco et al. (2008c) used it to detect the initial infective stages of M. refringens in M. galloprovincialis. In addition, an ISH assay was developed using a probe targeting the rDNA intergene spacer (IGS) (López-Flores 2008a, 2008b). This assay was demonstrated to be more specific than the SSU ISH assay but needs to be thoroughly validated. In situ hybridization can help to detect early infections which are more difficult to detect in traditional histological sections (Arzul and Joly 2011).
Analysis of segments of the small subunit ribosomal RNA genome in comparison with that of other eukaryotic organisms indicates that the phylum Paramyxea should continue to be recognized (Berthe et al. 2000). Le Roux et al. (2001) indicated that M. refringens and M. maurini are different species and developed a protocol of restriction fragment length polymorphism (RFLP) analysis applied to PCR products obtained using ITS1 primers that differentiates between Marteilia refringens and M. maurini. However, López-Flores et al. (2004) and Novoa et al. (2005) suggested that theses parasites were different strains of the same species.
Methods of control
Do not transfer mussels from areas known to be infected (currently or historically) to areas with no record of M. refringens/maurini. Mussels from areas where Ostrea edulis is known to carry Marteilia refringens should be treated with similar caution. Mussels from the inner part of two rías in Galicia, Spain, and those held at less depth (2 m rather than 5 m) in one ría had higher mean prevalence of infection. Thus, culture rafts located in the outer zones of the rías contribute to minimizing the impact of this parasite on the mussel culture industry in Galicia (Fuentes et al. 1995). In the Thermaikos Gulf, the prevalence of Marteilia sp. was significantly greater in mussels cultured on tables than on long-lines (Karagiannis and Angelidis 2007). Robledo et al. (1994b) suggested that the collection of mussel seed from areas free of Marteilia sp. may contribute to a reduction in the prevalence of the parasite in cultured stocks.
Arzul, I. and J.P. Joly. 2011. EURL (European Union Reference Laboratory) for Molluscs Diseases: Marteilia refringens. Web page hosted by Ifremer. URL: http://wwz.ifremer.fr/crlmollusc/Main-activities/Tutorials/Marteilia-refringens.
Audemard, C., A. Barnaud, C.M. Collins, F. Le Roux, P.-G. Sauriau, C. Coustau, P. Blachier and F.C.J. Berthe. 2001. Claire ponds as an experimental model for Marteilia refringens life-cycle studies: new perspectives. Journal of Experimental Marine Biology and Ecology 257: 87-108.
Audemard, C., F. Le Roux, A. Barnaud, C. Collins, B. Sautour, P.-G. Sauriau, X. De Montaudouin, C. Coustau, C. Combes and F. Berthe. 2002. Needle in a haystack: involvement of the copepod Paracartia grani in the life-cycle of the oyster pathogen Marteilia refringens. Parasitology 124: 315-323.
Auffret, M. and M. Poder. 1983 (1985). Recherches sur Marteilia maurini, parasite de Mytilus edulis sur les cotes de Bretagne nord. (Studies on Marteilia maurini, parasite of Mytilus edulis from the north coasts of Brittany). Revue des Travaux de l'Institut des Pêches Maritimes. 47: 105-109. (In French with English abstract).
Balseiro, P., A. Montes, G. Ceschia, C. Gestal, B. Novoa and A. Figueras. 2007. Molecular epizootiology of the European Marteilia spp., infecting mussels (Mytilus galloprovincialis and M. edulis) and oysters (Ostrea edulis): an update. Bulletin of the European Association of Fish Pathologists 27: 148-156.
Berthe, F.C.J. 2002. Pacem in terris pathogenibus bonae voluntatis: mollusc-pathogens relationships prospects. Bulletin of the European Association of Fish Pathologists 22: 52-57.
Berthe, F.C., M. Pernas, M. Zerabib, P. Haffner, A. Thébault and A.J. Figueras. 1998. Experimental transmission of Marteilia refringens with special consideration of its life cycle. Diseases of Aquatic Organisms 34: 135-144.
Berthe, F.C.J., F. Le Roux, E. Peyretaillade, P. Peyret, D. Rodriguez, M. Gouy and C.P. Vivarès. 2000. Phylogenetic analysis of the small subunit ribosomal RNA of Marteilia refringens validates the existence of Phylum Paramyxea (Desportes and Perkins, 1990). The Journal of Eukaryotic Microbiology 47: 288-293.
Berthe, F.C.J., F. Le Roux, R.D. Adlard and A. Figueras. 2004. Marteiliosis in molluscs: A review. Aquatic Living Resources 17: 433-448.
Bower, S.M. 1992. Diseases and parasites in mussels. In: E. Gosling (ed.) The Mussel Mytilus: Ecology, Physiology, Genetics and Culture. Elsevier Press, Amsterdam, p. 543-563.
Bower, S.M. 2006. Parasitic diseases of shellfish. In: Woo, P.T.K. (ed.) Fish Diseases and Disorders, Volume 1: Protozoa and Metazoan Infections, Second Edition, CABI, Wallingford. pp. 629-677.
Bower, S.M. and A.J. Figueras. 1989. Infectious diseases of mussels, especially pertaining to mussel transplantation. World Aquaculture 20(4): 89-93.
Carballal, M.J., A. Villalba and C. López. 1998. Seasonal variation and effects of age, food availability, size, gonad development, and parasitism on the hemogram of Mytilus edulis. Journal of Invertebrate Pathology 72: 304-312.
Carrasco, N., I. López-Flores, M. Alcaraz, M.D. Furones, F.C.J. Berthe and I. Arzul. 2007a. First record of a Marteilia parasite (Paramyxea) in zooplankton populations from a natural estuarine environment. Aquaculture 269: 63-70.
Carrasco, N., I. López-Flores, M. Alcaraz, M.D. Furones, F.C.J. Berthe and I. Arzul. 2007b. Dynamics of the parasite Marteilia refringens (Paramyxea) in Mytilus galloprovincialis and zooplankton populations in Alfacs Bay (Catalonia, Spain). Parasitology 134: 1541-1550.
Carrasco, N., I. Arzul, B. Chollet, M. Robert, J.P. Joly, M.D. Furones and F.C.J. Berthe. 2008a. Comparative experimental infection of the copepod Paracartia grani with Marteilia refringens and Marteilia maurini. Journal of Fish Diseases 31: 497-504.
Carrasco, N., I. Arzul, F.C.J. Berthe, M. Fernández-Tejedor, M. Durfort and M.D. Furones. 2008b. Delta de l'Ebre is a natural bay model for Marteilia spp. (Paramyxea) dynamics and life-cycle. Diseases of Aquatic Organisms 79: 65-73.
Carrasco, N., I. Arzul, F.C.J. Berthe and M.D. Furones. 2008c. In situ hybridization detection of initial infective stages of Marteilia refringens (Paramyxea) in its host Mytilus galloprovincialis. Journal of Fish Diseases 31: 153-157.
Comps, M., H. Grizel, G. Tig‚ and J.L. Duthoit. 1975. Parasites nouveaux de la glande digestive des mollusques marins Mytilus edulis L. et Cardium edule L. (New parasites in the digestive gland of Mytilus edulis L. and Cardium edule L.). Comptes Rendus Académie des Sciences de Paris, Série D 281: 179-181. (In French, for Open Access version see: http://archimer.ifremer.fr/doc/00000/5914/, for electronic version of publication see: http://archimer.ifremer.fr/doc/1975/publication-5914.PDF.
Comps, M. and J.P. Joly. 1980. Contamination expérimentale de Mytilus galloprovincialis Lmk par Marteilia refringens. Science et Pêche Bulletin d'Information et de Documentation de l'Institut Scientifique et Technique des Pêches Maritimes 301: 19-21. (In French).
Comps, M., H. Grizel, G. Tigé and J.-L. Duthoit. 1975. Parasites nouveaux de la glande digestive des mollusques marins Mytilus edulis L. et Cardium edule L. Comptes Rendus Hebdomadaire Séances de l'Academie Sciences, Paris (Ser.D.) 281: 179-181. (In French).
Comps, M., Y. Pichot and P. Papagianni. 1981. Research on Marteilia maurini n. sp. parasite of the mussel Mytilus galloprovincialis Lmk. Revue des Travaux de l'Institut des Pêches Maritimes 45: 211-214. (In French, with English summary).
Comps, M., H. Grizel and Y. Papayanni.1982. Infection parasitaire causée par Marteilia maurini sp. n. chez la moule Mytilus galloprovincialis. International Council for Exploration of the Sea C.M. 1982/F: 24: 3 pp.
Figueras, A.J. and J. Montes. 1988. Aber disease of edible oysters caused by Marteilia refringens. American Fisheries Society Special Publication 18: 38-46.
Figueras, A.J., C.F. Jardon and J.R. Caldas. 1991. Diseases and parasites of rafted mussels (Mytilus galloprovincialis Lmk): preliminary results. Aquaculture 99: 17-33.
Fuentes, J., A. Villalba, C. Zapata and G. Alvarez. 1995. Effects of stock and culture environment on infections by Marteilia refringens and Mytilicola intestinalis in the mussel Mytilus galloprovincialis cultured in Galicia (NW Spain). Diseases of Aquatic Organisms 21: 221-226.
Fuentes, J., J.L. López, E. Mosquera, J. Vázquez, A. Villalba and G. Alvarez. 2002. Growth, mortality, pathological conditions and protein expression of Mytilus edulis and M. galloprovincialis crosses cultured in the Ría de Arousa (NW of Spain). Aquaculture 213: 233-251.
Grizel, H., M. Comps, J.R. Bonami, F. Cousserans, J.L. Duthoit and M.A. LePennec. 1974. Research on the agent of digestive gland disease of Ostrea edulis Linné. Science et Pêche Bulletin d'Information et de Documentation de l'Institut Scientifique et Technique des Pêches Maritimes 240: 7-30. (In French).
Gutiérrez, M. 1977. Nota sobre marteiliasis en el mejillón, Mytilus edulis (L), de la costa Noroeste de España. Investigaciones pesquas 41: 637-642. (In Spanish).
Karagiannis, D. and P. Angelidis. 2007. Infection of cultured mussels Mytilus galloprovincialis by the protozoan Marteilia sp. in the Thermaikos Gulf (N Greece). Bulletin of the European Association of Fish Pathologists 27: 131-141.
Kleeman, S.N., R.D. Adlard and R.J.G. Lester. 2002a. Detection of the initial infective stages of the protozoan parasite Marteilia sydneyi in Saccostrea glomerata and their development through to sporogenesis. International Journal for Parasitology 32: 767-784.
Kleeman, S.N., F. Le Roux, F. Berthe and R.D. Adlard. 2002b. Specificity of PCR and in situ hybridization assays designed for detection of Marteilia sydneyi and M. refringens. Parasitology 125: 131-141.
Le Roux, F., C. Audemard, A. Barnaud and F. Berthe. 1999. DNA Probes as potential tools for the detection of Marteilia refringens. Marine Biotechnology 1: 588-597.
Le Roux, F., G. Lorenzo, P. Peyret, C. Audemard, A. Figueras, C. Vivarès, M. Gouy and F. Berthe. 2001. Molecular evidence for the existence of two species of Marteilia in Europe. The Journal of Eukaryotic Microbiology 48: 449-454.
Longshaw, M., S.W. Feist, R.A. Matthews and A. Figueras. 2001. Ultrastructural characterisation of Marteilia species (Paramyxea) from Ostrea edulis, Mytilus edulis and Mytilus galloprovincialis in Europe. Diseases of Aquatic Organisms 44: 137-142.
López-Flores, I., R. de la Herrán, M.A. Garrido-Ramos, J.I. Navas and M. Ruiz Rejón. 2004. The molecular diagnosis of Marteilia refringens and differentiation between Marteilia strains infecting oysters and mussels based on the rDNA IGS sequence. Parasitology 129: 411-419.
López-Flores, I., M.A. Garrido-Ramos, R. de la Herran, C. Ruiz-Rejón, M. Ruiz-Rejón and J.I. Navas. 2008a. Identification of Marteilia refringens infecting the razor clam Solen marginatus by PCR and in situ hybridization. Molecular and Cellular Probes 22: 151-155.
López-Flores, I., F. Robles, J.M. Valencia, A. Grau, A. Villalba, R. de la Herrán, M.A. Garrido-Ramos, C. Ruiz-Rejón, M. Ruiz-Rejón and J.I. Navas. 2008b. Detection of Marteilia refringens using nested PCR and in situ hybridisation in Chamelea gallina from the Balearic Islands (Spain). Diseases of Aquatic Organisms 82: 79-87.
Mialhe, E., E. Bachère, C. LeBec and H. Grizel. 1985. Isolement et purification de Marteilia (Protozoa: Ascetospora) parasites de bivalves marins. (Isolation and purification of Marteilia (Protozoa: Ascetospora) parasites of marine Bivalvia: ultrastructural study of pansporoblasts.). Compte Rendu Hebdomadaire des Séances de l'Académie des Sciences, Paris. Série III 301: 137-142. (In French, with English summary).
Mortensen, S., I. Arzul, L. Miossec, C. Paillard, S. Feist, G. Stentiford, T. Renault, D. Saulnier and A. Gregory. 2007. Molluscs and crustaceans. In: Raynard, R., T. Wahli, I. Vatsos, S. Mortensen (eds.) Review of disease interactions and pathogen exchange between farmed and wild finfish and shellfish in Europe. VESO on behalf of DIPNET, Oslo. Chapter 5.3.15, pp. 375-380. For electronic version see www.dipnet.info under "Documents" subgroup "Reports and project deliverables".
Novoa, B., D. Posada and A. Figueras. 2005. Polymorphisms in the sequences of Marteilia internal transcribed spacer region of the ribosomal RNA genes (ITS-1) in Spain: genetic types are not related with bivalve hosts. Journal of Fish Diseases 28: 331-338.
OIE. 2009. Manual of Diagnostic Tests for Aquatic Animals 2009. Chapter 2.4.4. — Infection with Marteilia refringens. There is an OIE (World Organisation for Animal Health) Reference Laboratory for Infection with Marteilia refringens (consult the OIE Web site for the most up-to-date list: www.oie.int).
Pascual, S., A. Villalba, E. Abollo, M. Garci, A.F. González, M. Nombela, D. Posada and A. Guerra. 2010. The mussel Xenostrobus securis: a well-established alien invader in the Ria de Vigo (Spain, NE Atlantic). Biological Invasions 12: 2091-2103.
Pérez Camacho, A., A. Villalba, R. Beiras and U. Labarta. 1997. Absorption efficiency and condition of cultured mussels (Mytilus edulis galloprovincialis Linnaeus) of Galicia (NW Spain) infected by parasites Marteilia refringens Grizel et al. and Mytilicola intestinalis Steuer. Journal of Shellfish Research 16: 77-82.
Perkins, F.O. 1976. Ultrastructure of sporulation in the European flat oyster pathogen, Marteilia refringens - taxonomic implications. Journal of Protozoology 23: 64-74.
Pernas, M., B. Novoa, C. Tafalla and A. Figueras. 2000. Efficiency of different monoclonal antibodies in immunological assays developed for the detection of Marteilia sp. isolated from Mytilus galloprovincialis. Bulletin of the European Association of Fish Pathologists 20: 193-198.
Pernas, M., B. Novoa, F. Berthe, C. Tafalla and A. Figueras. 2001. Molecular methods for the diagnosis of Marteilia refringens. Bulletin of the European Association of Fish Pathologists 21: 200-208.
Rayyan, A., P. Damianidis, C. Antoniadou and C.C. Chintiroglou. 2006. Protozoan parasites in cultured mussels Mytilus galloprovincialis in the Thermaikos Gulf (north Aegean Sea, Greece). Diseases of Aquatic Organisms 70: 251-254.
Robledo, J.A.F. and A. Figueras. 1995. The effect of culture-site, depth, season, and stock source on the prevalence of Marteilia refringens in cultured mussels (Mytilus galloprovincialis Lmk.) from Galicia, Spain. The Journal of Parasitology 81: 354-363.
Robledo, J.A.F., V. Boulo, E. Mialhe, B. Desprès and A. Figueras. 1994a. Monoclonal antibodies against sporangia and spores of Marteilia sp. (Protozoa: Ascetospora). Diseases of Aquatic Organisms 18: 211-216.
Robledo, J.A.F., J. Cáceres-Martínez and A. Figueras. 1994b. Marteilia refringens in mussel (Mytilus galloprovincialis Lmk.) beds in Spain. Bulletin of the European Association of Fish Pathologists 14: 61-63.
Robledo, J.A.F., M.M. Santarém, P. González and A. Figueras. 1995a. Seasonal variations in the biochemical composition of the serum of Mytilus galloprovincialis Lmk. and its relationship to the reproductive cycle and parasitic load. Aquaculture 133: 311-322.
Robledo, J.A.F., E. Mialhe and A. Figueras. 1995b. Purification of several phases of the parasite Marteilia (Protozoa: Ascetospora) from mussels (Mytilus edulis). In: Stolen, J.S., T.C. Fletcher, S.A. Smith, J.T. Zelikoff, S.L. Kaattari, R.S. Anderson, K. Söderhäll, B.A. Weeks-Perkins (eds.). Techniques in Fish Immunology, Immunology and Pathology of Aquatic Invertebrates, Vol. 4 Fish Immunology Technical Communications. SOS Publications, Fair Haven. pp. 117-121.
Tige, G. and M.A. Rabouin. 1976. Étude d'un lot de moules transférées dans un centre touché par l'épizootie affectant l'huître plate. International Council for Exploration of the Sea C.M.1976/K:21: 10 pp. (In French with English abstract).
Tiscar, P.G., M. Tempesta and M. Compagnucci. 1993. Peroxidase conjugated polyclonal antibody against Marteilia sp. purified from infected mussels (Mytilus galloprovincialis, Lmk) cultivated in Apulia, southern Italy. Bulletin of the European Association of Fish Pathologists 13: 53-55.
Villalba, A., S.G. Mourelle, M.C. López, M.J. Carballal and C. Azevedo. 1993. Marteiliasis affecting cultured mussels Mytilus galloprovincialis of Galicia (NW Spain). I. Etiology, phases of the infection, and temporal and spatial variability in prevalence. Diseases of Aquatic Organisms 16: 61-72.
Villalba, A., S.G. Mourelle, M.J. Carballal and M.C. López. 1993. Effects of infection by the protistan parasite Marteilia refringens on the reproduction of cultured mussels Mytilus galloprovincialis in Galicia (NW Spain). Diseases of Aquatic Organisms 17: 205-213.
Villalba, A., S.G. Mourelle, M.J. Carballal and C. López. 1997. Symbionts and diseases of farmed mussels Mytilus galloprovincialis throughout the culture process in the Rías of Galicia (NW Spain). Diseases of Aquatic Organisms 31: 127-139.
Virvilis, C., P. Angelidis and G. Photis. 2003. Presence of the parasite Marteilia sp. in the shellfish of the Thermaikos Gulf in northern Greece. Bulletin of the European Association of Fish Pathologists 23: 157-161.
Zrnčić, S., F. Le Roux, D. Oraić, B. Šoštarić and F.C.J. Berthe. 2001. First record of Marteillia sp. in mussels Mytilus galloprovincialis in Croatia. Diseases of Aquatic Organisms 44: 143-148.
Bower, S.M. (2011): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Marteilia refringens/maurini of Mussels.
Date last revised: July 2011
Comments to Susan Bower
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