Marteiliosis of Clams and Cockles

Category

Category 1 (Not Reported in Canada)

Common, generally accepted names of the organism or disease agent

Marteiliosis of clams.

Scientific name or taxonomic affiliation

Marteilia sp., in the phylum Paramyxea, have been reported from various species of clams and cockles in coastal waters of Europe and Asia. In some cases, molecular analysis was used to identify taxonomic affiliations with described species (i.e., Marteilia refrengins and Marteilia sydneyi). In other cases, nothing is know about the species identity (e.g., an unnamed species of Marteilia-like parasite in Tridacna maxima). In the following text, each reported geographic location and host species was assigned a letter code which is consistently applied to all information under each of the following headings.

Geographic distribution

  1. Iwakuni in Yamaguchi Prefecture, Japan (Itoh et al. 2005).
  2. Various locations along the coast of Brittany, France (Comps et al. 1975, Poder et al. 1983).
  3. North west (Galicia) and south west coasts of Spain (López and Darriba 2006, López-Flores et al. 2008a)
  4. Balearic Islands (López-Flores et al. 2008b) and Ebro Delta bays (Carrasco et al. 2011) in the Mediterranean regions of Spain.
  5. North east coast of Italy, Adriatic Sea (Berthe et al. 2004)

Host species

  1. Venerupis (=Tapes) philippinarum (Itoh et al. 2005).
  2. Cerastoderma (=Cardium) edule (Comps et al. 1975, Auffret and Poder 1987), Tapes pullastra, Tapes rhomboides (Poder et al. 1983, Auffret and Poder 1987).
  3. Solen marginatus (López and Darriba 2006, López-Flores et al. 2008a).
  4. Chamelea gallina (López-Flores et al. 2008b) and Cerastoderma edule (Carrasco et al. 2011, 2012).
  5. Ensis minor, Ensis siliqua (Berthe et al. 2004).

Impact on the host

  1. This parasite was detected for this first time in October 2003 in the epithelium of the digestive tubules in one of 40 clams experimentally deployed in April 2002 to investigate the drastic decrease in commercial V. philippinarum stocks in the area. No host reaction such as haemocyte infiltration or necrosis was observed in association with the infection (Itoh et al. 2005). Because other species of Marteilia are known to be pathogenic to their respective hosts, further investigations are required before the impact of this Marteilia sp. on Manila clams can be determined.
  2. The parasite was detected in cockles among moribund individual found on the surface of the substrate but only 2% of the examined specimens were infected (Comps et al. 1975). Auffret and Poder (1987) reported haemocyte infiltration and tissue necrosis around parasites or in intestinal tissues of parasitized bivalves.
  3. None reported.
  4. Marteilia refringens was detected in 3 of 69 C. gallina examined during a histopathological survey conducted to discover the cause of a mass mortality in this species of clam (López-Flores et al. 2008b). In C. edule, the prevalence of Marteilia sp. was significant (40% of 30 specimens most with high intensities of infection) and infection was potentially associated with a mortality event in the cockles (Carrasco et al. 2011).

Note that the developmental stages of these Marteilia are similar to that described for M. refringens. For details see the description provided in the Marteiliosis of oysters page and the schematic drawing that illustrates the stages.

Diagnostic techniques

Histology:

  1. Cross-sections of the digestive gland show the parasite in the epithelial cells of the digestive tubules. The unique feature of internal cleavage to produce cells within cells during sporulation differentiates Marteilia spp. from all other protista. Sporangiosori (plasmodia) were 16.8± 1.4 µm by 15.1 ± 1.3 µm (Itoh et al. 2005).
  2. Figure 1. Mature plasmodia (arrows) containing developing spores of Marteilia sp. in the digestive gland tubule epithelium of Venerupis philippinarum from Japan.

  3. The parasite resembled Marteilia refringens in histological sections (Comps et al. 1975, Poder et al. 1983).
  4. Early stages (or primary cells) of the parasite observed in the epithelial cells of the digestive ducts and tubules were eosinophilic, spherical or elongate in shape and uni- or multinucleated. More advanced developmental stages including sporangia were also observed in these tissues but were more abundant (López and Darriba 2006).
  5. Classical developmental stages of M. refringens were found only in the epithelium of the digestive diverticula of C. gallina (López-Flores et al. 2008b). Although developmental stages of the parasite in C. edule were similar to those of M. refringens in oysters and mussels, Carrasco et al. (2011) did not conclude that the parasite of infected cockles was M. refringens.

Electron Microscopy:

  1. The sporangiosorus (plasmodium) contained refringent granules, striated inclusions and endoplasmic reticulum. Usually four sporonts (secondary cells) were in each sporangiosorus and two spores were contained in each sporont. The spores had two larger cells and one of the cells included an inner cell suggesting that a spore consisted of three sporoplasms (Itoh et al. 2005). The occurrence of two spores in each sporont is a characteristic of Marteilia sydneyi but M. sydenyi usually has eight to sixteen sporonts in each sporangiosorus and not four as reported for this parasite.
  2. Figure 2. Plasmodia of Marteilia sp. containing developing spores from Venerupis philippinarum from Japan. RG, refringent granules; S, striated inclusions; C1, cytoplasm of sporangiosorus (plasmodium); C2, sporont (secondary cell); I, inclusion body; and ER, endoplasmic reticulum.

    Figure 3. Spore of Marteilia sp. from Venerupis philippinarum from Japan. Note the thickness of the spore wall, haplosporosomes (H), nuclei (N), cytoplasm of the spore (S), cytoplasm of the inner cell (SI), and the nucleus of the inner cell (NI).

  3. Not reported.
  4. The isolate from north west Spain had refringent bodies (0.58±0.11 µm in diameter, n=39) inside the presporangia (secondary cells) that were smaller then those described for M. refringens (2-6 µm in diameter). The presporangia delimited by two membranes contained the sporangial primordia (spore primordia or tertiary cells, 3.25±0.88 µm in diameter, n=15). The sporangial primordium matured into a sporont containing 6 spore primordia (tertiary cells, that mature into spores), unlike M. refringens which develops 2-4 sporonts per sporangial primordium. Mature spores (3.74±0.46 µm in diameter, n=44) had 3 uninuclate sporoplasms or protoplasts (outermost, intermediate, and innermost) one inside the other. A spore nucleus was in the innermost sporoplasm. The outermost sporoplasm contains several spherical haplosporosomes (95±28 nm in diameter, n=30) unlike the oblate haplosporosomes reported for M. refringens. The intermediate sporoplasm had flattened, vermiform, double membrane—limited vesicles (238±51 nm long and 61±9 nm wide, n=30) which were shorter and wider than those found in M. refringens. Spores were surrounded by a thickened wall (41.4±12.8 nm, n=30) (López and Darriba 2006).
  5. Not reported.

DNA Probes:

  1. Not reported
  2. Not reported
  3. The polymerase chain reaction (PCR) assay was used to amplify a fragment of the intergenic spacer of the ribosomal RNA (IGS rDNA) region of an isolate from the south west coasts of Spain. Analysis of the sequence of the resulting product indicated between 98.2 and 99.5 % identity with M. refringens nested within the clade containing parasite strains mainly isolated from mussels (López-Flores et al. 2008a). In situ hybridization (ISH) analysis showed tissue distribution and presence of different developmental stages of the parasite in the digestive diverticula epithelium, which suggested a true parasitism in these individuals (López-Flores et al. 2008a).
  4. Genomic DNA samples were extracted from tissues of C. gallina embedded in a paraffin block that had been prepared for histological examination of the clam. The polymerase chain reaction (PCR) assay was used to amplify a fragment of the intergenic spacer of the ribosomal RNA (IGS rDNA) region of the extract. Because the sample was extracted from paraffin with probable extensive DNA degradation and possible presence of PCR inhibitors, a combination of nested and short length PCR was used to overcome decreased efficiency of amplification by standard PCR. Analysis of the sequence of the resulting product had 99.1% identity with M. refringens isolated from O. edulis (López-Flores et al. 2008b). In situ hybridization (ISH) analysis confirmed the presence of the Marteilia sp. in the digestive gland tissues of C. gallina and C. edule (López-Flores et al. 2008b, Carrasco et al. 2011). Research into different regions of the ribosomal DNA cistron of the Marteilia sp. in C. edule indicated that it may be a new species because maximum identity with M. refringens when analyzed by BLAST was 83% for the partial IGS rDNA sequences, 86% for the partial internal transcribed spacer 1 (ITS-1) and 98% for the partial 18S rRNA regions studied (Carrasco et al. 2012). Also, comparison by multiple alignment of ITS-1 sequences, genetic distance matrix of the IGS rDNA, and a phylogenetic analysis using the IGS rDNA sequence supported the existence of a new Marteilia species infecting bivalves in Europe. Carrasco et al. (2012) described, an IGS rDNA polymerase chain reaction-restriction fragment length polymorphism (PCR–RFLP) digestion with the BgL II enzyme that should facilitate discrimination between the cockle Marteilia and M. refringens (types O and M, for oysters and mussels, respectively) infecting other bivalves in Europe.

Methods of control

There are no known methods of prevention or control. Infected clams should not be transported into areas known to be free of the disease.

References

Auffret, M. and M. Poder. 1987. Pathology of the main bivalve mollusc species from oyster rearing areas in Brittany (France). Aquaculture 67: 255-257.

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.

Carrasco, N., A. Roque, K.B. Andree, C. Rodgers, B. Lacuesta and M.D. Furones. 2011. A Marteilia parasite and digestive epithelial virosis lesions observed during a common edible cockle Cerastoderma edule mortality event in the Spanish Mediterranean coast. Aquaculture 321: 197-202.

Carrasco, N., K.B. Andree, B. Lacuesta, A. Roque, C. Rodgers and M.D. Furones. 2012. Molecular characterization of the Marteilia parasite infecting the common edible cockle Cerastoderma edule in the Spanish Mediterranean coast. A new Marteilia species affecting bivalves in Europe? Aquaculture 324-325: 20-26.

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).

Itoh, N., K. Momoyama and K. Ogawa. 2005. First report of three protozoan parasites (a haplosporidian, Marteilia sp. and Marteilioides sp.) from the Manila clam, Venerupis (=Ruditapes) philippinarum in Japan. Journal of Invertebrate Pathology 88: 201-206.

López, C. and S. Darriba. 2006. Presence of Marteilia sp. (Paramyxea) in the razor clam Solen marginatus (Pennántt, 1777) in Galicia (NW Spain). Journal of Invertebrate Pathology 92: 109-111.

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.

Poder, M., M. Auffret and G. Balouet. 1983. Etudes pathologiques et epidemiologiques des lesions parasitaires chez Ostrea edulis: Premiers resultats d'un recherche prospective comparative chez les principales especes de mollusques des zones ostreicoles de Bretagne nord. (Pathological and epidemiological studies of parasitic diseases of Ostrea edulis: First results from a retrospective and comparative research of main species of molluscs in oyster farm in North Brittany.). Bases biologiques de l'aquaculture, Montpellier, 12-16 decembre 1983, IFREMER. Actes de Colloques 1: 125-138. (In French, URL: http://archimer.ifremer.fr/doc/00000/1182/).

Citation Information

Bower, S.M., Itoh, N. (2012): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Marteiliosis of clams and cockles.

Contact information for co-author:

Naoki Itoh, Graduate School of Agricultural Science, Tohoku University, 1-1 Amamiya-machi, Tsutsumidori, Aoba-ku, Sendai 981-8555, Miyagi Japan. E-mail: nitoh@bios.tohoku.ac.jp

Date last revised: January 2012
Comments to Susan Bower

Date modified: