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메뉴The rate of marine pathogen spread is increasing because of the increase in ocean temperatures, transportation, ocean currents, and marine product trade worldwide. In Korean waters, several species of single-celled or metazoan pathogenic organisms have been identified that may hamper aquaculture or international trade of the Manila clam Ruditapes philippinarum. In this study, we reviewed the different types of pathogenic organisms isolated and reported from Manila clams worldwide. Among these pathogens, the diseases caused by two protozoan parasites, Perkinsus olseni and Marteilia refringens, are listed as OIE notifiable. P. olseni infection in Manila clam causes retarded growth and reproduction and mass mortality of the clam and has been reported in Korea, China, and Japan. M. refringens infection in Manila clams has been reported only once in China, although further information is unavailable. Trematode infections in the Manila clam often result in slow gonad maturation or gonad castration and may result in a decline in recruitment. The introduction of various invasive pathogens via the import of host organisms or discharge of ballast water of commercial shipping vessels may cause various ecological and evolutionary issues in the native ecosystem. Therefore, it is recommended to improve the quarantine methods of imported shellfishes and monitor the commercially important shellfish species in Korean waters to prevent the spread of exotic pathogenic organisms.
Azevedo, C. (1989) Fine structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) parasite of the clam Ruditapes decussatus from Portugal. Journal of Parasitology, 75(4): 627-35.
Azevedo, C. (2001) Ultrastructural description of the spore maturation stages of the clam parasite Minchinia tapetis (Vilela, 1951) (Haplosporida:Haplosporidiidae). Systematic Parasitology, 49:189-194.
Auzoux-Bordenave, S., Vigario, A.M., Ruano, F., Domart-Coulon, I. and Doumenc, D. (1995) In vitro sporulation of the clam pathogen Perkinsus atlanticus (Apicomplexa, Perkinsea) under various environmental conditions. Journal of Shellfish Research, 14: 469-475.
Binias, C., Gonzalez, P., Provost, M., Lambert, C. and de Montaudouin, X. (2014) Brown muscle disease:Impact on Manila clam Venerupis (= Ruditapes)philippinarum biology. Fish & Shellfish Immunology, 36: 510-518.
Bower, S.M., Blackbourn, J. and Meyer, G.R. (1992)Parasite and symbiont fauna of Japanese littlenecks, Tapes philippinarum (Adams and Reeve, 1850), in British Columbia. Journal of Shellfish Research, 11:13-19.
Bower, S.M. (2007) Synopsis of infectious diseases and parasites of commercially exploited shellfish:Haplosporidian infection of clams.
Cao, H. (1989) Life cycle of Proctoeces orientalis sp. nov. in marine bivalves. Acta Zoologica Sinica, 35(1):58-65.
CABI (2019) https://www.cabi.org/isc/datasheet/61697.
Chen, M. (1995) The parasitized location of larval Cercaria elegans Tang 1992 in Ruditapes philippinarum and its histochemistry. Chinese Science Abstracts Series, 2(B14): Part B, 29.
Cho, M., Kim, K.I., Min, E.Y. and Jung, S.H. (2019)Global outbreak and strategies to control emerging diseases in aquaculture farms in Korea. Ocean Policy Research, 34: 67-88.
Chun, S.-K. and Kim, Y-G. (1980) A trematode genus Bacciger parasitic in bivalves. The Korean Society Fisheries and Sciences Education, 13(4): 173-178.
Comps, M. (1982) Étude morphologique d'une infection rickettsienne de la palourde Ruditapes philippinarum Adams and Reeve. Revue des Travaux de l'Institut des Pêches Maritimes, 46: 141-145. [In French]
Dang, C., de Montaudouin, X., Gonzalez, P., Mesmer-Dudons, N. and Caill-Milly, N. (2008)Brown muscle disease (BMD), an emergent pathology affecting Manila clam Ruditapes philippinarum in Arcachon Bay (SW France). Diseases of Aquatic Organisms, 80: 219-228.
Dang, C., Gonzalez, P., Mesmer-Dudons, N., Bonami, J.R., Caill-Milly, N. and de Montaudouin, X. (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.
Dungan, C.F. and Reece, K.S. (2006) In vitro propagation of two Perkinsus spp. parasites from Japanese Manila clams Venerupis philippinarum and description of Perkinsus honshuensis n. sp. Journal of Eukaryotic Microbiology, 53: 316-326.
Elston, R.A. (1986) Occurrence of branchial rickettsialeslike infection in two bivalve molluscs, Tapes japonica and Patinopecten yessoensis, with comments on their significance. Journal of Fish Diseases, 9: 69-71.
EURL for mollusk diseases : 2020 http://www.eurl-mollusc.eu/Main-activities/Tutorials/Marteilia-refringens.
FAO (2020) FishStatJ. http://www.fao.org/fishery/statistics/software/fishstatj/en
Gao, W.H. (2016) The development of nested PCR detection method and genotyping system for ostreid herpesvitus-1. Shanghai Ocean University. [Dissertation]
Goedknegt, M.A., Feis, M., Wegner, M., Luttikhuizen, P.C., Buschbaum, C., Camphuysen, K., Van der Meer, J. and Thieltges, D.W. (2015) Parasites and marine invasions: Ecological and evolutionary perspectives. Journal of Sea Research, 113: 11-27.
Gómez-León, J., Villamil, L., Lemos, M.L., Novoa, B. and Figueras, A. (2005) Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Applied and Environmental Microbiology, 71: 98–104.
Gray, J.E., Belver, E., Adams, A., Richardson, J., Reeve, L. and White, A. (1850) The zoology of the voyage of H.M.S. Samarang, under the command of Captain Sir Edward Belcher, C.B., F.R.A.S., F.G.S., during the years 1843-1846. Reeve & Benham, London.
Grizel, H. (1985) Etude des récentes épizooties de l’huître plate (Ostrea edulis Linné) et leur impact sur l’ostréiculture bretonne. Thèse Doctorat es Sciences, Université des Sciences et Techniques du Languedoc, Montpellier, France, 145.
Grizel, H., Comps, M., Bonami, J.R., Cousserans, F., Duthoit, J.L. and LePennec, M.A. (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.
Han, J.E., Lee, S.C., Park, S.C., Jeon, H.Y., Kim, K.Y., Lee, Y.S., Park, S., Han, S.H., Kim, J.H. and Choi, S.K. (2020) Molecular detection of Enterocytozoon hepatopenaei and Vibrio parahaemolyticus-associated acute hepatopancreatic necrosis disease in Southeast Asian Penaeus vannamei shrimp imported into Korea. Aquaculture, 517: 734812.
Hamaguchi, M., Suzuki, N. and Usuki, H. (1998)Perkinsus protozoan infection in short-necked clam Tapes (= Ruditapes) philippinarum in Japan. Fish Pathology, 33: 473-480.
Hamaguchi, M., Sasaki, M. and Usuki, H. (2002)Prevalence of a Perkinsus protozoan in the clam Ruditapes philippinarum in Japan. Japanese Journal of Benthology, 57: 168-176.
Hwang, J.-Y., Park, J.-J., Yu, H.-J., Hur, Y.-B., Arzul, I., Couraleau, Y. and Park, M.A. (2013) Ostreid herpesvirus 1 infection in farmed Pacific oyster larvae Crassostrea gigas (Thunberg) in Korea. Journal of Fish Diseases, 36 (11): 969–972.
Itoh, N., Momoyama, K. and Ogawa, K. (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.
Itoh, N., Yamamoto, T., Kang, S.H., Choi, K.S., Green, T.J., Carrasco, N., Awaji, M. and Chow, S. (2014) A novel paramyxean parasite, Marteilia granula sp. nov. (Cercozoa), from the digestive gland of Manila clam Ruditapes philippinarum in Japan. Fish Pathology, 49: 181-193.
Itoh, N. EURL presentation http://www.eurl-mollusc.eu/content/download/39914/545434/file/1_Japan_mollusc_It oh.pdf.
Kang, H.-S., Yang, H.S., Reece, K., Cho, Y.G., Lee, H.-M., Kim, C.W. and Choi, K.-S. (2017) survey on Perkinsus species in Manila clam Ruditapes philippinarum in Korean waters using species-specific PCR. Fish Pathology, 52: 202-205.
Kang, H.-S., Itoh, N., Limpanont, Y., Lee, H.-M., Whang, I. and Choi, K.-S. (2019) A novel paramyxean parasite, Marteilia tapetis sp. nov. (Cercozoa)infecting the digestive gland of Manila clam Ruditapes philippinarum from the southeast coast of Korea. Journal of Invertebrate Pathology, 163: 86–93.
Kim, J.-H., Park, S.-W., Park, C.-I., Oh, M.-J., Jung, S.-J. and Huh, M.-D. (2006) Infectious and parasitic diseases of fish and shellfish. Life Science Publishing Co., Seoul.
Kim, W.S., Oh, M.J., Nishizawa, T., Park, J.W., Kurath, G. and Yoshimizu, M. (2007) Genotyping of Korean isolates of infectious hematopoietic necrosis virus (IHNV) based on the glycoprotein gene. Archives Virology, 152: 2119-2124.
Kim, W.S. and Oh, M.J. (2014) Genetic positioning of aquabirnavirus isolates from cultured Japanese eel Anguilla japonica in Korea. Diseases of Aquatic Organisms, 109: 9-14.
Kim, Y.G. and Chun, S.K. (1981) A trematode, Cercaria tapidis parasitic in the natural stock Tapes philippinarum. Bulletin of the Korean Fisheries Society, 14(4): 217-220.
Kim, Y.G. and Chun, S.K. (1983) Studies on a trematode parasitic in bivalves Ⅲ. On a new gymnophallid cercaira. Cercaria tapes n. sp. (trematoda) form a short-necked clam Tapes philippinarum. Bulletin of the Korean Fisheries Society, 16: 154-159.
Kim, Y.G., Lee, K.K. and Kim, Y.J. (1995) Studies on parasitic trematodes in bivalves – variation of infection rate of Cercaria tapidis and Cercaria harengulae. Journal of Fish Pathology, 8(1): 23-30.
KOSIS (2020) Domestic statistics. http://kosis.kr/index/index.do.
Lee, M.K., Cho, B.Y., Lee, S.J., Kang, J.Y., Jeong, H.D., Huh, S.H. and Huh, M.D. (2001) Histopathological lesions of Manila clam, Tapes philippinarum, from Hadong and Namhae coastal areas of Korea. Aquaculture, 201: 199–209.
Li, Y.G., Guo, Y.J. and Xing, K.Z. (2013) The causative survey of sudden death of Manila clam Ruditapes philippinarum cultured in Hangu. Tianjin. Fisheries Science, 32: 424-427.
Liang, Y.B., Zhang, X.C., Wang, L.J., Yang, B., Zhang, Y. and Cai, C.L. (2001) Prevalence of Perkinsus sp. in the Manila clam, Ruditapes philippinarum, along the Northern coast of the Yellow Sea in China. Chinese Journal of Oceanologia et Limunologia Sinica, 32: 502-511.
Ma, S., Chen. J., Chen, B., Xin, F., Zhou, S. and Cui, Y. (1997) Test simulation of environmental factors’ effects on short-necked clam (Ruditapes philippinarum Adams and Reeve) mortality. Marine Fisheries Research, 18:9-12.
Matsuyama, T., Sakai, T., Kiryu, I., Yuasa, K., Yasunobu, H., Kawamura, Y. and Sano, M. (2010)First isolation of Vibrio tapetis, the etiological agent of Brown Ring Disease (BRD), in Manila Clam Ruditapes philippinarum in Japan. Fish Pathology, 45: 77-79.
Mccallum, H., Harvell, C. and Dobson, A. (2003) Rates of spread of marine pathogens. Ecology Letter, 6:1062–1067.
NFQS (2020) Import quarantine statistics. http://nfqs.go.kr/2013/index.asp
Nakamura, K.C. and Kajihara, T.K.S. (1979) Distribution of a cyclopoid copepod, Pseudomylicola ostreae Yamaguti, associated with the marine mussel, Mytilus edulis galloprovincialis Lamarck, in Tokyo bay, Japan. Japanese Society of Systematic Zoology, 16: 17-22.
Nam, K.W., Jeung, H.D., Song, J.H., Park, K.H., Choi, K.S. and Park, K.I. (2018) High parasite burden increase the surfacing and mortality of the Manila clam (Ruditapes philippinarum) in intertidal sandy mudflats on the west coast of Korea during hot summer. Parasites & Vectors, 11(1): 42. DOI:10.1186/s13071-018-2620-3.
NFRDI (2009) A study on the stability of aquaculture in Manila clam, Ruditapes philippinarum. Report of National Fisheries Research & Development Institute.
NFRDI (2010) A report of Manila clam mortality on the west coast of Korea. http://m.nifs.go.kr/bbs?id=insmaterial&flag=pre&boardIdx=178&site=&cPage=230&depthFlag=&gu bun=A
Nicolas, J.L., Ansquer, D. and Cochard, J.C. (1992)Isolation and characterization of a pathogenic bacterium specific to Manila clam Tapes philippinarum larvae. Diseases of Aquatic Organisms, 14: 153-159.
Paillard, C. and Maes, P. (1994) Brown ring disease in the Manila clam Ruditapes philippinarum:establishment of a classification system. Diseases of Aquatic Organisms, 19: 137-146
Paillard, C. (2004) A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus. Aquatic Living Resources, 17: 467-475.
Park, G.-M. (2012) Korean molluscs as auxiliary hosts for parasites: A study of implications for pathogen transmission in a changing climate. The Korean Journal of Malacology, 28(2): 13-19
Park, K.I. and Choi, K.S., (2001) Spatial distribution of the protozoan parasite Perkinsus sp. found in the Manila clam Ruditapes philippinarum in Korea. Aquaculture, 203: 9–22.
Park, K.I., Figueras, A. and Choi, K.S. (2006)Application of enzyme-linked immunosorbent assay (ELISA) for the study of reproduction in the Manila clam Ruditapes philippinarum (Mollusca: Bivalvia):II. Impacts of Perkinsus olseni on clam reproduction. Aquaculture, 251: 182-191.
Park, K.I., Paillard, C., Le Chevalier, P. and Choi, K.S. (2006) Report on the occurrence of brown ring Disease (BRD) in Manila clam, Ruditapes philippinarum, on the West Coast of Korea. Aquaculture, 255: 610-613.
Park, K.I., Tsutsumi, H., Hong, J.S. and Choi, K.S. (2008) Pathology survey of the short-neck clam Ruditapes philippinarum occurring on sandy tidal flats along the coast of Ariake Bay, Kyushu, Japan. Journal of Invertebrate Pathology, 99(2): 212-9.
Pretto, T., Zambon, M., Civettini, M., Caburlotto, G., Boffo, L., Rossetti, E. and Arcangeli, G. (2014)Massive mortality in Manila clam (Ruditapes philippinarum) farm in the Lagoon of Venice, caused by Perkinsus olseni. Bulletin of the European Association of Fish Pathologists, 34: 43-53.
Renault, T., Lipart, C. and Arzul, I. (2001) A herpes-like virus infects a non-ostreid bivalve species: virus replication in Ruditapes philippinarum larvae. Disease of Aquatic Organisms, 45: 1-7.
Shimura, S., Yoshinaga, T. and Wakabayashi, H. (1982a)Three marine cercariae in the clam Tapes philippinarum from lake Hamana, Japan:morphology and level of infection. Fish Pathology, 17: 129-137.
Shimura, S.G., Yoshinaga, T.M.S. and Wakabayash, H.S.G. (1982b) Two Species of Marine Metacercariae, Parvatrema duboisi (Gymnophallidae) and Proctoeces sp. (Fellodistomidae), in the Clam Tapes philippinarum from Lake Hamana, Japan:Morphology and Level of Infection. Fish Pathology, 17(3): 187-194.
Song, J.-H. (2015) Strategy for the sustainable development of Manila clam farming industry. Aquaculture (Korean "Yangsik"). 9: 70–74. (in Korean).
Suh, H.L. and Choi, S.D. (1990) Two copepods (Crustacea) parasitic on the Blue mussel, Mytilus galloprovincialis, from the Yongsan river esturay in Korea. The Korean Society Fisheries and Sciences Education, 23(2): 137-140.
Taru, M., Nakayama, S., Takasaki, H. and Komai, T. (2007) Circumstances that bivalves are infested by Nymphonella tapetis at the Banzu-Tide-Land in Tokyo Bay. Umiushi Tsushin, 56: 4-5. [In Japanese]
Toba, M., Kobayashi, Y., Kakino, J., Yamakawa, H., Ishii, R. and Okamoto, R. (2016) Stocks and fisheries of asari in Japan. Bulletin of Japan Fisheries Research and Education Agency, 42: 9-21.
Thebault, A., Bergman, S., Pouillot, R., Le Roux, F. and Berthe, F.C. (2005) Validation of in situ hybridisation and histology assays for the detection of the oyster parasite Marteilia refringens. Diseases of Aquatic Organisms, 65(1): 9-16.
Tun, K.L., Itoh, N., Shimizu, Y., Yamanoi, H., Yoshinaga, T. and Ogawa, K. (2008) Pathogenicity of the protozoan parasite Marteilioides chungmuensis in the Pacific oyster Crassostrea gigas. International Journal for Parasitology, 38: 211-217.
Waki, T., Takahashi, M., Eki, T., Hiasa, M., Umeda, K., Karakawa, N. and Yoshinaga, T. (2018) Impact of Perkinsus olseni infection on a wild population of Manila clam Ruditapes philippinarum in Ariake Bay, Japan. Journal of Invertebrate Pathology, 153:134-144.
Waki, T. and Yoshinaga, T. (2018) Experimental evaluation of the impact of Perkinsus olseni on the physiological activities of juvenile Manila clams. Journal of Shellfish Research, 37(1): 29-39
Ward, G.M., Bennett, M., Bateman, K., Stentiford, G.D., Kerr, R., Feist, S.W., Williams, S.T., Berney, C. and Bass, D. (2016) A new phylogeny and environmental DNA insight into paramyxids: an increasingly important but enigmatic clade of protistan parasites of marine invertebrates. International Journal of Parasitology, 46: 605–619.
Wu, S.Q., Wang, C.X., Lin, X.M., Wang, Z.X., Li, X.F., Liu, J., Deng, J.H. and Qiu, S.Y. (2011) Infection prevalence and phylogenetic analysis of Perkinsus olseni in Ruditapes philippinarum from East China. Diseases of Aquatic Organisms, 96: 55-60.
Wu, Y.Q., Zhang, B.L. and Sun, D.Y. (1993) A study of the relation between the distribution of dead shells of Ruditapes philippinarum and the ecological environment in Jiaozhou Bay. Transactions of Oceanology and limnology, 4: 61-67.
Xie, L.J., Xie, Z.X., Pang, Y.S., Liu, J.P., Deng, X.W., Xie, Z.Q., Fan, Q. and Luo, S.S. (2012) Epidemiogical survey of four protozoans in shellfish of the coastlines in China. Genomica and Applied Biology, 31(6): 559-566.
Xu, K.D., Meng, F.L., Cao, J.X. and Song, W.B. (1997)Morphological studies on the thigmotrichine ciliate, Ancistrum crissum Fenchel, 1965 on the gills of short-necked clam. Journal of Ocean University of Qingdao, 27: 466-470.
Yang, H.-S., Park, K.-J. and Choi, K.-S. (2010)Pathologic survey on the Manila clam Ruditapes philippinarum (Adams and Reeve 1850) from Haeju off the western coastal Yellow Sea. Ocean Science Journal, 45(2): 93–100. doi:10.1007/s12601-010-0008-1
Yanin, L.P., Kang, H.-S., Hong, H.K., Jeung, H.-D., Kim, B.K., Le T.C., Kim, Y.O. and Choi K.-S. (2013)Molecular and histological identification of Marteilioides infection in suminoe oyster Crassostrea ariakensis, Manila clam Ruditapes philippinarum and pacific oyster Crassostrea gigas on the south coast of Korea. Journal of Invertebrate Pathology, 114(3): 277-284.
Yao, C.L. and Somero, G. (2014) The impact of ocean warming on marine organisms. Chinese Science Bulletin, 59: 468-479.
Yonhapnews agency. (2019) https://www.yna.co.kr/view/AKR20190923136100063
Yu, J.R., Chai, J.Y. and Lee, S.H. (1993) Parvatrema timondavidi (Digenea; Gymnophallidae) transmitted by a clam, Tapes philippinarum, in Korea. The Korean Journal of Parasitology, 31: 7-12.