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Morphological characterisation and identification of four species of Cardicola Short, 1953 (Trematoda: Aporocotylidae) infecting the Atlantic bluefin tuna Thunnus thynnus (L.) in the Mediterranean Sea

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Abstract

Blood flukes of the genus Cardicola Short, 1953 are considered the most potentially pathogenic parasites in bluefin tuna cultures. Morphological study and genetic analyses of the ribosomal internal transcribed spacer ITS-2 and the mitochondrial cytochrome c oxidase 1 (cox1) gene fragments revealed the occurrence of four aporocotylid species (C. forsteri Cribb, Daintith & Munday, 2000, C. orientalis Ogawa, Tanaka, Sugihara & Takami, 2010, C. opisthorchis Ogawa, Ishimaru, Shirakashi, Takami & Grabner, 2011 and Cardicola sp.) in 421 Thunnus thynnus (L.) from the Western Mediterranean (274 fished from the wild and 147 from sea-cages). Cardicola opisthorchis was the most abundant species, with higher prevalence in the cage-reared fish than in those fished in the wild (21 vs 6%, p < 0.05). Adults of three species were recovered: C. forsteri from both gills and heart, C. opisthorchis from heart and C. orientalis from gills. The secondary gill lamellae were profusely infected by eggs of C. orientalis. A fourth species was found in four tunas, based on the molecular analyses of eggs apparently indistinguishable in size and shape from the eggs of C. orientalis. The findings provided evidence that infections with Cardicola spp. differed in relation to locality, host origin (wild vs cage-reared) and site of infection. It is necessary to estimate the possible different pathogenic effects of each species of Cardicola in order to take appropriate control measures.

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References

  • Aiken, H. M., Bott, N. J., Mladineo, I., Montero, F. E., Nowak, B. F., & Hayward, C. J. (2007). Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). Fish and Fisheries, 8, 167–180.

    Article  Google Scholar 

  • Aiken, H. M., Hayward, C. J., & Nowak, B. F. (2006). An epizootic and its decline of a blood fluke Cardicola forsteri in farmed southern bluefin tuna, Thunnus maccoyii. Aquaculture, 254, 40–45.

    Article  Google Scholar 

  • Anderson, G. R., & Barker, S. C. (1998). Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) ribosomal DNA. Systematic Parasitology, 41, 87–94.

    Article  Google Scholar 

  • Bullard, S. A., Goldstein, R. J., Goodwin, R. H, I. I. I., & Overstreet, R. M. (2004). Cardicola forsteri (Digenea: Sanguinicolidae) from the heart of a northern bluefin tuna, Thunnus thynnus (Scombridae), in the Northwest Atlantic Ocean. Comparative Parasitology, 71, 245–246.

    Article  Google Scholar 

  • Bush A. O., Lafferty K. D., Lotz J. M., & Shostak A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revised. Journal of Parasitology, 83, 575–583.

  • Collette, B., Acero, A., Boustany, A., Canales Ramirez, C., Cardenas, G., Carpenter, K. E., Chang, S. K., Chiang, W., Di Natale, A., Die, D., Fox, W., Graves, J., Hinton, M., Juan Jorda, M., Minte Vera, C., Miyabe, N., Montano Cruz, R., Nelson, R., Restrepo, V., Schaefer, K., Schratwieser, J., Serra, R., Sun, C., Uozumi, Y. & Yanez, E. (2011). Thunnus orientalis. In: IUCN 2011. IUCN Red List of Threatened Species. Version 2011.2.

  • Cribb, T. H., Adlard, R. D., Hayward, C. J., Bott, N. J., Ellis, D., Evans, D., & Nowak, B. F. (2011). The life cycle of Cardicola forsteri (Trematoda: Aporocotylidae), a pathogen of ranched southern bluefin tuna, Thunnus maccoyi. International Journal for Parasitology, 41, 861–870.

    Article  PubMed  Google Scholar 

  • Cribb, T. H., Daintith, M., & Munday, B. (2000). A new blood-fluke, Cardicola forsteri,(Digenea: Sanguinicolidae) of southern blue-fin tuna (Thunnus maccoyii) in aquaculture. Transactions of the Royal Society of South Australia Incorporated, 124, 117–120.

    Google Scholar 

  • Culurgioni, J., Mele, S., Merella, P., Addis, P., Figus, V., Cau, A., Karakulak, F. S., Garippa, G. (2014). Metazoan gill parasites of the Atlantic bluefin tuna Thunnus thynnus (Linnaeus) (Osteichthyes: Scombridae) from the Mediterranean and their possible use as biological tags. Folia Parasitologica, 61, 148–156.

    PubMed  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772–772.

  • Dennis, M. M., Landos, M., & D’Antignana, T. (2011). Case - control study of epidemic mortality and Cardicola forsteri-associated disease in farmed southern bluefin tuna (Thunnus maccoyii) of South Australia. Veterinary Pathology Online, 48, 846–855.

    Article  CAS  Google Scholar 

  • FAO (1994). FAO Fisheries Technical Paper No. 337. World review of highly migratory species and straddling stocks. Rome: FAO, 70 pp.

  • Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hardy-Smith, P., Ellis, D., Humphrey, J., Evans, M., Evans, D., Rough, K., Valdenegro, V., Nowak, B. (2012). In vitro and in vivo efficacy of anthelmintic compounds against blood fluke Cardicola forsteri. Aquaculture, 334, 39–44.

    Article  Google Scholar 

  • Hayward, C. J., Ellis, D., Foote, D., Wilkinson, R. J., Crosbie, P. B., Bott, N. J., & Nowak, B. F. (2010). Concurrent epizootic hyperinfections of sea lice (predominantly Caligus chiastos) and blood flukes (Cardicola forsteri) in ranched southern bluefin tuna. Veterinary Parasitology, 173, 107–115.

    Article  PubMed  Google Scholar 

  • Holzer, A. S., Montero, F. E., Repullés, A., Nolan, M. J., Sitja-Bobadilla, A., Alvarez-Pellitero, P., Zarza, C., Raga, J. A., (2008). Cardicola aurata sp. n. (Digenea: Sanguinicolidae) from Mediterranean Sparus aurata L. (Teleostei: Sparidae) and its unexpected phylogenetic relationship with Paradeontacylix McIntosh, 1934. Parasitology International, 57, 472–482.

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru, K., Mine, R., Shirakashi, S., Kaneko, E., Kubono, K., Okada, T., Sawada, Y., Ogawa, K., (2013). Praziquantel treatment against Cardicola blood flukes: Determination of the minimal effective dose and pharmacokinetics in juvenile Pacific bluefin tuna. Aquaculture, 402, 24–27.

    Article  Google Scholar 

  • Mladineo, I. (2006). Parasites of Adriatic cage reared fish. Acta Adriatica, 47, 23–28.

    Google Scholar 

  • Mladineo, I., & Tudor, M. (2004). Digenea of Adriatic cage-reared Northern bluefin tuna (Thunnus thynnus thynnus). Bulletin of the European Association of Fish Pathologists, 24, 144–152.

    Google Scholar 

  • Mladineo, I., Zilic, J., & Cankovic, M. (2008). Health survey of Atlantic bluefin tuna, Thunnus thynnus (Linnaeus, 1758), reared in Adriatic cages from 2003 to 2006. Journal of the World Aquaculture Society, 39, 281–289.

    Article  Google Scholar 

  • Morgan, J. A. T., & Blair, D. (1998). Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology, 116, 289–297.

    Article  CAS  PubMed  Google Scholar 

  • Nolan, M. J., & Cribb, T. H. (2004). Two new blood flukes (Digenea: Sanguinicolidae) from Epinephelinae (Perciformes: Serranidae) of the Pacific Ocean. Parasitology International, 53, 327–335.

    Article  PubMed  Google Scholar 

  • Nolan, M. J., & Cribb, T. H. (2006a). An exceptionally rich complex of Sanguinicolidae von Graff, 1907 (Platyhelminthes: Trematoda) from Siganidae, Labridae and Mullidae (Teleostei: Perciformes) from the Indo-west Pacific Region. Zootaxa, 1218, 3–80.

    Google Scholar 

  • Nolan, M. J., & Cribb, T. H. (2006b). Cardicola Short 1953 and Braya n. gen. (Digenea: Sanginicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa, 1265, 1–80.

    Google Scholar 

  • Nowak, B. F. (2004). Assessment of health risks to southern bluefin tuna under current culture conditions. Bulletin of the European Association of Fish Pathologists, 24, 45–51.

    Google Scholar 

  • Nowak, B., Mladineo, I., Aiken, H., Bott, N., & Hayward, C. (2006). Results of health surveys of two species of farmed tuna: Southern bluefin tuna (Thunnus maccoyii) in Australia and northern bluefin tuna (Thunnus thynnus) in the Mediterranean. Bulletin of the European Association of Fish Pathologists, 26, 38–42.

    Google Scholar 

  • Ogawa, K., Ishimaru, K., Shirakashi, S., Takami, I., & Grabner, D. (2011). Cardicola opisthorchis n. sp. (Trematoda: Aporocotylidae) from the Pacific bluefin tuna, Thunnus orientalis (Temminck & Schlegel, 1844), cultured in Japan. Parasitology International, 60, 307–312.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa, K., Tanaka, S., Sugihara, Y., & Takami, I. (2010). A new blood fluke of the genus Cardicola (Trematoda: Sanguinicolidae) from Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel, 1844) cultured in Japan. Parasitology International, 59, 44–48.

    Article  CAS  PubMed  Google Scholar 

  • Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.

    Article  CAS  PubMed  Google Scholar 

  • Padrós, F., Zarza, C., & Crespo, S. (2001). Histopathology of cultured sea bream Sparus aurata infected with sanguinicolid trematodes. Diseases of Aquatic Organisms, 44, 47–52.

    Article  PubMed  Google Scholar 

  • Paperna, I., & Dzikowski, R. (2006). Digenea (Phylum Platyhelminthes). In: Woo P. T. K. (Ed.) Fish diseases and disorders, Volume 1, 2nd edn. Wallingford, UK: CAB International.

  • Polinski, M., Hamilton, D. B., Nowak, B., & Bridle, A. (2013). SYBR, TaqMan, or both: Highly sensitive, non-invasive detection of Cardicola blood fluke species in Southern Bluefin Tuna (Thunnus maccoyii). Molecular and Biochemical Parasitology, 191, 7–15.

    Article  CAS  PubMed  Google Scholar 

  • Razo-Mendivil, U., Rosas-Valdez, R., & Pérez-Ponce de León, G. (2008). A new cryptogonimid (Digenea) from the Mayan cichlid, Cichlasoma urophthalmus (Osteichthyes: Cichlidae), in several localities of the Yucatán Peninsula, Mexico. Journal of Parasitology, 94, 1371–1378.

    Article  CAS  PubMed  Google Scholar 

  • Reiczigel, J., & Rózsa, L. (2005). Quantitative Parasitology 3.0. Budapest. Distributed by the authors.

  • Repullés-Albelda, A., Montero, F. E., Holzer, A. S., Ogawa, K., Hutson, K. S., & Raga, J. A. (2008). Speciation of the Paradeontacylix spp. (Sanguinicolidae) of Seriola dumerili two new species of the genus Paradeontacylix from the Mediterranean. Parasitology International, 57, 405–414.

    Article  PubMed  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Ruíz de Ybáñez, R. R., Peñalver, J., Martínez-Carrasco, C., Del Rio, L., Mª Dolores, E., Berriatua, E., & Muñoz, P. (2011). Blood fluke infection of cage reared Atlantic bluefin tuna, Thunnus thynnus in West Mediterranean. Fish Pathology, 46, 87–90.

    Article  Google Scholar 

  • Shirakashi, S., Kishimoto, Y., Kinami, R., Katano, H., Ishimaru, K., Murata, O., Itoh, N., Ogawa, K., (2012). Morphology and distribution of blood fluke eggs and associated pathology in the gills of cultured pacific bluefin tuna, Thunnus orientalis. Parasitology International, 61, 242–249.

    Article  PubMed  Google Scholar 

  • Shirakashi, S., Tsunemoto, K., Webber, C., Rough, K., Ellis, D., & Ogawa, K. (2013). Two species of Cardicola (Trematoda: Aporocotylidae) found in southern bluefin tuna Thunnus maccoyii ranched in South Australia. Fish Pathology, 48, 1–4.

    Article  Google Scholar 

  • Sibeni, F., & Calderini, F. (2014). FishStatJ: Universal software for fishery statistical time series. FAO Fisheries and Aquaculture Department, Statistics and Information Service.

  • Sun, X., Yoshinaga, T., Doi, H., Shirakashi, S., Ishimaru, K., & Ogawa K. (2011). In vitro efficacy of praziquantel against fish blood flukes. Annual meeting of the Japanese Society of Fish Pathology, Tokyo: Japan, p. 30.

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are indebted to Grup Balfegó for their support and collaboration. We are grateful to P. Addis, J. Culurgioni (University of Cagliari), D. Macías and E. Rodríguez-Marín (Spanish Institute of Oceanography) for their support and collaboration during sampling. We also thank N. Fraija (University of Valencia) for her help in the laboratory analyses. Thanks are also due to F. Barraclough for revising the English. JP-A benefits from a “Atracció de talent” PhD student grant from the University of Valencia and JR-L benefits from a PhD fellowship from the Spanish Ministry of Education and Science (ESM).

Funding

This study was funded by the Ministry of Science and Innovation, Spanish Government (project AGL 2010-20892) and by the Valencian Local Government (projects PROMETEO 2015-018 and ISIC/2012/003).

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The authors declare that they have no conflict of interest.

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All applicable institutional, national and international guidelines for the care and use of animals were followed.

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Correspondence to José F. Palacios-Abella.

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Palacios-Abella, J.F., Rodríguez-Llanos, J., Mele, S. et al. Morphological characterisation and identification of four species of Cardicola Short, 1953 (Trematoda: Aporocotylidae) infecting the Atlantic bluefin tuna Thunnus thynnus (L.) in the Mediterranean Sea. Syst Parasitol 91, 101–117 (2015). https://doi.org/10.1007/s11230-015-9568-x

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