Helminth parasites of fish and shellfish from the Santa Gilla Lagoon in southern Sardinia, Italy | Journal of Helminthology | Cambridge Core (original) (raw)

Abstract

An extensive survey of helminth parasites in fish and shellfish species from Santa Gilla, a brackish water lagoon in southern Sardinia (western Mediterranean), resulted in the identification of 69 helminth parasite taxa and/or species from 13 fish species (n= 515) and seven bivalve species (n= 2322) examined between September 2001 and July 2011. The list summarizes information on the helminth parasites harboured by fish and molluscs contained in the available literature. Digenea species (37), both adults and larvae, dominated the parasite fauna, whereas Cestoda were the least represented class (three species). Monogenea, Nematoda and Acanthocephala were present with 17, 6 and 6 species, respectively, which were mainly adults. The most widespread parasite species was the generalist Contracaecum rudolphii A (Nematoda). Other species, such as the Haploporidae and Ascocotyle (Phagicola) spp. 1 and 2 (Digenea), showed a high family specificity in Mugilidae. Importantly, the study recorded the occurrence of potential zoonotic agents, such as Heterophyes heterophyes, Ascocotyle (Phagicola) spp. and C. rudolphii A, the latter two reaching the highest indices of infection in the highly marketed fish grey mullet and sea bass, respectively. The highest parasite richness was detected in Dicentrarchus labrax, which harboured 17 helminth species, whereas the lowest value was observed in Atherina boyeri, infected by only three species. The list includes the first geographical record in Italian coastal waters of Robinia aurata and Stictodora sawakinensis, and 30 reports of new host–parasite complexes, including the larval stages of Ascocotyle (Ascocotyle) sp. and Southwellina hispida in D. labrax.

References

Abollo, E., Gestal, C. & Pascual, S. (1998) Parasites in the rock goby Gobius paganellus L. (Pisces: Gobiidae) and the shanny Lipophrys pholis L. (Pisces: Blenniidae) in NW Spain. Bulletin of European Association of Fish Pathologists 18, 162–164.Google Scholar

Anderson, M. (1981) The change with host age of the composition of the ancyrocephalinae (Monogenean) populations of parasites on thick-lipped grey mullets at Plymouth. Journal of the Marine Biological Association of the United Kingdom 61, 833–842.Google Scholar

Antonelli, L., Quilichini, Y. & Marchand, B. (2010a) Biological study of Furnestinia echeneis Euzet & Audouin 1959 (Monogenea: Monopisthocotylea: Diplectanidae), parasite of cultured Gilthead sea bream Sparus aurata (Linnaeus 1758) (Pisces: Teleostei) from Corsica. Aquaculture 307, 179–186.CrossRefGoogle Scholar

Antonelli, L., Quilichini, Y. & Marchand, B. (2010b) Sparicotyle chrysophrii (Van Beneden & Hesse 1863) (Monogenea: Polyopisthocotylea) parasite of cultured Gilthead sea bream Sparus aurata (Linnaeus 1758) (Pisces: Teleostei) from Corsica: ecological and morphological study. Parasitology Research 107, 389–398.Google Scholar

Bartoli, P. & Gibson, D.I. (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History 41, 1553–1570.Google Scholar

Bartoli, P., Gibson, D.I. & Bray, R.A. (1993) The Opecoelidae (Digenea) of sparid fishes of the western Mediterranean. VI. A redescription of Macvicaria mormyri (Stossich, 1885) n. comb. and a key to the opecoelids from western Mediterranean sparids. Systematic Parasitology 26, 59–67.CrossRefGoogle Scholar

Blasco-Costa, I., Montero, F.E., Gibson, D.I., Balbuena, J.A., Raga, J.A. & Kostadinova, A. (2009a) A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Saccocoelium Looss, 1902. Systematic Parasitology 72, 159–186.Google Scholar

Blasco-Costa, I., Montero, F.E., Balbuena, J.A., Raga, J.A. & Kostadinova, A. (2009b) A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Dicrogaster Looss, 1902 and Forticulcita Overstreet, 1982. Systematic Parasitology 72, 187–206.Google Scholar

Blasco-Costa, I., Montero, F.E., Gibson, D.I., Balbuena, J.A. & Kostadinova, A. (2009c) A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): two new haploporine genera and a key to the genera of the subfamily. Systematic Parasitology 72, 207–215.CrossRefGoogle Scholar

Blasco-Costa, I., Gibson, D.I., Balbuena, J.A., Raga, J.A. & Kostadinova, A. (2009d) A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Haploporus Looss, 1902 and Lecithobotrys Looss, 1902. Systematic Parasitology 73, 107–133.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. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar

Chai, J.Y., Hong, S.J., Lee, H.S. & Seo, B.S. (1988) Stictodora sp. (Trematoda: Heterophyidae) recovered from a man in Korea. The Korean Journal of Parasitology 26, 127–132.Google Scholar

Čož-Rakovac, R., Strunjak-Perović, I., Topić Popović, N., Hacmanjek, M., Šimpraga, B. & Teskeredžić, E. (2002) Health status of wild and cultured sea bass in the northern Adriatic Sea. Veterinary Medicine - Czech 47, 222–226.Google Scholar

Culurgioni, J., D'Amico, V., De Murtas, R., Canestri Trotti, G. & Figus, V. (2006) Parasitological monitoring of commercial native bivalves from St. Gilla lagoon (Sardinia, South Western Mediterranean). Ittiopatologia 3, 253–261.Google Scholar

Culurgioni, J., D'Amico, V., De Murtas, R., Cannella, S. & Figus, V. (2008) Contribution to the study of parasites infecting Mugilidae from Sardinian brackish waters: first data from St. Gilla lagoon (south western Mediterranean). Parassitologia 50, 26.Google Scholar

Culurgioni, J., De Murtas, R., Cannella, S. & Figus, V. (2010a) Parasites of wild European sea bass Dicentrarchus labrax (Linnaeus, 1758) from St. Gilla lagoon (Sardinia, South Western Mediterranean). Ittiopatologia 7, 123–133.Google Scholar

Culurgioni, J., De Murtas, R. & Figus, V. (2010b) Helminth parasites of European eel Anguilla anguilla L. from St. Gilla lagoon (Sardinia, South western Mediterranean). Ittiopatologia 7, 97–106.Google Scholar

Culurgioni, J., D'Amico, V., De Murtas, R. & Figus, V. (2010c) Parasite helminths from fish and shellfish from St. Gilla Lagoon (South Sardinia, western Mediterranean). Parassitologia 52, 350.Google Scholar

Culurgioni, J., Cannella, S., Sabatini, A., Sanna, N., Torcivia, A. & Figus, V. (2011) Metazoan parasites of wild gilthead seabream Sparus aurata L. from three Sardinian lagoons (South Western Mediterranean). Atti del XVII Convegno Nazionale della Società Italiana di Patologia Ittica S.I.P.I., Ostuni (BR), 19–21 May, p. 43.Google Scholar

Culurgioni, J., Sabatini, A., Cannella, S., De Murtas, R. & Figus, V. (2012) Zoonotic helminth parasites in commercial fish from three coastal lagoons of southern Sardinia (western Mediterranean). Atti del XVIII Convegno Nazionale della Società Italiana di Patologia Ittica S.I.P.I., Udine, 9–11 June, p. 46.Google Scholar

D'Amico, V., Culurgioni, J., De Murtas, R., Cannella, S. & Figus, V. (2008) Metazoan parasites of the killifish, Aphanius fasciatus Nardo 1827 (Teleostei: Cyprinodontidae), from St. Gilla lagoon, South Sardinia. Parassitologia 50, 25.Google Scholar

Daponte, M.C., Gil de Pertierra, A.A., Palmieri, M.A. & Ostrowski de Núñez, M. (2006) Parasite infections (Trematoda, Digenea) of Sagitta friderici (Chaetognatha) from the southwestern Atlantic Ocean: prevalence and distribution. Diseases of Aquatic Organisms 71, 225–232.CrossRefGoogle ScholarPubMed

Dezfuli, B.S., Volponi, S., Beltrami, I. & Poulin, R. (2002) Intra- and interspecific density-dependent effects on growth in helminth parasites of the cormorant, Phalacrocorax carbo sinensis. Parasitology 124, 537–544.CrossRefGoogle ScholarPubMed

Di Cave, D., Berrilli, F., De Liberato, C., Orecchia, P. & Kennedy, C.R. (2001) Helminth communities in eels Anguilla anguilla from Adriatic coastal lagoons in Italy. Journal of Helminthology 75, 7–13.Google Scholar

Elsheikha, H.M. & Elshazly, A.M. (2008) Preliminary observations on infection of brackish and fresh water fish by heterophyid encysted metacercariae in Egypt. Parasitology Research 103, 971–977.Google Scholar

Esch, G.W., Kennedy, C.R., Bush, A.O. & Aho, J.M. (1988) Patterns in helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96, 519–532.Google Scholar

Euzet, L. & Suriano, D.M. (1977) Ligophorus n.g. (Monogenea, Ancyrocephalidae) parasite des Mugilidae (Téléostéens) en Méditerranée. Bulletin du Muséum National d'Histoire Naturelle. Troisieme Serie 472, 799–822.Google Scholar

Farjallah, S., Merella, P., Ingrosso, S., Rotta, A., Ben Slimane, B., Garippa, G., Said, K. & Busi, M. (2008) Molecular evidence for the occurrence of Contracaecum rudolphii A (Nematoda: Anisakidae) in shag Phalacrocorax aristotelis (Linnaeus) (Aves: Phalacrocoracidae) from Sardinia (western Mediterranean Sea). Parasitology International 57, 437–440.CrossRefGoogle ScholarPubMed

Figus, V., Corriga, V. & Canestri Trotti, G. (2002a) Elminti parassiti di Anguilla anguilla nelle lagune di Cabras, S.ta Giusta e S.ta Gilla (Sardegna, Italia). Bollettino della Società Italiana di Patologia Ittica 34, 23–33.Google Scholar

Figus, V., Culurgioni, J. & Canestri Trotti, G. (2002b) Parasitological monitoring of Paphia aurea and P. aurea var. bicolor from St. Gilla lagoon (Cagliari-Italy). Bollettino della Società Italiana di Patologia Ittica 35, 55–63.Google Scholar

Figus, V., Culurgioni, J., De Murtas, R. & Canestri Trotti, G. (2004a) Parasites of Cerastoderma glaucum (Poiret,1789) (Bivalvia: Cardiidae), from Marceddì and St. Gilla lagoons (Sardinia, Western Mediterranean). Biologia Marina Mediterranea 11, 385–388.Google Scholar

Figus, V., Curridori, C., De Murtas, R. & Canestri Trotti, G. (2004b) Monitoring of parasitic infection in native bivalves from St. Gilla lagoon (Cagliari – Italy). Biologia Marina Mediterranea 11, 95.Google Scholar

Figus, V., Culurgioni, J., De Murtas, R. & Canestri Trotti, G. (2006) Parassiti di Cerastoderma glaucum (Poiret, 1879) (Bivalvia: Cardiidae) della laguna di S.ta Gilla, Sardegna meridionale. Ittiopatologia 3, 69–74.Google Scholar

Fioravanti, M.L., Caffara, M., Florio, D., Gustinelli, A. & Marcer, F. (2006) A parasitological survey of European sea bass (Dicentrarchus labrax) and gilthead bream (Sparus aurata) cultured in Italy. Veterinary Research Communications 30, 249–252.Google Scholar

Fried, B., Graczyk, T.K. & Tamang, L. (2004) Food-borne intestinal trematodiases in humans. Parasitology Research 93, 159–170.Google Scholar

Gargouri-Ben Abdallah, L. & Maamouri, F. (2002) Cycle evolutif de Bucephalus anguillae Spakulova, Macko, Berrilli & Dezfuli, 2002 (Digenea, Bucephalidae) parasite de Anguilla anguilla (L.). Systematic Parasitology 53, 207–217.Google Scholar

Gargouri-Ben Abdallah, L. & Maamouri, F. (2005) The life cycle of Bucephalus labracis Paggi & Orecchia, 1965 (Digenea, Bucephalidae), a parasite of Dicentrarchus labrax in Tunisia. Bulletin of the European Association of Fish Pathologists 25, 297–302.Google Scholar

Golvan, Y.J. (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi, 1801). L'ordre des Paleacanthocephala Meyer 1931. I. La super-famille des Echinorhynchoidea (Cobbold, 1876) Golvan et Houin 1963. Memoires du Muséum National d'Histoire Naturelle 57, 1–373.Google Scholar

Jousson, O. & Bartoli, P. (2001) Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. International Journal for Parasitology 31, 706–714.Google Scholar

Laffargue, P., Baudouin, G., Sasal, P., Arnaud, C., Begout Anras, M.L. & Lagardère, F. (2004) Parasitic infection of sole Solea solea by Prosorhynchus spp. metacercariae (Digenea, Bucephalidae) in Atlantic nurseries under mussel cultivation influence. Diseases of Aquatic Organisms 58, 179–184.Google Scholar

Lebre, C. & Petter, A.J. (1984) Cucullanus campanae n. sp. (Cucullanidae, Nematoda), parasite de la Sole: Solea vulgaris vulgaris (Pleuronectiformes). Bulletin de Museum National d'Histoirie Naturelle 6, 999–1005.Google Scholar

Maillard, C. (1971) Cycle évolutif de Cainocreadium labracis (Dujardin, 1845) (Trematoda, Allocreadiidae). Comptes Rendus de l'Académie des Sciences. Serie D 272, 3303–3306.Google Scholar

Maillard, C. (1974) Cycle évolutif de Timoniella praeteritum (Looss, 1901) (Trematoda, Acanthostomidae) parasite de Morone labrax (Teleostei, Serranidae). Bulletin de la Société Zoologique de France 99, 245–257.Google Scholar

Maillard, C. & Saad-Fares, A. (1981) Bucephalus baeri n. sp. (Trematoda) parasite de Dicentrarchus labrax (Teleostei): description et cycle évolutif. Zeitschrift für Parazitenkunde 66, 31–40.Google Scholar

Maillard, C., Euzet, L. & Silan, P. (1988) Création du genre Serranicotyle (Monogenea, Microcotylidae): Serranicotyle labracis (Van Beneden et Hesse, 1863) n. comb. ectoparasite de Dicentrarchus labrax (Teleostei). Annales de Parasitologie Humaine et Comparée 63, 33–36.Google Scholar

Maíllo, P.A., Vich, M.A., Salvadó, H., Marqués, A. & Gracia, M.P. (2005) Parasites of Anguilla anguilla (L.) from three coastal lagoons of the River Ebro delta (Western Mediterranean). Acta Parasitologica 50, 156–160.Google Scholar

Mattiucci, S., Turchetto, M., Brigantini, F. & Nascetti, G. (2002) On the occurrence of the sibling species of Contracaecum rudolphii complex (Nematoda: Anisakidae) in cormorants (Phalacrocorax carbo sinensis) from Venetian and Caorle lagoons: genetic markers and ecological studies. Parassitologia 44, 105.Google Scholar

Mattiucci, S., Paoletti, M., Olivero-Verbel, J., Baldiris, R., Arroyo-Salgado, B., Garbin, L., Navone, G., & Nascetti, G. (2008) Contracaecum bioccai n. sp. from the brown pelican Pelecanus occidentalis (L.) in Colombia (Nematoda: Anisakidae): morphology, molecular evidence and its genetic relationship with congeners from fish-eating birds. Systematic Parasitology 69, 101–121.Google Scholar

Merella, P. & Garippa, G. (2001) Metazoan parasites of grey mullets (Teleostea: Mugilidae) from the Mistras Lagoon (Sardinia, western Mediterranean). Scientia Marina 65, 201–206.Google Scholar

Merella, P., Marino, G. & Garippa, G. (2004) Heterophyid metacercariae (Trematoda: Heterophyidae) in grey mullets (Osteichthyes: Mugilidae) from the Cabras and Mistras lagoons (Sardinia, western Mediterranean). Parassitologia 46, 157.Google Scholar

Merella, P., Garippa, G. & Salati, F. (2006) Parasites of cage cultured European sea bass Dicentrarchus labrax and gilthead sea bream Sparus aurata from Sardinia (western Mediterranean): first results. Parassitologia 48, 290.Google Scholar

Moravec, F. (1994) Parasitic nematodes of freshwater fishes of Europe. 473 pp. Dordrecht, Kluwer Academic Publishers.Google Scholar

Moravec, F. (2009) Experimental studies on the development of Contracaecum rudolphii (Nematoda: Anisakidae) in copepod and fish paratenic hosts. Folia Parasitologica 56, 185–193.Google Scholar

Moravec, F., Di Cave, D., Orecchia, P. & Paggi, L. (1993) Studies on the development of Anguillicola crassus Kuwahara Niimi et Itagaki 1974 (Nematoda: Dracunculoidea) in the intermediate host. Folia Parasitologica 40, 39–48.Google Scholar

Moravec, F., Glamuzin, B., Marino, G., Merella, P. & Di Cave, D. (2003) Occurrence of Philometra lateolabracis (Nematoda: Philometridae) in the gonads of marine perciform fishes in the Mediterranean region. Diseases of Aquatic Organisms 53, 267–269.Google Scholar

Öktener, A., Yurdakul, N., Alaş, A. & Solak, K. (2010) Fish-borne parasitic zoonoses in Turkish waters. Gazi University Journal of Science 23, 255–260.Google Scholar

Paggi, L. & Orecchia, P. (1965) Su un nuovo trematode parassita dell'intestino di Morone labrax: Bucephalus labracis n. sp. Parassitologia 7, 69–74.Google Scholar

Palombi, A. (1933) Cercaria pectinata Huet e Bacciger bacciger (Rud.). Rapporti genetici e biologia. Bolletino di Zoologia 4, 1–11.Google Scholar

Palombi, A. (1934) Gli stadi larvali dei Trematodi del Golfo di Napoli. 1. Contributo allo studio della morfologia, biologia e sistematica delle cercarie marine. Pubblicazioni della Stazione Zoologica di Napoli 14, 51–94.Google Scholar

Palombi, A. (1949) Trematodi d'Italia. Parte I. Trematodi Monogenetici. Archivio Zoologico Italiano 34, 203–408.Google Scholar

Pankov, P., Webster, B.L., Blasco-Costa, I., Gibson, D.I., Littlewood, I.T.J., Balbuena, J.A. & Kostadinova, A. (2006) Robinia aurata n.g., n. sp. (Digenea: Hemiuridae) from the mugilid Liza aurata with a molecular confirmation of its position within the Hemiuroidea. Parasitology 133, 217–227.CrossRefGoogle Scholar

Paperna, I. & Overstreet, R.M. (1981) Parasites and diseases of mullets (Muligidae). pp. 410–493_in_ Oren, O.H. (Ed.) Aquaculture of grey mullets. Cambridge, Cambridge University Press.Google Scholar

Pearson, J.C. (1973) A revision of the subfamily Haplorchinae Looss, 1899 (Trematoda: Heterophyidae) II. Genus Galactosomum. Philosophical Transactions of the Royal Society of London 266, 341–446.Google Scholar

Pina, S., Barandela, T., Santos, M.J., Russell-Pinto, F. & Rodrigues, P. (2009) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological, and molecular data. Journal of Parasitology 95, 353–359.Google Scholar

Priore, G., Orecchia, P., Ortis, M., Palladino, S. & Paggi, L. (1992) Indagine parassitologica su alcune delle specie ittiche eurialine di interesse commerciale del lago di Lesina (Foggia, Italia). Oebalia Suppl. XVII, 227–228.Google Scholar

Ragias, V., Athanassopoulou, F. & Sinis, A. (2005) Parasites of Mugilidae spp. reared under semiintensive and intensive conditions in Greece. Bulletin of European Association of Fish Pathologists 25, 107–115.Google Scholar

Sanmartìn, M.L., Alvarez, F., Peris, D., Iglesias, R. & Leiro, J. (2001) Helminth parasites of the black goby Gobius niger in the Arousa and Muros estuaries on the Northwest coast of Spain. Revista Ibérica de Parasitologia 61, 24–30.Google Scholar

Schmidt, G.D. (1973) Resurrection of Southwellina Witenberg, 1932, with a description of Southwellina dimorpha sp. n., and a key to genera in Polymorphidae (Acanthocephala). Journal of Parasitology 59, 299–305.Google Scholar

Scholz, T., Aguirre-Macedo, M.L. & Salgado-Maldonado, G. (2001) Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records. Journal of Natural History 35, 1733–1772.Google Scholar

Sey, O., Nahhas, F.M., Uch, S. & Vang, C. (2003) Digenetic trematodes from marine fishes off the coast of Kuwait, Arabian Gulf: Fellodistomidae and some smaller families, new host and geographic records. Acta Zoologica Academiae Scientiarum Hungaricae 49, 179–200.Google Scholar

Sohn, W.M. (2009) Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean Journal of Parasitology 47, 103–113.Google Scholar

Spakulova, M., Macko, J.K., Berrilli, F. & Dezfuli, B.S. (2002) Description of Bucephalus anguillae n. sp. (Trematoda: Bucephalidae), a parasite of the eel Anguilla anguilla (Anguillidae) from a brackish water lagoon of the Adriatic Sea. Journal of Parasitology 88, 382–387.Google Scholar

Stunkard, H.W. (1977) Studies on Tetraphyllidean and Tetrarhynchidean metacestodes from squids taken on the New England coast. The Biological Bulletin 153, 387–412.Google Scholar

Yemmen, C., Ktari, M.H. & Bahri, S. (2012) Parasitofauna of some mugilid and soleid fish species from Tunisian lagoons. Acta Adriatica 52, 173–182.Google Scholar

Youssef, M.M., Mansour, N.S., Hammouda, N.A., Awadalla, H.N., Khalifa, R. & Boulos, L.M. (1987) Studies on some developmental stages in the life cycle of Pygidiopsis genata Looss 1901 (Trematoda: Heterophyidae) from Egypt. Journal of the Egyptian Society of Parasitology 17, 463–474.Google Scholar