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Morphological and molecular study of Didymodiclinus marginati n. sp. (Trematoda: Didymozoidae) gill parasite of Epinephelus marginatus from the central and western Mediterranean Sea

Published online by Cambridge University Press:  27 May 2022

Salvatore Mele
Affiliation:
Department of Veterinary Medicine, University of Sassari, 07100 Sassari, Italy
Giovanni De Benedetto
Affiliation:
Department of Veterinary Sciences, University of Messina, Messina, Italy
Alessia Giannetto
Affiliation:
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy
Kristian Riolo
Affiliation:
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy
Sabrina Oliva
Affiliation:
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy
Olga Reñones
Affiliation:
Instituto Español de Oceanografía (IEO, CSIC), Centro Oceanográfico de Baleares, Ecosystem Oceanography Group (GRECO), Palma 07015, Spain
Giovanni Garippa
Affiliation:
Department of Veterinary Medicine, University of Sassari, 07100 Sassari, Italy
Paolo Merella
Affiliation:
Department of Veterinary Medicine, University of Sassari, 07100 Sassari, Italy
Gabriella Gaglio*
Affiliation:
Department of Veterinary Sciences, University of Messina, Messina, Italy
*
Author for correspondence: Gabriella Gaglio, Email: ggaglio@unime.it

Abstract

The current study provides a morphological and molecular characterization of a new species of Didymodiclinus (Trematoda: Didymozoidae) infecting the dusky grouper, Epinephelus marginatus (Teleostei: Serranidae) from the Mediterranean Sea. A total of 279 dusky grouper specimens were examined for didymozoid gill parasites from the Mediterranean Sea between 1998 and 2020. New species differs from the most similar congeneric species by the rudiments of female reproductive organs in functional male specimens, and the seminal receptacle, Mehlis gland and accessory gland cells in functional female specimens, not observed in Didymodiclinus branchialis (Yamaguti, 1970), Didymodiclinus epinepheli (Abdul-Salam, Sreelatha and Farah, 1990) and Didymodiclinus pacificus (Yamaguti, 1938), respectively. These species are also characterized by their different hosts and location within the host tissues, being from other geographical localities. Moreover, this is the first species reported in E. marginatus from the central and western Mediterranean Sea. Genetic analyses were performed on partial 28S and partial internal transcribed spacer-2 ribosomal RNA regions and the mitochondrial cytochrome oxidase 1 (cox1) gene by polymerase chain reaction. Comparison of genetic sequences of Didymodiclinus marginati n. sp. with the available deposited sequences of 28S revealed that the new isolates cluster with several unidentified didymozoids and groups as a sister clade of the Nematobothrinae subfamily. Moreover, 28S and cox1 phylogenetic trees evidenced that Didymodiclinae is well separated from Didymozoinae and other gonochoric didymozoids. Following both morphological and genetic results, a key of identification for the genus Didymodiclinus is proposed.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

Both authors contributed equally and share the first position.

References

Abdul-Salam, J, Sreelatha, B and Farah, M (1990) Gonapodasmius epinepheli n. sp. (Didymozoidae) from the grouper Epinephelus tauvina from the Arabian Gulf. Systematic Parasitology 17, 6774.CrossRefGoogle Scholar
Abe, N and Okamoto, M (2015) Molecular characterization of muscle-parasitizing didymozoid from a chub mackerel, Scomber japonicus. Acta Parasitologica 60, 557562.CrossRefGoogle ScholarPubMed
Abe, N, Okamoto, M and Maehara, T (2014) Molecular characterization of muscle-parasitizing didymozoids in marine fishes. Acta Parasitologica 59, 354358.CrossRefGoogle ScholarPubMed
Anderson, GR and Barker, SC (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology 41, 8794.CrossRefGoogle Scholar
Azzurro, E, Berrilli, F, De Liberato, C, Di Cave, D and Orecchia, P (2002) Contributo alla conoscenza dei metazoi parassiti della cernia di scoglio (Epinephelus marginatus Lowe, 1834) del Mediterraneo. Atti del IX Convegno Nazionale della Società Italiana di Patologia Ittica 9, 14.Google Scholar
Canestri-Trotti, G, Fioravanti, ML, Patarnello, PP and Restani, R (1994) Capsule branchiali da trematodi Didymozoidae in cernie (Epinephelus guaza) (Perciformes: Serranidae) dell'Adriatico meridionale. Parassitologia 36, 26.Google Scholar
Cruz-Lacierda, ER, Lester, RJG, Eusebio, PS, Marcial, HS and Pedrajas, SAG (2001) Occurrence and histopathogenesis of a didymozoid trematode Gonapodasmius epinepheli in pond-reared orange-spotted grouper, Epinephelus coioides. Aquaculture 201, 211217.CrossRefGoogle Scholar
De Benedetto, G, Arfuso, F, Ferrara, MC, Brianti, E and Gaglio, G (2021) Parasite fauna of the dusky grouper (Epinephelus marginatus, Lowe 1834) from the Central Mediterranean Sea. Animals 11, 2523.CrossRefGoogle ScholarPubMed
Gijón-Botella, H and López-Román, R (1987) Branchial parasites of Epinephelus guaza (L.) in the Canary Archipelago. Parasitology International 47, 620.Google Scholar
Gu, CD and Shen, JW (1983) Four new species of didymozoid trematodes from China. Acta Zootaxonomica Sinica 8, 1723.Google Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Lefort, V, Longueville, J-E and Gascuel, O (2017) SMS: Smart Model Selection in PhyML. Molecular Biology and Evolution 34(9), 24222424.CrossRefGoogle ScholarPubMed
Madhavi, R and Murugesh, M (1994) Gonapodasmid didymozoids (Digenea: Didymozoidae) from serranid fishes of the Visakhapatnam Coast, Bay of Bengal. Rivista di Parassitologia 55, 4755.Google Scholar
Mele, S, Pennino, MG, Piras, MC, Macías, D, Gómez-Vives, MJ, Alemany, F, Montero, FE, Garippa, G and Merella, P (2016) Ecology of the Atlantic black skipjack Euthynnus alletteratus (Osteichthyes: Scombridae) in the western Mediterranean Sea inferred by parasitological analysis. Parasitology 143, 13301339.CrossRefGoogle ScholarPubMed
Melo, FT, Silva, JP, Gonçalves, EC, Furtado, AP, Giese, EG, Santos, CP and Santos, JN (2013) Taxonomic status and redescription of the genus Brasicystis Thatcher, 1979 (Digenea: Didymozoidae). Parasitology International 62, 208214.CrossRefGoogle Scholar
Mladineo, I and Tudor, M (2004) Digenea of Adriatic cage-reared bluefin tuna Thunnus thynnus. Bulletin of the European Association of Fish Pathologists 24, 114153.Google Scholar
Mladineo, I, Bott, NJ, Nowak, BF and Block, BA (2010) Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas. Parasitology 137, 10131025.CrossRefGoogle ScholarPubMed
Mladineo, I, Tomaš, M and Stanić, R (2015) Cross-fertilization as a reproductive strategy in a tissue fluke Didymosulcus katsuwonicola (Platyhelminthes: Didymozoidae) inferred by genetic analysis. Parasitology 142, 14221429.CrossRefGoogle Scholar
Moore, BR, Lestari, P, Cutmore, SC, Proctor, C and Lester, RJG (2019) Movement of juvenile tuna deduced from parasite data. ICES Journal of Marine Science 76, 16781689.CrossRefGoogle Scholar
Munday, BL, Sawada, Y, Cribb, T and Hayward, CJ (2003) Diseases of tunas, Thunnus spp. Journal of Fish Diseases 26, 187206.CrossRefGoogle ScholarPubMed
Nikolaeva, VM (1985) Trematodes – Didymozoidae fauna, distribution and biology. In Hargis, WJ (ed.), NOAA Technical Report NMFS Parasitology and Pathology of Marine Organisms of the World Ocean. Springfield, VA, USA: Department of Commerce, 6772.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle Scholar
Panebianco, A, Giannetto, S and Conte, F (1995) Infestione da Gonapodasmius epinepheli in cernie del Mar Tirreno. Descrizione e considerazioni ispettive. Atti Della Societa’ Italiana Delle Scienze Veterinarie 49, 441442.Google Scholar
Pérez-del-Olmo, A, Kostadinova, A and Gibson, DI (2016) The Mediterranean: high discovery rates for a well-studied trematode fauna. Systematic Parasitology 93(3), 249256.CrossRefGoogle ScholarPubMed
Polinas, M, Mele, S, Padrós, F, Merella, P, Antuofermo, E, Gouraguine, A and Reñones, O (2018) Ecological and histopathological aspects of Didymodiclinus sp. (Trematoda: Didymozoidae) parasite of the dusky grouper, Epinephelus marginatus (Osteichthyes: Serranidae), from the western Mediterranean Sea. Journal of Fish Diseases 41, 13851393.CrossRefGoogle Scholar
Pozdnyakov, SE (1993) The systematics of trematodes of the suborder Didymozoata. Parazitologiya 27, 415425.Google Scholar
Pozdnyakov, SE and Gibson, DI (2008) Family Didymozoidae Monticelli, 1888. In Bray, RA, Gibson, DI and Jones, A (eds), Keys to the Trematoda. Wallingford, UK: CABI Publishing and the Natural History Museum, pp. 631734.Google Scholar
Reimer, LW (1980) Beschreibung des Weibchens eines neuen Didymozoiden: Gonapodasmius microovatus spec. nov. Angewandte Parasitologie 21, 2631.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 15721574.CrossRefGoogle ScholarPubMed
Schrandt, MN, Andres, MJ, Powers, SP and Overstreet, RM (2016) Novel infection site and ecology of cryptic Didymocystis sp. (Trematoda) in the fish Scomberomorus maculatus. Journal of Parasitology 102, 297305.CrossRefGoogle ScholarPubMed
Urabe, M, Nishimura, T and Shimazu, T (2012) Taxonomic revision of three species of the genus Genarchopsis (Digenea: Hemiuroidea: Derogenidae) in Japan by molecular phylogenetic analyses. Parasitology International 61(4), 554560.CrossRefGoogle ScholarPubMed
Vidal-Martínez, VM, Velázquez-Abunader, I, Centeno-Chalé, OA, May-Tec, AL, Soler-Jiménez, LC, Pech, D, Mariño-Tapia, I, Enriquez, C, Zapata-Pérez, O, Herrera-Silveira, J, Hernández-Mena, DI, Herzka, SZ, Ordoñez-López, U and Leopoldina, A-MM (2019) Metazoan parasite infracommunities of the dusky flounder (Syacium papillosum) as bioindicators of environmental conditions in the continental shelf of the Yucatan Peninsula, Mexico. Parasites & Vectors 12(1), 381.CrossRefGoogle ScholarPubMed
Yamaguti, S (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes. I. Japanese Journal of Zoology 5, 249541.Google Scholar
Yamaguti, S (1938) Studies on the helminth fauna of Japan. Part 24. Trematodes of fishes, V. Japanese Journal of Zoology 8, 1517.Google Scholar
Yamaguti, S (1940) Studies on the helminth fauna of Japan. Part 31. Trematodes of fishes, VII. Japanese Journal of Zoology 9, 35108.Google Scholar
Yamaguti, S (1970) Digenetic Trematodes of Hawaiian Fishes. Tokyo, Japan: Keigaku Publishing Co.Google Scholar
Yamaguti, S (1971) Synopsis of Digenetic Trematodes of Vertebrates, vols I and II. Tokyo, Japan: Keigaku Publishing Co., pp. 247277.Google Scholar