Abstract
The species diversity of Lepidapedon Stafford, 1904 (Lepidapediae) in the Western Mediterranean was assessed based on samples from five deep-sea gadiform fishes collected between the Balearic Islands and the Catalonian coast of Spain: Lepidion lepidion (Risso) and Mora moro (Risso) (both Moridae); Coelorinchus mediterraneus Iwamoto & Ungaro and Trachyrincus scabrus (Rafinesque) (both Macrouridae); and Phycis blennoides (Brünnich) (Phycidae). Integration of morphological and molecular evidence (28S rRNA gene and the mitochondrial nad1 gene) revealed that the deep-sea fishes in the Western Mediterranean share two species of Lepidapedon. Lepidapedon desclersae Bray & Gibson, 1995 was recovered in all five fish species of three families [Moridae (L. lepidion and M. moro); Macrouridae (C. mediterraneus and T. scabrus); and Phycidae (P. blennoides)] and L. guevarai Lopez-Roman & Maillard, 1973 was recovered in three fish species of three families [Phycidae (P. blennoides); Macrouridae (T. scabrus); and Moridae (L. lepidion)]. Therefore, both species are considered to be euryxenic but restricted to gadiforms. The voucher material for the two species from different fish hosts is described in detail and the host-related variability based on the morphometric data is assessed.
Similar content being viewed by others
References
Blend, C. K., Dronen, N. O., & Armstrong, H. W. (2000). Six new species of Lepidapedon Stafford, 1904 (Digenea: Lepocreadiidae) from deep-sea macrourid fishes from the Gulf of Mexico and Caribbean Sea, with revised keys to the species of the genus. Systematic Parasitology, 45, 29–51.
Bray, R. A., & Cribb, T. H. (2012). Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Systematic Parasitology, 83, 169–177.
Bray, R. A., & des Clers, S. A. (1992). Multivariate analyses of metrical features in the Lepidapedon elongatum (Lebour, 1908) species-complex (Digenea: Lepocreadiidae) in deep and shallow water gadiform fishes of the NE Atlantic. Systematic Parasitology, 21, 223–232.
Bray, R. A., Faliex, E., Allienne, J. F., & Mouahid, G. (2013). Lepidapedon sereti n. sp. (Digenea: Lepidapedidae) in Coelorinchus sereti (Gadiformes: Macrouridae) from deep waters off Vanuatu. Parasitology Research, 112, 3981–3989.
Bray, R. A., & Gibson, D. I. (1990). The Lepocreadiidae (Digenea) of fishes of the north-east Atlantic: review of the genera Opechona Looss, 1907 and Prodistomum Linton, 1910. Systematic Parasitology, 15, 159–202.
Bray, R. A., & Gibson, D. I. (1995). The Lepocreadiidae (Digenea) of fishes of the north-east Atlantic: a review of the genus Lepidapedon Stafford, 1904. Systematic Parasitology, 31, 81–132.
Bray, R. A., & Gibson, D. I. (1997). The Lepocreadiidae Odhner, 1905 (Digenea) of fishes from the north-east Atlantic: summary paper, with keys and checklists. Systematic Parasitology, 36, 223–228.
Bray, R. A., Littlewood, D. T. J., Herniou, E. A., Williams, B., & Henderson, R. E. (1999). Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology, 119 (Supplement), S125–S144.
Bray, R. A., Waeschenbach, A., Cribb, T. H., Weedall, G. D., Dyall, P., & Littlewood, D. T. J. (2009). The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitologica, 54, 310–329.
Constenla, M., Montero, F. E., Padrós, F., Cartes, J. E., Papiol, V., & Carrassón, M. (2015). Annual variation of parasite communities of deep-sea macrourid fishes from the western Mediterranean Sea and their relationship with fish diet and histopathological alterations. Deep-Sea Research Part I, 104, 106–121.
Dallarés, S., Georgieva, S., Kostadinova, A., Carrassón, M., Gibson, D., & Pérez-del-Olmo, A. (2013). Morphometric and molecular characterisation of specimens of Lepidapedon Stafford, 1904 (Digenea: Lepidapedidae) from deep-sea fish Mora moro (Risso) (Teleostei: Moridae) in the western Mediterranean. Systematic Parasitology, 85, 243–253.
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
Dolgikh, A. V., & Naidenova, N. N. (1967). [Some studies on the helminth fauna of the sea bream (Diplodus annularis L.).] Nauchnye Doklady Vysshei Shkoli. Biologicheskie Nauki, 11, 13–16 (In Russian).
Gaevskaya, A. V. (1990). Lepidapedon elongatum (Trematoda, Lepocreadiidae) - an erroneously identified parasite of the Black Sea mackerel. Vestnik Zoologii, 4, 66–67 (In Russian).
Gaevskaya, A. V. (1995). Lepidapedon cambrensis (Trematoda: Lepocreadiidae) parasite of the Atlantic Ocean fishes. Parazitologiya, 29, 26–29 (In Russian).
Gaevskaya, A. V., & Mordvinova, T. N. (1996). On changes in taxonomic status of the trematode species Lepidapedon carcini Mordvinova, 1985. Vestnik Zoologii, 1–2, 51 (In Russian).
Galtier, N., Gouy, M., & Gautier, C. (1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications & Biosciences, 12, 543–548.
Georgieva, S., Pérez-del-Olmo, A., Dallarés, S., Constenla, M., Kostadinova, A., & Carrassón, M. (2015). Molecules for ecology: Diversity and distribution of Lepidapedon spp. in deep-sea fishes of the Western Mediterranean. In: 9th International Symposium on Fish Parasites, Valencia, 2015, p. 29.
Huelsenbeck, J. P., Ronquist, F., Nielsen, R., & Bollback, J. P. (2001). Bayesian Inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.
Jardas, I., & Hristovski, N. (1985). A new contribution to the knowledge of helminth parasite fauna of fishes from the channels between the mid-Dalmation Islands, Adriatic Sea. Acta Adriatica, 26, 145–164.
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology & Evolution, 30, 772–780.
Kovaleva, A. A. (1963). Helminth fauna of large horse mackerel in the Black Sea. Materialy Nauchnoi Konferentsii Vsesoyuznogo Obshchestva Germintologov, 1, 140–141 (In Russian).
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology & Evolution, 33, 1870–1874.
Littlewood, D. T. J., Curini-Galletti, M., & Herniou, E. A. (2000). The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics & Evolution, 16, 449–466.
Lockyer, A. E., Olson, P. D., & Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.
Lopez-Roman, R., & Maillard, C. (1973). Lepidapedon (Lepidapedon) guevarai n. sp. (Digenea Lepocreadiidae) parasito de Phycis blennoides (Briinnich) (Gadidae). Revista lbérica de Parasitologia, 33, 617–624.
Mateu, P., Montero, F. E., & Carrasón, M. (2014). Geographical variation in metazoan parasites of the deep-sea fish Bathypterois mediterraneus Bauchot, 1962 (Osteichthyes: Ipnopidae) from the Western Mediterranean. Deep-Sea Research Part I, 87, 24–29.
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, pp. 1–8.
Mordvinova, T. N. (1985). Helminth fauna of certain species of the Black Sea highest Crustacea class. Ekologiya Morya, 20, 50–58 (In Russian).
Morgan, J. A., & Blair, D. (1998). Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. International Journal for Parasitology, 28, 493–502.
Nikolaeva, V. M., & Kovaleva, A. A. (1966). [Parasite fauna of Trachurus from the Mediterranean Basin.] Delyamure, S. L. (Ed.) [Helminth fauna of animals in southern seas.] Kiev: Naukova Dumka, pp. 67–79 (In Russian).
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.
Orecchia, P., & Paggi, L. (1978). Aspetti di sistematica e di ecologia degli elminti parassiti di pesci marini studiati presso l’Istituto di Parassitologia Roma. Parassitologia, 20, 73–89.
Pérez-i-García, D., Constenla, M., Padrós, F., Soler-Membrives, A., Sole, M., & Carrasson, M. (2015). Parasite communities of the deep-sea fish Alepocephalus rostratus Risso, 1820 in the Balearic Sea (NW Mediterranean) along the slope and relationships with enzymatic biomarkers and health indicators. Deep-Sea Research Part I, 99, 65–74.
Pérez-i-García, D., Constenla, M., Soler-Membrives, A., Cartes, J. E., Sole, M., & Carrasson, M. (2017). Natural variability of parasite communities of Macrouridae of the middle and lower slope of the Mediterranean Sea and their relation with fish diet and health indicators. Deep-Sea Research Part I, 124, 1–17.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
Sey, O. (1970). Parasitic helminths occurring in Adriatic fishes. Part II. (Flukes and tapeworms). Acta Adriatica, 8, 3–15.
Telford, M. J., Herniou, E. A., Russell, R. B., & Littlewood, D. T. J. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. Proceedings of the National Academy of Sciences of the USA, 97, 11359–11364.
Tkach, V. V., Littlewood, D. T. J., Olson, P. D., Kinsella, J. M., & Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology, 56, 1–15.
Acknowledgements
We thank two anonymous reviewers for their constructive comments.
Funding
This study was supported by the Spanish Ministry of Science and Innovation (MICINN) projects (ANTROMARE CTM2009-12214-C02-02 to MCa, MCo, SD and APDO and AGL2015-68405-R to APDO), the Czech Science Foundation (project P505/12/G112 to AK, APDO and SG) and Valencian Local Government (PROMETEO 2015-018 to APDO). SG benefited from a postdoctoral fellowship ‘Juan de la Cierva-Formaciónʼ of the MICINN (FJCI-2016-29535), Spain.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable institutional, national and international guidelines for the care and use of animals were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection Digenea.
Rights and permissions
About this article
Cite this article
Pérez-del-Olmo, A., Dallarés, S., Georgieva, S. et al. Species of Lepidapedon Stafford, 1904 (Digenea: Lepidapedidae) from deep-sea fishes in the Western Mediterranean: molecular and morphological evidence. Syst Parasitol 96, 149–169 (2019). https://doi.org/10.1007/s11230-019-09845-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11230-019-09845-z