دورية أكاديمية
Integrative taxonomy of metazoan parasites of the bluntnose sixgill shark Hexanchus griseus (Bonnaterre, 1788) in the Mediterranean Sea, with the resurrection of Grillotia acanthoscolex Rees, 1944 (Cestoda: Trypanorhyncha).
العنوان: | Integrative taxonomy of metazoan parasites of the bluntnose sixgill shark Hexanchus griseus (Bonnaterre, 1788) in the Mediterranean Sea, with the resurrection of Grillotia acanthoscolex Rees, 1944 (Cestoda: Trypanorhyncha). |
---|---|
المؤلفون: | Lopez-Verdejo A; Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Paterna, Spain.; Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Naples, Italy., Palomba M; Department of Biological and Ecological Sciences, University of Tuscia, Viterbo, Italy.; NBFC, National Biodiversity Future Center, Palermo, Italy., Crocetta F; Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Naples, Italy.; NBFC, National Biodiversity Future Center, Palermo, Italy., Santoro M; Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Naples, Italy.; NBFC, National Biodiversity Future Center, Palermo, Italy. |
المصدر: | Journal of fish biology [J Fish Biol] 2024 Jun; Vol. 104 (6), pp. 1754-1763. Date of Electronic Publication: 2024 Mar 07. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Blackwell Publishing Country of Publication: England NLM ID: 0214055 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1095-8649 (Electronic) Linking ISSN: 00221112 NLM ISO Abbreviation: J Fish Biol Subsets: MEDLINE |
أسماء مطبوعة: | Publication: 2003- : Oxford, UK : Blackwell Publishing Original Publication: London, New York, Published for the Fisheries Society of the British Isles by Academic Press. |
مواضيع طبية MeSH: | Sharks*/parasitology , Cestoda*/classification , Phylogeny* , Fish Diseases*/parasitology, Animals ; Mediterranean Sea ; Cestode Infections/veterinary ; Cestode Infections/parasitology ; Italy |
مستخلص: | Appropriate diagnoses of parasites of apex marine predators are crucial to understand their biodiversity, host specificity, biogeography, and life cycles. Such diagnoses are also informative of ecological and biological characteristics of both host and environment in which the hosts and their parasites live. We here (i) investigate the parasite fauna of a bluntnose sixgill shark Hexanchus griseus (Bonnaterre, 1788) obtained from the Gulf of Naples (Tyrrhenian Sea), (ii) characterize molecularly all its metazoan parasites, and (iii) resurrect and report the main morphological features and phylogenetic position of Grillotia acanthoscolex, a cestode species previously synonymized with Grillotia adenoplusia. A rich parasite fauna represented by eight different taxa was found, including two monogeneans (Protocotyle grisea and Protocotyle taschenbergi), one digenean (Otodistomum veliporum), four cestodes (Crossobothrium dohrnii, Clistobothrium sp., G. acanthoscolex, and G. adenoplusia), and one copepod (Protodactylina pamelae). Sequencing of these samples accounts for an important molecular baseline to widen the knowledge on the parasitic fauna of bluntnose sixgill sharks worldwide and to reconstruct their correct food chains. The bluntnose sixgill shark was found to be a definitive host for all endoparasites found here, confirming that it occupies an apex trophic level in the Mediterranean Sea. The taxa composition of the trophic parasite fauna confirms that the bluntnose sixgill shark mostly feeds on teleost fish species. However, the occurrence of two phillobothrid cestodes (C. dohrnii and Clistobothrium sp.) suggests that it also feeds on squids. Finally, we emphasize the importance of using integrative taxonomic approaches in the study of parasites from definitive and intermediate hosts to elucidate biology and ecology of taxa generally understudied in the Mediterranean Sea. (© 2024 Fisheries Society of the British Isles.) |
References: | Beveridge, I., & Campbell, R. A. (2013). A new species of Grillotia Guiart, 1927 (Cestoda: Trypanorhyncha) with redescriptions of congeners and new synonyms. Systematic Parasitology, 85, 99–116. Brinkman, A., Jr. (1988). Presence of Otodistomum sp. metacercariae in Norwegian marine fishes. Sarsia, 73, 79–82. Brooks, D. R., & Hoberg, E. P. (2001). Parasite systematics in the 21st century: Opportunities and obstacles. Trends in Parasitology, 17(6), 273–275. Caira, J. N., Bueno, V., & Jensen, K. (2021). Emerging global novelty in phyllobothriidean tapeworms (Cestoda: Phyllobothriidea) from sharks and skates (Elasmobranchii). Zoological Journal of the Linnean Society, 193(4), 1336–1363. Caira, J. N., Jensen, K., Hayes, C., & Ruhnke, T. R. (2020). Insights from new cestodes of the crocodile shark, Pseudocarcharias kamoharai (Lamniformes: Pseudocarchariidae), prompt expansion of Scyphyophyllidum and formal synonymization of seven phyllobothriidean genera–at last! Journal of Helminthology, 94(e132), 1–25. Celona, A., De Maddalena, A., & Romeo, T. (2005). Bluntnose sixgill shark, Hexanchus griseus (Bonnaterre, 1788), in the eastern north Sicilian waters. Bollettino del Museo Civico di Storia Naturale di Venezia, 56, 137–151. Cerfontaine, P. (1899). Contribution à l'étude des Octocotylidés V ‐ Les Onchocotylinae. Archives de Biologie, 16, 345–478. Chisholm, L. A., Morgan, J. A. T., Adlard, R. D., & Whittington, I. D. (2001). Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology, 31(11), 1253–1263. Cressey, R. F. (1977). Boylea longispica n. g., n. sp., and other parasitic copepods from Pacific fishes. Transactions of the American Microscopical Society, 96(4), 467–476. Dallarés, S., Padrós, F., Cartes, J. E., Solé, M., & Carrassón, M. (2017). The parasite community of the sharks Galeus melastomus, Etmopterus spinax and Centroscymnus coelolepis from the NW Mediterranean deep‐sea in relation to feeding ecology and health condition of the host and environmental gradients and variables. Deep Sea Research Part I: Oceanographic Research Papers, 129, 41–58. Dollfus, R. P. (1969). De quelques cestodes tétrarhynques (hétéracanthes et pécilacanthes) récoltés chez des poisons de la Méditerranée. Vie et Milieu, Série A, 20, 491–542. Dollfus, R. P. (1973). Trematodes de selaciens et de cheloniens. Bulletin du Comité d'Études Historiques et Scientifiques de l'Afrique Occidentale Française, 19, 397–519. Ebert, D. A. (1986). Biological aspects of the sixgill shark. Hexanchus Griseus. Copeia, 1986(1), 131–135. Ebert, D. A., & Dando, M. (2021). Field guide to sharks (p. 384). Princeton University Press, Princeton. Euzet, L., & Maillard, C. (1974). Les monogènes Hexabothriidae Price, 1942. Historique, systématique, phylogenèse. Bulletin du Muséum National d'Histoire Naturelle, 206, 113–141. Gibson, D. I. (1976a). Monogenea and Digenea from fishes. Discovery Reports, 36, 179–266. Gibson, D. I. (1976b). The Otodistomum veliporum – cestoides problem. Norwegian Journal of Zoology, 24(4), 468. Hewitt, G. C., & Hine, P. M. (1972). Checklist of parasites of New Zealand fishes and of their hosts. New Zealand Journal of Marine and Freshwater Research, 6(1–2), 69–114. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755. Huys, R., Llewellyn‐Hughes, J., Conroy‐Dalton, S., Olson, P. D., Spinks, J. N., & Johnston, D. A. (2007). Extraordinary host switching in siphonostomatoid copepods and the demise of the Monstrilloida: Integrating molecular data, ontogeny and antennulary morphology. Molecular Phylogenetics and Evolution, 43, 368–378. Isbert, W., Dallarés, S., Grau, A., Petrou, A., García‐Ruiz, C., Guijarro, B., Jung, A., & Catanese, G. (2023). A molecular and epidemiological study of Grillotia (Cestoda: Trypanorhyncha) larval infection in Etmopterus spinax (Elasmobranchii: Squaliformes) in the Mediterranean Sea and Northeast Atlantic Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 199, 104102. Justine, J. L. (2011). Protocotyle euzetmaillardi n. sp. (Monogenea: Hexabothriidae) from the bigeye sixgill shark Hexanchus nakamurai Teng (Elasmobranchii: Hexanchidae) off New Caledonia. Systematic Parasitology, 78(1), 41–55. Kheddam, H., Justine, J. L., & Tazerouti, F. (2016). Hexabothriid monogeneans from the gills of deep‐sea sharks off Algeria, with the description of Squalonchocotyle euzeti n. sp (Hexabothriidae) from the kitefin shark Dalatias licha (Euselachii, Dalatiidae). Helminthologia, 53(4), 354–362. Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGAX: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and clustal X version 20. Bioinformatics, 23(21), 2947–2948. Laubier, L. (1966). Crustacea Copepoda. Vie et Milieu, 17(3A), 1217–1233. Laubier, L., Maillard, C., & Oliver, G. (1966). Contribution a l'étude des parasites du ‘Griset’: Hexanchus griseus (Bonnaterre, 1788). Vie et Milieu, Série A: Biologie Marine, 17(3A), 1197–1233. Littlewood, D. T. J., & Olson, P. D. (2001). Small subunit rDNA and the Platyhelminthes: Signal, noise, conflict and compromise. In D. T. J. Littlewood & R. A. Bray (Eds.), Interrelationships of the Platyhelminthes (pp. 262–278). CRC Press. Merlo‐Serna, A. I., & Garcia‐Prieto, L. (2016). A checklist of helminth parasites of Elasmobranchii in Mexico. ZooKeys, 563, 73–128. Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T. L., Agarwala, R., & Schaffer, A. A. (2008). Database indexing for production MegaBLAST searches. Bioinformatics, 24(16), 1757–1764. Olson, P. D., & Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology, 60, 165–243. Olsson, P. (1876). Bidrag till skandinaviens Helminthfauna. Kongl. Svenska Vetenskaps–Akademiens Handlingar, 14(1), 1–35. Palm, H. W. (2004). The Trypanorhyncha Diesing, 1863 (p. 710). PKSPL‐IPB Press. Palm, H. W., Waeschenbach, A., Olson, P. D., & Littlewood, D. T. J. (2009). Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution, 52(2), 351–367. Palomba, M., Marchiori, E., Tedesco, P., Fioravanti, M., Marcer, F., Gustinelli, A., Aco‐Alburqueque, R., Belli, B., Canestrelli, D., Santoro, M., Cipriani, P., & Mattiucci, S. (2023). An update and ecological perspective on certain sentinel helminth endoparasites within the Mediterranean Sea. Parasitology, 150(12), 1139–1157. Pérez‐del‐Olmo, A., Georgieva, S., Dallarés, S., Constenla, M., Kostadinova, A., & Carrassón, M. (2023). Linking integrative taxonomy and ecology: Diversity and population structure of two platyhelminth parasites (Digenea: Lepidapedidae) of sympatric deep‐sea fishes in the Western Mediterranean. Deep Sea Research Part I, 192, 103948. Pintner, T. (1903). Studien über tetrarhynchen nebst beobachtungen an anderen bandwürmern. III. Mitteilung. Zwei eigentümliche drüsensystem bei Rhynchobothrium adenoplusius n. und histologische notizen über Anthocephalus, Amphilina und Taenia saginata. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften, Mathematisch‐Naturwissenschaftliche Klasse, Abt, 1(122), 541–597. Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25(7), 1253–1256. Posada, D., & Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: Advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53(5), 793–808. Poulin, R., Hay, E., & Jorge, F. (2019). Taxonomic and geographic bias in the genetic study of helminth parasites. International Journal for Parasitology, 49(6), 429–435. Rees, G. (1944). A new cestode of the genus Grillotia from a shark. Parasitology, 35, 180–185. Ruszkowski, J. S. (1934). Etudes sur le cycle évolutif et sur la structure des cestodes de mer. III‐e partie. Le cycle évolutif du tétrarhynque Grillotia erinaceus (Van Beneden 1858). Mémoires de l'Académie Polonaise Des Sciences, Série B, 6, 1–9. Santoro, M., Bellisario, B., Crocetta, F., Uberti, B. D., & Palomba, M. (2021). A molecular and ecological study of Grillotia (Cestoda: Trypanorhyncha) larval infection in small to mid‐sized benthonic sharks in the Gulf of Naples, Mediterranean Sea. Ecology and Evolution, 11(20), 13744–13755. Santoro, M., Bellisario, B., Fernández‐Álvarez, F. Á., Crocetta, F., & Palomba, M. (2023). Parasites and prey of the nursehound shark Scyliorhinus stellaris (Linnaeus, 1758): Insights into hidden trophic web interactions in the Mediterranean Sea. Journal of Fish Biology, 102(1), 271–280. Santoro, M., Bellisario, B., Tanduo, V., Crocetta, F., & Palomba, M. (2022). Drivers of parasite communities in three sympatric benthic sharks in the Gulf of Naples (central Mediterranean Sea). Scientific Reports, 12(1), 9969. Santoro, M., Iaccarino, D., & Bellisario, B. (2020). Host biological factors and geographic locality influence predictors of parasite communities in sympatric sparid fishes off the southern Italian coast. Scientific Reports, 10, 13283. Santoro, M., Palomba, M., Alburqueque, R. A., & Mattiucci, S. (2022). Integrative taxonomy reveals Molicola uncinatus and Gymnorhynchus gigas (Cestoda: Trypanorhyncha) coinfection in the Atlantic pomfret Brama brama from the Mediterranean Sea, with notes on the phylogenetic position of G. Gigas within the family Gymnorhynchidae. Frontiers in Veterinary Science, 9, 909163. Santoro, M., Uberti, B. D., Corrado, F., Cutarelli, A., Iaccarino, D., Di Nocera, F., D'Amore, M., De Luca, G., Cerrone, A., Capuano, F., & Galiero, G. (2018). Grillotia (Cestoda: Trypanorhyncha) plerocerci in an anglerfish (Lophius piscatorius) from the Tyrrhenian Sea. Parasitology Research, 117(11), 3653–3658. Sinnappah, N. D., Lim, L. H. S., Rohde, K., Tinsley, R., Combes, C., & Verneau, O. (2001). A paedomorphic parasite associated with a neotenic amphibian host: Phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Molecular Phylogenetics and Evolution, 18(2), 189–201. Sproston, N. G. (1946). A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London, 25, 185–600. Van der Auwera, G., Chapelle, S., & De Wachter, R. (1994). Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Letters, 338(2), 133–136. Williams, H. H. (1968). The taxonomy, ecology and host‐specificity of some Phyllobothriidae (Cestoda: Tetraphyllidea), a critical revision of Phyllobothrium Beneden, 1849 and comments on some allied genera. Philosophical Transactions of the Royal Society B: Biological Sciences, 253(786), 231–307. |
معلومات مُعتمدة: | National Biodiversity Future Centre (NBFC) Program; Italian Ministry of University and Research; PNRR; CN00000033 Missione 4 Componente 2 Investimento 1.4 |
فهرسة مساهمة: | Keywords: Trypanorhyncha; cestodes; copepods; host specificity; molecular characterization; monogeneans; trematodes |
تواريخ الأحداث: | Date Created: 20240307 Date Completed: 20240626 Latest Revision: 20240626 |
رمز التحديث: | 20240627 |
DOI: | 10.1111/jfb.15703 |
PMID: | 38450741 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1095-8649 |
---|---|
DOI: | 10.1111/jfb.15703 |