Anatomical study of "Onchidella celtica" (Gastropoda, Eupulmonata, Onchidiidae) by micro-computed tomography (micro-CT). A first approach to its applicability in Onchidiidae (Gastropoda, Eupulmonata).
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Abstract
The family Onchidiidae comprises a group of air-breathing marine slugs that can be very abundant in the intertidal zone of temperate shores worldwide. Recently, the phylogeny of the genus Onchidella has been reassessed by means of molecular markers, but anatomical studies are still needed to support these conclusions. In the present work, the anatomy of Onchidella celtica has been studied by using X-ray micro-computed tomography (micro-CT), a non-invasive technique that allows for 2D and 3D imaging of the external and internal anatomy of specimens without irreversible damage. To date, the potential of this technique for the anatomical study of onchidiids had not been assessed yet and therefore a reconstruction of the whole internal anatomy of O. celtica is provided here. Most of the organs and structures were clearly visualized; our observations largely agree with previous descriptions also highlighting the usefulness of micro-CT for the anatomical study of onchidiids.
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ALBA-TERCEDOR, J., & SÁNCHEZ-TOCINO, L. (2011). The use of the SkyScan 1172 high-resolution micro-CT to elucidate if the spicules of the sea slugs (Mollusca: Nudibranchia, Opisthobranchia) have a structural or a defensive function. SkyScan Users Meeting, 2011, 113-121.
BARILLÉ-BOYER, A. L., GRUET, Y., PÉRUSSON, O., & BARILLÉ, L. (2000). Écologie et distribution du mollusque gastropode Onchidella celtica (Cuvier, 1817) sur l'estran rocheux de la Pointe de Saint-Gildas (Loire-Atlantique, France). Bulletinde la Société des sciences naturelles de l'Ouest de la France, 22(3), 123-138.
BINOT, D. (1965). Histologie, histochimie, cytologie de quelques formations glandulaires du tégument d'Oncidiella celtica (Cuv.) (Gastéropode Pulmoné). Cahiers de Biologie Marine, 6, 325-346.
BRITTON, K. M. (1984). The Onchidiacea (Gastropoda, Pulmonata) of Hong Kong with a worldwide review of the genera. Journal of Molluscan Studies, 50(3), 179-191. https://doi.org/10.1093/oxfordjournals.mollus.a065863
CANDÁS, M., DÍAZ-AGRAS, G., & URGORRI, V. (2014). The use of micro-CT for the study of the internal anatomy of sea slugs (Opisthobranchia, Nudibranchia, Dotidae). SkyScan Users Meeting, 2014, 241-243.
CANDÁS, M., DÍAZ-AGRAS, G., ABAD, M., BARRIO, L., CUNHA, X., PEDROUZO, L., SEÑARÍS, M. P., GARCÍA-ÁLVAREZ, Ó., & URGORRI, V. (2016). Application of micro-CT in the study of the anatomy of small marine molluscs. Microscopy and Analysis, 30(2), S8-S11.
CANDÁS, M., DÍAZ-AGRAS, G., GARCÍA-ÁLVAREZ, Ó., & URGORRI, V. (2018). Study of the applicability of micro-CT for identification of Mollusca Solenogastres. In Proceedings of the Bruker Micro-CT User Meeting Abstract Book (pp. 32-40).
CHEMELLO, R., & D’ANNA, G. (1986). Studio preliminare di una popolazione mediterranea di Onchidella celtica (Cuvier, 1817) (Mollusca: Onchidiida). Lavori Società Italiana di Malacologia, 22, 133-144.
DAYRAT, B. (2009). Review of the current knowledge of the systematics of Onchidiidae (Mollusca: Gastropoda: Pulmonata) with a checklist of nominal species. Zootaxa, 2068(1), 1-26. https://doi.org/10.11646/zootaxa.2068.1.1
DAYRAT, B. (2010). Anatomical re-description of the terrestrial onchidiid slug Semperoncis montana (Plate, 1893). Malacologia, 52(1), 1-20. https://doi.org/10.4002/040.052.0101
DAYRAT, B., & GOULDING, T. C. (2017). Systematics of the onchidiid slug Onchidina australis (Mollusca: Gastropoda: Pulmonata). Archiv für Molluskenkunde, 146(1), 121-133. https://doi.org/10.1127/arch.moll/146/121-133
DAYRAT, B., CONRAD, M., BALAYAN, S., WHITE, T. R., ALBRECHT, C., GOLDING, R., GOMES, S. R., HARASEWYCH, M. G. & DE FRIAS MARTINS, A. M. (2011a). Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. Molecular phylogenetics and evolution, 59(2), 425-437. https://doi.org/10.1016/j.ympev.2011.02.014
DAYRAT, B., GOULDING, T. C., APTE, D., ASLAM, S., BOURKE, A., COMENDADOR, J., KHALIL, M., XUÂN, Q. N., TAN, S. H., & TAN, S. H. (2020). Systematic revision of the genus Peronia Fleming, 1822 (Gastropoda, Euthyneura, Pulmonata, Onchidiidae). ZooKeys, 972, 1-224. https://doi.org/10.3897/zookeys.972.52853
DAYRAT, B., GOULDING, T. C., APTE, D., BHAVE, V., COMENDADOR, J., QUA, N. X., TAN, S. K., & TAN, S. H. (2016). Integrative taxonomy of the genus Onchidium Buchannan, 1800 (Mollusca, Gastropoda, Pulmonata, Onchidiidae). ZooKeys, 636, 1-40. https://doi.org/10.3897/zookeys.636.8879
DAYRAT, B., GOULDING, T. C., BOURKE, A. J., KHALIL, M., & TAN, S. H. (2019a). New species and new records of Melayonchis slugs (Gastropoda: Euthyneura: Pulmonata: Onchidiidae). Raffles Bulletin of Zoology, 67, 557-585. https://doi.org/10.26107/RBZ-2019-0043
DAYRAT, B., GOULDING, T. C., KHALIL, M., APTE, D., & TAN, S. H. (2019c). A new species and new records of Onchidium slugs (Gastropoda, Euthyneura, Pulmonata, Onchidiidae) in South-East Asia. ZooKeys, 892, 27-58. https://doi.org/10.3897/zookeys.892.39524
DAYRAT, B., GOULDING, T. C., KHALIL, M., COMENDADOR, J., XUÂN, Q. N., TAN, S. K., & TAN, S. H. (2019b). A new genus of air-breathing marine slugs from South-East Asia (Gastropoda, Pulmonata, Onchidiidae). ZooKeys, 877, 31-80. https://doi.org/10.3897/zookeys.877.36698
DAYRAT, B., GOULDING, T. C., KHALIL, M., DEEPAK, A., BOURKE, A. J., COMENDADOR, J., & TAN, S. (2019d). A new genus and three new species of mangrove slugs from the Indo-West Pacific (Mollusca: Gastropoda: Euthyneura: Onchidiidae). European Journal of Taxonomy, 500, 1-77. https://doi.org/10.5852/ejt.2019.500
DAYRAT, B., GOULDING, T. C., KHALIL, M., LOZOUET, P., & TAN, S. H. (2018). Systematic revision one clade at a time: A new genus of onchidiid slugs from the Indo-West Pacific (Gastropoda: Euthyneura: Pulmonata). Raffles Bulletin of Zoology, 66, 814-837.
DAYRAT, B., ZIMMERMANN, S., & RAPOSA, M. (2011b). Taxonomic revision of the Onchidiidae (Mollusca: Gastropoda: Pulmonata) from the Tropical Eastern Pacific. Journal of Natural History, 45(15-16), 939-1003. https://doi.org/10.1080/00222933.2010.545486
DE WINTER, A. J., & DE GIER, W. (2019). A new Nigerian hunter snail species related to Enneaserrata d’Ailly, 1896 (Gastropoda, Pulmonata, Streptaxidae) with notes on the West African species attributed to Parennea Pilsbry, 1919. ZooKeys, 840, 21-34. https://doi.org/10.3897/zookeys.840.33878
DELLE CHIAJE, S. (1841-1844). Descrizione e notomia degli animali invertebrati della Sicilia citeriore osservati vivi negli anni 1822-1830. Parts 1-8. Batteli & Co., Naples.
EHRLICH, H. (2019). Spicular structures in Molluscs. In Marine Biological Materials of Invertebrate Origin (pp. 133-157). Springer, Cham. https://doi.org/10.1007/978-3-319-92483-0_10
FAULWETTER, S., DAILIANIS, T., VASILEIADOU, A., & ARVANITIDIS, C. (2013). Contrast enhancing techniques for the application of micro-CT in marine biodiversity studies. Microscopy and analysis, 27(2), S4-S7.
FRETTER, V. (1943). Studies in the functional morphology and embryology of Onchidella celtica (Forbes and Hanley) and their bearing on its relationships. Journal of the Marine Biological Association of the United Kingdom, 25(4), 685-720. https://doi.org/10.1017/S0025315400012467
GIGNAC, P.M., KLEY, N.J., CLARKE, J.A., COLBERT, M.W., MORHARDT, A.C., CERIO, D., COST, I.N., COX, P.G., DAZA, J.D., EARLY, C.M., ECHOLS, M.S., HENKELMAN, R.M., HERDINA, A.N., HOLLIDAY, C.M., LI, Z., MAHLOW, K., MERCHANT, S., MÜLLER, J., ORSBON, C.P., PALUH, D.J., THIES, M.L., TSAI, H.P., & WITMER, L.M. (2016). Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy, 228, 889-909. https://doi.org/10.1111/joa.12449
GOLDING, R. E., & JONES, A. S. (2007). Micro-CT as a novel technique for 3D reconstruction of molluscan anatomy. Molluscan Research, 27(3), 123-128.
GOULDING, T. C., BOURKE, A. J., COMENDADOR, J., KHALIL, M., QUANG, N. X., TAN, S. H., TAN, S. K., & DAYRAT, B. (2021). Systematic revision of Platevindex Baker, 1938 (Gastropoda: Euthyneura: Onchidiidae). European Journal of Taxonomy, 737, 1-133. https://doi.org/10.5852/ejt.2021.737.1259
GOULDING, T. C., KHALIL, M., TAN, S. H., & DAYRAT, B. (2018a). A new genus and a new species of onchidiid slugs from eastern Indonesia (Gastropoda: Euthyneura: Onchidiidae). Raffles Bulletin of Zoology, 66, 337-349.
GOULDING, T. C., KHALIL, M., TAN, S. H., & DAYRAT, B. (2018a). Integrative taxonomy of a new and highly-diverse genus of onchidiid slugs from the Coral Triangle (Gastropoda, Pulmonata, Onchidiidae). ZooKeys, 763, 1-111. https://doi.org/10.3897/zookeys.763.21252
GOULDING, T. C., KHALIL, M., TAN, S. H., CUMMING, R. A., & DAYRAT, B. (2022). Global diversification and evolutionary history of onchidiid slugs (Gastropoda, Pulmonata). Molecular Phylogenetics and Evolution, 168, 107360. https://doi.org/10.1016/j.ympev.2021.107360
GOULDING, T. C., TAN, S. H., TAN, S. K., APTE, D., BHAVE, V., NARAYANA, S., SALUNKHE, R., & DAYRAT, B. (2018b). A revision of Peronina Plate, 1893 (Gastropoda: Euthyneura: Onchidiidae) based on mitochondrial and nuclear DNA sequences, morphology and natural history. Invertebrate Systematics, 32(4), 803-826. https://doi.org/10.1071/IS17094
HOFFMANN, K. (1928) Zur Kenntniss der Oncidiiden. Ein Beitrag zur geographischen Verbreitung, Phylogenie und Systematik dieser Tiere. I. Teil. Untersuchung neuen Materials und Revision der Familie. Zoologische Jahrbücher, Systematik Ökologie und Geographie der Tiere, 55, 29-118.
INÄBNIT, T., JOCHUM, A., KAMPSCHULTE, M., MARTELS, G., RUTHENSTEINER, B., SLAPNIK, R., NESSELHAUF, C., & NEUBERT, E. (2019). An integrative taxonomic study reveals carychiid microsnails of the troglobitic genus Zospeum in the Eastern and Dinaric Alps (Gastropoda, Ellobioidea, Carychiinae). Organisms Diversity & Evolution, 19, 135-177. https://doi.org/10.1007/s13127-019-00400-8
JOCHUM, A., PRIETO, C. E., KAMPSCHULTE, M., MARTELS, G., RUTHENSTEINER, B., VRABEC, M., DÖRGE, D. D., & DE WINTER, A. J. (2019). Re-evaluation of Zospeum schaufussi von Frauenfeld, 1862 and Z. suarezi Gittenberger, 1980, including the description of two new Iberian species using Computer Tomography (CT) (Eupulmonata, Ellobioidea, Carychiidae). Zookeys, 4(835), 65-86. https://doi.org/10.3897/zookeys.835.33231
JOCHUM, A., RUTHENSTEINER, B., KAMPSCHULTE, M., MARTELS, G., KNEUBÜHLER, J., & FAVRE, A. (2018). Fulfilling the taxonomic consequence after DNA Barcoding: Carychium panamaense sp. n. (Eupulmonata, Ellobioidea, Carychiidae) from Panama is described using computed tomographic (CT) imaging. ZooKeys, 795, 1-12. https://doi.org/10.3897%2Fzookeys.795.29339
JOCHUM, A., WEIGAND, A. M., BOCHUD, E., INÄBNIT, T., DÖRGE, D.D., RUTHENSTEINER, B., FAVRE, A., MARTELS, G., & KAMPSCHULTE, M. (2017). Three new species of Carychium O.F. Müller, 1773 from the Southeastern USA, Belize and Panama are described using computer tomography (CT) (Eupulmonata, Ellobioidea, Carychiidae). Zookeys, 675, 97-127. https://doi.org/10.3897/zookeys.675.12453
JOYEUX-LAFFUIE, J. (1882). Organisation et développement de l'Oncidie, Oncidium celticum cuv. A. Hennuyer.
KEKLIKOGLOU, K., FAULWETTER, S., CHATZINIKOLAOU, E., WILS, P., BRECKO, J., KVAČEK, J., METSCHER, B., & ARVANITIDIS, C. (2019). Micro-computed tomography for natural history specimens: a handbook of best practice protocols. European Journal of Taxonomy, 522, 1-55. https://doi.org/10.5852/ejt.2019.522
LABBÉ, A. (1933). Les Oncidiadés, Mollusques à silice. Notes des Comptes-Rendus de l’Académie des Sciences, 197, 697-699.
LABBÉ, A. (1934). Opisthobranches et Silicodermés (Oncidiadés). Résultats scientifiques du Voyage aux Indes Orientales Néerlandaises, 2(14), 3-83, pl. I.
MANIEI, F., ESPELAND, M., MOVAHEDI, M., & WAEGELE, H. (2020). Description of a new Peronia species (Gastropoda: Eupulmonata: Onchidiidae) from Iran, Persian Gulf. Zootaxa, 4758(3), 501-531. https://doi.org/10.11646/zootaxa.4758.3.5
MARCONDES MACHADO, F., PASSOS, F. D., & GIRIBET, G. (2019). The use of micro-computed tomography as a minimally invasive tool for anatomical study of bivalves (Mollusca: Bivalvia). Zoological Journal of the Linnean Society, 186(1), 46-75. https://doi.org/10.1093/zoolinnean/zly054
MARCUS, E. D. B. R. (1978). The western Atlantic species of Onchidella (Pulmonata). Sarsia, 63(4), 221-224. https://doi.org/10.1080/00364827.1978.10411343
MARCUS, E. D. B. R. (1979). The Atlantic species of Onchidella (Gastropoda Pulmonata) part 2. Boletim de Zoologia, São Paulo, 4, 1-38.
MARTÍNEZ-SANJUÁN, J., KOCOT, K., GARCÍA-ÁLVAREZ, Ó., CANDÁS, M., & DÍAZ-AGRAS, G. (2022). Computed Microtomography (Micro-CT) in the Anatomical Study and Identification of Solenogastres (Mollusca). Frontiers in Marine Science, 8, 760194. https://doi.org/10.3389/fmars.2021.760194
PARAPAR, J., CANDÁS, M., CUNHA-VEIRA, X., & MOREIRA, J. (2017). Exploring annelid anatomy using micro-computed tomography: A taxonomic approach. Zoologischer Anzeiger, 270, 19-42. https://doi.org/10.1016/j.jcz.2017.09.001
PAZ-SEDANO, S., CANDÁS, M., GOSLINER, T. M., & POLA, M. (2021). Undressing Lophodoris danielsseni (Friele & Hansen, 1878) (Nudibranchia: Goniodorididae). Organisms Diversity & Evolution, 21(1), 107-117. https://doi.org/10.1007/s13127-020-00470-z
PENNEY, B. K., EHRESMANN, K. R., JORDAN, K. J., & RUFO, G. (2020). Micro‐computed tomography of spicule networks in three genera of dorid sea‐slugs (Gastropoda: Nudipleura: Doridina) shows patterns of phylogenetic significance. Acta Zoologica, 101(1), 5-23. https://doi.org/10.1111/azo.12266
PHILIPPI, R.A. (1841). Zoologische Bemerkungen. Archiv für Naturgeschichte, Berlin, 7(1), 42-59.
PLATE, L. VON (1893) Studien über opisthopneumone Lungeschnecken, II, Die Oncidiidien. Zoologische Jahrbücher, Anatomie und Ontogenie der Thiere, 7, 93-234.
ROLÁN, E., SCHMITT, J. O., & ÁLVAREZ, E. R. (1989). Moluscos de la Ría de Vigo: Poliplacoforos, bivalvos, escafopodos, cefalopodos. Universidade de Santiago de Compostela, Servizo de publicacións e intercambio científico.
SEMPER C. 1885. Dritte familie, Onchidiidae. In: Semper, C. (Ed.) Reisen im Archipel der Philippinen, Wissenschaftliche Resultate, III (7). Wiesbaden: C.W. Kreidel; pp. 251-290.
STANTSCHINSKY, W. (1907). Zur Anatomie und Systematik der Gattung Oncidium. Zoologische Jahrbücher, Systematik. Geographie und Biologie der Tiere, 25, 353-402.
TRONCOSO, J. S., & URGORRI, V. (1990). Nuevos datos sobre la distribución de seis especies de moluscos en las costas de Galicia. Iberus, 9(1-2), 247-252.
Tween T.C. (1987) On the occurrence, ecology and behaviour of Onchidella celtica (Gastropoda, Onchidiacea) in the littoral of Cornwall. PhD thesis. University of Bedfordshire, United Kingdom.
URGORRI, V. (1981). Opistobranquiosde Galicia: estudio faunístico y zoográfico. PhD thesis. University of Santiago de Compostela, Spain.
URGORRI, V., SEÑARÍS, M. P., AGRAS, G. J. D., CANDÁS, M., & RODRÍGUEZ, C. G. (2021). Doris adrianae sp. nov. (Heterobranchia; Nudibranchia; Doridina) from the Galician coasts (NW Iberian Peninsula). Nova Acta Científica Compostelana (Bioloxía), 28, 1-33. https://doi.org/10.15304/nacc.id7500
VAILLANT, M. L. (1872). Anatomico-zoological remarks upon Oncidium celticum, Cuvier. Annals and Magazine of Natural History, 9(49), 101-104.
VON WISSEL, K. (1898). Beiträge zur Anatomie der Gattung Oncidiella. Zoologische Jahrbücher, Suppl. 4: 583-640.
WATSON, H. (1925). The South African species of the molluscan genus Onchidella. Annals of the South African Museum, 20, 237-308.
WEISS, K., & WÄGELE, H. (1998). On the morphology, anatomy and histology of three species of Onchidella (Gastropoda: Gymnomorpha: Onchidiida). Archiv für Molluskenkunde, 127, 69-91. http://dx.doi.org/10.1127/arch.moll/127/1998/69
XU, G., YANG, T., WANG, D., LI, J., LIU, X., WU, X., & SHEN, H. (2018). A comprehensive comparison of four species of Onchidiidae provides insights on the morphological and molecular adaptations of invertebrates from shallow seas to wetlands. Plos one, 13(4), e0196252. https://doi.org/10.1371/journal.pone.0196252
ZIEGLER, A., BOCK, C., KETTEN, D. R., MAIR, R. W., MUELLER, S., NAGELMANN, N., PRACHT, E. D., & SCHRÖDER, L. (2018). Digital three-dimensional imaging techniques provide new analytical pathways for malacological research. American Malacological Bulletin, 36(2), 248-273. https://doi.org/10.4003/006.036.0205
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