Abstract
The sponge class Homoscleromorpha has a challenging taxonomy and its systematics is still a matter of debate. A significant effort has recently been deployed to better evaluate the diversity of these sponges, and each new exploration of cryptic habitats reveals new species. Although several undescribed or wrongly determined Oscarella-like sponges have been reported by different authors, the Oscarellidae family still lacks description of its true Caribbean representatives. The exploration of various submarine caves in the Lesser Antilles has allowed us to find and to formally describe the first two Oscarellidae of the Caribbean Sea, Oscarella filipoi sp. nov. and Oscarella zoranja sp. nov. Both new species are quite common in semi-dark habitats throughout the Lesser Antilles. Moreover, O. filipoi sp. nov. is the largest Oscarellidae ever observed world-wide. Both species harbor a sylleibid aquiferous system and a high density of ovoid to spherical choanocyte chambers. The molecular taxonomy clearly shows their affiliation to the Oscarella clade containing the type species of the Oscarellidae family. In addition to their growth forms, these two species differ in the shape of their mesohylar cells, and in the degree of development of their basal region. This latter trait is particularly remarkable in large specimens of O. filipoi which can have a very thick ectosome.
References
Bergquist, P.R. (1978) Sponges. Hutchinson & Co (Publishers) Ltd, London, 268 pp.
Boury-Esnault, N., Solé-Cava, A.M. & Thorpe, J.P. (1992) Genetic and cytological divergence between colour morphs of the Mediterranean sponge Oscarella lobularis Schmidt (Porifera, Demospongiae, Oscarellidae). Journal of Natural History, 26 (2), 271–284.
https://doi.org/10.1080/00222939200770131
Boury-Esnault, N., De Vos, L., Donadey, C. & Vacelet, J. (1984) Comparative study of the choanosome of Porifera: 1. The Homoscleromorpha. Journal of Morphology, 180 (1), 3–17.
https://doi.org/10.1002/jmor.1051800103
Boury-Esnault, N., Muricy, G., Gallissian, M.F. & Vacelet, J. (1995) Sponges without skeleton: A new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia, 43 (1), 25–43.
https://doi.org/10.1080/00785326.1995.10430575
Boury-Esnault, N., Lavrov, D.V., Ruiz, C.A. & Pérez, T. (2013) The Integrative Taxonomic Approach Applied to Porifera: A Case Study of the Homoscleromorpha. Integrative and Comparative Biology, 53 (3), 416–427.
https://doi.org/10.1093/icb/ict042
Cárdenas, P., Pérez, T. & Boury-Esnault, N. (2012) Sponge Systematics Facing New Challenges. Advances in Marine Biology, 61, 79–209.
https://doi.org/10.1016/B978-0-12-387787-1.00010-6
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772–772.
https://doi.org/10.1038/nmeth.2109
Dendy, A. (1905) Report on the sponges collected by Professor Herdman at Ceylon, in 1902. Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar, 3, 57–246.
Ereskovsky, A.V., Ivanišević, J. & Perez, T. (2009a) Overview of the Homoscleromorpha sponges diversity in the Mediterranean. Available from: https://www.researchgate.net/publication/257527355_Overview_of_the_Homoscleromorpha_sponges_diversity_in_the_Mediterranean (accessed 7 December 2017)
Ereskovsky, A.V., Sanamyan, K. & Vishnyakov, A.E. (2009b) A new species of the genus Oscarella (Porifera: Homosclerophorida: Plakinidae) from the North-West Pacific. Cahiers de Biologie Marine, 50, 369–381. Available from: https://www.researchgate.net/publication/235891161_A_new_species_of_the_genus_Oscarella_Porifera_Homoscleropho
rida_Plakinidae_from_the_North-West_Pacific (accessed 7 December 2017)Ereskovsky, A.V., Lavrov, D.V. & Willenz, P. (2014) Five new species of Homoscleromorpha (Porifera) from the Caribbean Sea and re-description of Plakina jamaicensis. Journal of the Marine Biological Association of the United Kingdom, 94 (2), 285–307.
https://doi.org/10.1017/S0025315413000295
Erpenbeck, D., Hooper, J.N.A. & Worheide, G. (2006) CO1 phylogenies in diploblasts and the ‘Barcoding of Life’ — are we sequencing a suboptimal partition? Molecular Ecology Notes, 6 (2), 550–553.
https://doi.org/10.1111/j.1471-8286.2005.01259.x
Fauvelot, C. (2015) PACOTILLES-1 cruise, RV Antea.
http://dx.doi.org/10.17600/15005200
Gazave, E., Lapébie, P., Renard, E., Vacelet, J., Rocher, C., Ereskovsky, A.V., Lavrov, D.V. & Borchiellini, C. (2010) Molecular Phylogeny Restores the Supra-Generic Subdivision of Homoscleromorph Sponges (Porifera, Homoscleromorpha) PLOS ONE, 5, e14290.
https://doi.org/10.1371/journal.pone.0014290
Gazave, E., Lapébie, P., Ereskovsky, A.V., Vacelet, J., Renard, E., Cárdenas, P. & Borchiellini, C. (2012) No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia, 687 (1), 3–10.
https://doi.org/10.1007/s10750-011-0842-x
Gerovasileiou, V. & Voultsiadou, E. (2012) Marine Caves of the Mediterranean Sea: A Sponge Biodiversity Reservoir within a Biodiversity Hotspot. PLOS ONE, 7, e39873.
https://doi.org/10.1371/journal.pone.0039873
Gray, J. (1873) Notes on mud-tortoises (Trionyx Geoffroy), and on the skulls of the different kinds. Proceedings of the Zoological Society of London, 1873, 38–72.
Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321.
https://doi.org/10.1093/sysbio/syq010
Hall, T. (1999) BioEdit, a user-friendly biological alignement editor and analysis program for Windows 95/98/NT. Nucleic Symposium Series, 41, 95–98. Available from: http://brownlab.mbio.ncsu.edu/JWB/papers/1999Hall1.pdf (accessed 7 December 2017)
Ivanišević, J., Thomas, O.P., Lejeusne, C., Chevaldonné, P. & Pérez, T. (2011) Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics, 7 (2), 289–304.
https://doi.org/10.1007/s11306-010-0239-2
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, G.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. & others (2007) ClustalW and ClustalX version 2. Bioinformatics, 23 (21), 2947–2948.
https://doi.org/10.1093/bioinformatics/btm404
Lendenfeld, R. (1887) On the Systematic position and classification of Sponges. Proceedings of the Zoological Society of London, 1886, 558–662.
Misof, B., Erpenbeck, D. & Sauer, K.P. (2000) Mitochondrial gene fragments suggest paraphyly of the genus Panorpa (Mecoptera, Panorpidae). Molecular Phylogenetics and Evolution, 17 (1), 76–84.
https://doi.org/10.1006/mpev.2000.0817
Muricy, G., Boury-Esnault, N., Bézac, C. & Vacelet, J. (1996) Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Canadian Journal of Zoology 74 (5), 881–896.
https://doi.org/10.1139/z96-102
Muricy, G. & Díaz, M.C. (2002) Order Homosclerophorida Dendy, 1905, Family Plakinidae Schulze, 1880. In: Hooper, J.N.A & Van Soest, R.W.M. (Eds.), Systema Porifera: a guide to the classification of Sponges. Kluwer Academic/Plenum Publishers, New York, pp. 71–82.
https://doi.org/10.1007/978-1-4615-0747-5_6
Pérez, T., Ivanišević, J., Dubois, M., Pedel, L., Thomas, O.P., Tokina, D. & Ereskovsky, A.V. (2011) Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: cytological description, reproductive cycle and ecology. Marine Ecology, 32 (2), 174–187.
https://doi.org/10.1111/j.1439-0485.2011.00435.x
Pérez, T. (2015) PACOTILLES-2 cruise, RV Antea.
http://dx.doi.org/10.17600/15005300
Pérez, T., Díaz, M.C., Ruiz, C., Cóndor-Luján, B., Klautau, M., Hajdu, E., Lobo-Hajdu, G., Zea, S., Pomponi, S.A., Thacker, R.W., Carteron, S., Tollu, G., Pouget-Cuvelier, A., Thélamon, P., Marechal, J.P., Thomas, O.P., Ereskovsky, A.V., Vacelet, J. & Boury-Esnault, N. (2017) How a collaborative integrated taxonomic effort has trained new spongiologists and improved knowledge of Martinique Island (French Antilles, eastern Caribbean Sea) marine biodiversity. PLOS ONE 12 (3), e0173859.
https://doi.org/10.1371/journal.pone.0173859
Ruiz, C., Ivanišević, J., Chevaldonné, P., Ereskovsky, A.V., Boury-Esnault, N., Vacelet, J., Thomas, O.P. & Pérez, T. (2015) Integrative taxonomic description of Plakina kanaky, a new polychromatic sponge species from New Caledonia (Porifera: Homoscleromorpha). Marine Ecology, 36 (4), 1129–1143.
https://doi.org/10.1111/maec.12209
Ruiz, C., Muricy, G., Lage, A., Domingos, C., Chenesseau, S. & Pérez, T. (2017) Descriptions of new sponge species and genus, including aspiculate Plakinidae, overturn the Homoscleromorpha classification. Zoological Journal of the Linnean Society, 179 (4), 707–724.
https://doi.org/10.1111/zoj.12480
Schmidt, O. (1862) Die Spongien des adriatischen Meeres. Wilhelm Engelmann, Leipzig, 88 pp.
Schmidt, O. (1868) Die Spongien der Küste von Algier. Mit Nachträgen zu den Spongien des Adriatischen Meeres (Drittes Supplement). Wilhelm Engelmann, Leipzig, pp. 1–44.
Schmidt, O. (1870) Grundzüge einer Spongien-Fauna des atlantischen Gebietes. Wilhelm Engelmann, Leipzig, 88 pp.
Ternon, E., Zarate, L., Chenesseau, S., Croué, J., Dumollard, R., Suzuki, M.T. & Thomas, O.P. (2016) Spherulization as a process for the exudation of chemical cues by the encrusting sponge Crambe crambe. Scientific reports, 6, 1–11.
https://doi.org/10.1038/srep29474
Topsent, E. (1895) Etude monographique des spongiaires de France. II Carnosa. Archives de Zoologie Expérimentale et Générale, 3, 493–590.
Topsent, E. (1896) Matériaux pour servir à l’étude de la faune des spongiaires de France. Mémoires de la Société Zoologique de France, 9, 113–133.
Turon, X., Becerro, M.A. & Uriz, M.J. (2000) Distribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques. Cell and Tissue Research, 301 (2), 311–322.
https://doi.org/10.1007/s004410000233
Tuzet, O. & Paris, J. (1963) Octavella galangaui n.g n.sp. Demospongiae, Oscarellidae de Banyuls-sur-Mer. Vie et Milieu, 1, 71–89.
Vacelet, J. (1998) Les éponges. In: Quéro, J., Arzel, P., Dardignac, M.J., Latrouite, D., Veron, G. & Vayne, J. (Eds.), Les fruits de la mer et plantes des pêches françaises. Delachaux & Niestle, Paris, pp. 49–54.
Van Soest, R.W.M., Boury-Esnault, N., Hooper, J.N.A., Rützler, K., de Voogd, N.J., Alvarez de Glasby, B., Hajdu, E., Pisera, A.B., Manconi, R., Schoenberg, C., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.C., Cárdenas, P., Carballo, J.L. & Rios Lopez, P. (2017) World Porifera database. Available from: http://www.marinespecies.org/porifera (accessed 10 Feburary 2017)
Vacelet, J. & Pérez, T. (1998) Two new genera and species of sponges (Porifera, Demospongiae) without skeleton from a Mediterranean cave. Zoosystema, 20 (1), 5–22.
Vosmaer, G.C.J. (1881) Über Leucandra aspera H. nebst allgemeinen Bemerkungen über das Canalsystem der Spongien. Tijdschrift der Nederlandsche Dierkundige Vereeniging, 5, 144–166.
Vosmaer, G.C.J. (1884) Porifera. In: Bronn, H.G. (Ed.), Die Klassen und Ordnungen des Thierreichs, Volume II. C.F. Winter, Leipzig, pp. 65–176.