Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-10-27
Page range: 128-148
Abstract views: 337
PDF downloaded: 52

NEW SKELETON-LESS HOMOSCLEROMORPHS (PORIFERA, HOMOSCLEROMORPHA) FROM THE CARIBBEAN SEA: EXCEPTIONS TO RULES ARE DEFINITELY COMMON IN SPONGE TAXONOMY

Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale, UMR 7263 CNRS, Aix Marseille Université, IRD, Avignon Université, Station Marine d’Endoume, Chemin de la Batterie des Lions, 13007, Marseille, France.
Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale, UMR 7263 CNRS, Aix Marseille Université, IRD, Avignon Université, Station Marine d’Endoume, Chemin de la Batterie des Lions, 13007, Marseille, France. Faculty of Biology, Saint-Petersburg State University, Universitetskaya emb. 7/9, 199034, Saint-Petersburg, Russia
Institut Méditerranéen de Biodiversité et d’Ecologie marine et continentale, UMR 7263 CNRS, Aix Marseille Université, IRD, Avignon Université, Station Marine d’Endoume, Chemin de la Batterie des Lions, 13007, Marseille, France.
PORIFERA Sponge Biodiversity Caribbean Sea Submarine caves Integrative Taxonomy

Abstract

Currently composed of only one order and two families, the class Homoscleromorpha has undergone significant changes in its systematics over the past 20 years. We combined morphological, cytological and molecular (CO1) data to describe three new aspiculate Homoscleromorpha, two Plakinidae and one Oscarellidae. These three sponges live in the dark submarine caves of the Lesser Antilles (Caribbean Sea). Aspiculortis gen. nov. is part of a clade including spiculate Plakortis species. Aspiculortis garifuna gen. nov. sp. nov. is characterized by an original pseudo criblate smooth surface, with a network of translucent canals ending in prominent oscula, and by one type of vacuolar cell concentrated in the ectosome. Aspiculophora papillata sp. nov. is characterized by a papillate surface, a morphological trait that is recorded for the first time among Homoscleromorpha, and one abundant type of vacuolar cell randomly distributed in the mesohyl. Oscarella minka sp. nov. is characterized by a smooth surface and two types of vacuolar cells, one principally found in the ectosome, and a second type which is randomly distributed and which harbors original inclusions. These three new Homoscleromorpha present an abundant microbial community in their mesohyl. After this work, the skeleton-less representatives of this sponge class include four species of Plakinidae belonging to three different genera, and all Oscarellidae described so far. The putative absence of skeleton underlines the need of more cytological descriptions of Plakinidae representatives.

 

References

  1. Bergquist, P.R. (1978) Sponges. Hutchinson, London, 268 pp.
    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., 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., Muricy, G., Gallissian, M. & Vacelet, J. (1995) Sponges without skeleton: A new mediterranean genus of Homoscleromopha (Porifera, Demospongiae). Ophelia, 43 (1), 25–43. https://doi.org/10.1080/00785326.1995.10430575
    Boury-Esnault, N., Lavrov, D.V., Ruiz, C. & 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
    Carter, H. (1879) Mr. H.J Carter´s contribution. s.n., s.n., 44 pp.
    Cedro, V.R., Hajdu, E. & Correia, M.D. (2013) Three new intertidal sponges (Porifera: Demospongiae) from Brazil’s fringing urban reefs (Maceió, Alagoas, Brazil), and support for Rhabderemia ’s exclusion from Poecilosclerida. Journal of Natural History, 47, 2151–2174. https://doi.org/10.1080/00222933.2013.792962
    Cruz-Barraza, J.A., Vega, C. & Carballo, J.L. (2014) Taxonomy of family Plakinidae (Porifera: Homoscleromorpha) from eastern Pacific coral reefs, through morphology and cox1 and cob mtDNA data. Zoological Journal of the Linnean Society, 171, 254–276. https://doi.org/10.1111/zoj.12137
    de Voogd, N., Alvarez, B., Boury-Esnault, N., Carballo, J.L., Cárdenas, P., Díaz, M.C., Dohrmann, M., Downey, R., Hajdu, E., Hopper, J.N.A., Klautau, M., Manconi, R., Morrow, C., Pisera, A., Ríos, P., Rützler, K., Schönberg, C.H.L., Vacelet, J. & Van Soest, R.W.M. World Porifera Database. Available from: http://www.marinespecies.org/porifera/index.php (accessed 1 September 2022)
    Dendy, A. (1905) Report on the sponges collected by Professor Herdman at Ceylon, in 1902. In: Herdman, W.A. (Ed.), Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar. Royal society of London, London, pp. 57–246.
    Domingos, C., Moraes, F. & Muricy, G. (2013) Four new species of Plakinidae (Porifera: Homoscleromorpha) from Brazil. Zootaxa, 3718 (6), 530-544. https://doi.org/10.11646/zootaxa.3718.6.2
    Domingos, C., Lage, A. & Muricy, G. (2016) Overview of the biodiversity and distribution of the Class Homoscleromorpha in the Tropical Western Atlantic. Journal of the Marine Biological Association of the United Kingdom, 96 (2), 379–389. https://doi.org/10.1017/S0025315415000375
    Ereskovsky, A.V. (2006) A new species of Oscarella (Demospongiae: Plakinidae) from the Western Sea of Japan. Zootaxa, 1376 37–51. https://doi.org/10.11646/zootaxa.1376.1.2
    Ereskovsky, A.V., Sanamyan, K. & Vishnyakov, A.E. (2009) A new species of the genus Oscarella (Porifera: Homosclerophorida: Plakinidae) from the North-West Pacific. Cahiers de Biologie Marine, 2009, 369–381.
    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, 285–307. https://doi.org/10.1017/S0025315413000295
    Ereskovsky, A.V., Richter, D.J., Lavrov, D.V., Schippers, K.J. & Nichols, S.A. (2017) Transcriptome sequencing and delimitation of sympatric Oscarella species (O. carmela and O. pearsei sp. nov) from California, USA. PLOS ONE, 12 (9), e0183002. https://doi.org/10.1371/journal.pone.0183002
    Erpenbeck, D., Hooper, J.N.A. & Wörheide, 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
    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, 3–10. https://doi.org/10.1007/s10750-011-0842-x
    Gazave, E., Lavrov, D.V., Cabrol, J., Renard, E., Rocher, C., Vacelet, J., Adamska, M., Borchiellini, C. & Ereskovsky, A.V. (2013) Systematics and molecular phylogeny of the family Oscarellidae (Homoscleromorpha) with description of two new Oscarella Species. PLoS ONE, 8 (5), e63976. https://doi.org/10.1371/journal.pone.0063976
    Grant, R.E. (1836) Animal Kingdom. In: Todd, R.B. (Ed.), The Cyclopaedia of Anatomy and Physiology. s.n., London, pp. 107–118.
    Grenier, M., Ruiz, C., Lage, A. & Pérez, T. (2020) New cave-dwelling Plakina (Plakinidae, Homoscleromorpha, Porifera) from Martinique Island (French Antilles). Zootaxa, 4729 (1), 92–104. https://doi.org/10.11646/zootaxa.4729.1.6
    Idan, T., Shefer, S., Feldstein, T. & Ilan, M. (2021) New discoveries in Eastern Mediterranean mesophotic sponge grounds: updated checklist and description of three novel sponge species. Mediterranean Marine Science, 22, 270–284. https://doi.org/10.12681/mms.25837
    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
    Kohler, K.E. & Gill, S.M. (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers & Geosciences, 32 (9), 1259–1269. https://doi.org/10.1016/j.cageo.2005.11.009
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35 (6), 1547–1549. https://doi.org/10.1093/molbev/msy096
    Lage, A., Muricy, G., Ruiz, C. & Pérez, T. (2018) New sciaphilic plakinids (Porifera, Homoscleromorpha) from the Central-Western Pacific. Zootaxa, 4466 (1), 8–38. https://doi.org/10.11646/zootaxa.4466.1.4
    Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, G.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) ClustalW and ClustalX version 2. Bioinformatics, 23 (21), 2947–2948. https://doi.org/10.1093/bioinformatics/btm404
    Laubenfels, M.W. (1934) New sponges from the Puerto Rican deep. Smithsonian Miscellaneous Collections, 91, 1–28.
    Lendenfeld, R. (1887) On the Systematic position and classification of Sponges. Proceedings of the Zoological Society of London, London, 1887, 558–662.
    Lehnert, H., Stone, R. & Heimler, W. (2005) Two new species of Plakina Schulze, 1880 (Porifera, Plakinidae) from the Aleutian Islands (Alaska, USA). Zootaxa, 1068 (1), 27–38. https://doi.org/10.11646/zootaxa.1068.1.2
    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
    Moraes, F. & Muricy, G. (2003) Taxonomy of Plakortis and Plakinastrella (Demospongiae: Plakinidae) from oceanic islands off north-eastern Brazil, with description of three new species. Journal of the Marine Biological Association of the United Kingdom, 83 (2), 385–397. https://doi.org/10.1017/S0025315403007239h
    Muricy, G., Boury-Esnault, N., Bézac, C. & Vacelet, J. (1996a) Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Canadian Journal of Zoology, 74, 881–896. https://doi.org/10.1139/z96-102
    Muricy, G., Solé-Cava, A.M., Thorpe, J.P. & Boury-Esnault, N. (1996b) Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera: Demospongiae: Homoscleromorpha) from the Western Mediterranean. Marine Ecology Progress Series, 138, 181–187. https://doi.org/10.3354/meps138181
    Muricy, G. & Díaz, M.C. (2002) Order Homosclerophorida Dendy, 1905, Family Plakinidae Schulze, 1880. In: Hopper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera: a guide to the classification of sponges. Kluwer Academic, New York, New York, pp. 71–82. https://doi.org/10.1007/978-1-4615-0747-5_6
    Muricy, G. & Pearse, J. (2004) A New Species of Oscarella (Demospongiae: Plakinidae) from California. Proceedings of the California Academy of Sciences, San Francisco, 55, 598–612.
    Muricy, G. (2011) Diversity of Indo-Australian Plakortis (Demospongiae: Plakinidae), with description of four new species. Journal of the Marine Biological Association of the United Kingdom, 91, 303–319. https://doi.org/10.1017/S0025315410000743
    Muricy, G., Domingos, C., Lage, A., Lanna, E., Hardoim, C.C.P., Laport, M.S. & Zilberberg, C. (2019) Integrative taxonomy widens our knowledge of the diversity, distribution and biology of the genus Plakina (Homosclerophorida: Plakinidae). Invertebrate Systematics, 33 (2), 367–401. https://doi.org/10.1071/IS18027
    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, Antea R/V. Available from: https://campagnes.flotteoceanographique.fr/campagnes/15005300/ (accessed 4 October 2022) https://doi.org/10.17600/15005300
    Pérez, T. & Ruiz, C. (2018) Description of the first Caribbean Oscarellidae (Porifera: Homoscleromorpha). Zootaxa, 4369 (4), 501-514. https://doi.org/10.11646/zootaxa.4369.4.3
    Pozdnyakov, I., Sokolova, A., Karpov, S., Ruiz, C., Pérez, T., Ekimova, I. & Ereskovsky, A. (2020) Morphological variability of choanocyte kinetids supports a novel systematic division within Oscarellidae (Porifera, Homoscleromorpha). Journal of Zoological Systematics and Evolutionary Research, 59, 31–43. https://doi.org/10.1111/jzs.12417
    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
    Rützler, K., Piantoni, C., van Soest, R.W.M. & Díaz, M.C. (2014) Diversity of sponges (Porifera) from cryptic habitats on the Belize barrier reef near Carrie Bow Cay. Zootaxa, 3805 (1), 1–29. https://doi.org/10.11646/zootaxa.3805.1.1
    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, 44 pp.
    Schmidt, O. (1870) Grundzüge einer Spongien-Fauna des atlantischen Gebietes. Wilhelm Engelmann, Leipzig, pp. iii–iv + 1–88, pls. I–IV.
    Schulze, F.E. (1880) Untersuchungen über den Bau und die Entwicklung der Spongien. Neunte Mittheilung. Die Plakiniden. Zeitschrift für wissenschaftliche. Zoologie, 34, 407–451.
    Sollas, W.J. (1886) Preliminary account on the Tetractinellid sponges dredged by H.M.S. “Challenger” 1872-76. Part I. The Choristida. Scientific Proceedings of the Royal Dublin Society (new series). 5: 177-199.
    Stillitani, D., Ereskovsky, A.V., Pérez, T., Ruiz, C., Laport, M.S., Puccinelli, G., Hardoim, C.P., Willenz, P. & Muricy, G. (2022) Solving a taxonomic puzzle integrative taxonomy reveals new cryptic and polymorphic species of Oscarella in south-eastern Brazil (Homoscleromorpha Oscarellidae). Invertebrate Systematics, 36 (8), 714–750.
    Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular biology and evolution, 10 (3), 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
    Ubare, V.V. & Mohan, P. (2016) A New Species of Genus Plakortis Schulze 1880 (Porifera: Homoscleromorpha) from Badabalu, Andaman and Nicobar Islands, India. Zoological Studies, 55 (2), 1–9. https://doi.org/10.6620/ZS.2016.55-02
    Uliczka, E. (1929) Die tetraxonen Schwämme Westindiens (auf Grund der Ergebnisse der Reise Kükenthal-Hartmeyer). In: Kükenthal, W. & Hartmeyer, R. (Eds.), Ergebnisse einer zoologischen Forschungsreise nach Westindien. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Thiere, Supplement 16, pp. 35–62.
    Vicente, J., Zea, S. & Hill, R.T. (2016) Sponge epizoism in the Caribbean and the discovery of new Plakortis and Haliclona species, and polymorphism of Xestospongia deweerdtae (Porifera). Zootaxa, 4178 (2), 209. https://doi.org/10.11646/zootaxa.4178.2.3
    Vosmaer, G.C.J. (1884) Porifera. Die Klassen und Ordnungen des Thierreichs, II, 65–176.
    Wilson, H.V. (1902) The sponges collected in Porto Rico in 1899 by the U.S. Fish Commission Steamer Fish Hawk. Bulletin of the United States Fish Commission, 2, 375–411.
    Zeng, C., Thomas, L.J., Kelly, M. & Gardner, J.P.A. (2016) The complete mitochondrial genome of the deep-sea sponge Poecillastra laminaris (Astrophorida, Vulcanellidae). Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis, 27, 1658–1659. https://doi.org/10.3109/19401736.2014.958716