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Morphological and molecular systematics of the ‘Cliona viridis complex’ from south-eastern Brazil

Published online by Cambridge University Press:  12 October 2015

Camille V. Leal
Affiliation:
Departamento de Invertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, 20940-040 Rio de Janeiro, RJ, Brazil
Thiago S. De Paula
Affiliation:
Departamento de Genética, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 – PHLC – Sala 205, 20550-013 Rio de Janeiro, RJ, Brazil
Gisele Lôbo-Hajdu
Affiliation:
Departamento de Genética, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 – PHLC – Sala 205, 20550-013 Rio de Janeiro, RJ, Brazil
Christine H. L. Schönberg
Affiliation:
The University of Western Australia Oceans Institute (MO96), 39 Fairway, Crawley, WA 6009, Australia Western Australian Museum, 49 Kew Street, Welshpool, WA 6106, Australia
Eduardo L. Esteves*
Affiliation:
Departamento de Zoologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 – PHLC – Sala 520, 20550-013 Rio de Janeiro, RJ, Brazil
*
Correspondence should be addressed to:E.L. Esteves, Departamento de Zoologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524 – PHLC – Sala 520, 20550-013 Rio de Janeiro, RJ, Brazil email: [email protected]

Abstract

Bioeroding sponges of the Cliona viridis species complex play a large role in carbonate cycling and reef health. In the present study we provide the first record and a description of a Mediterranean lineage of C. viridis (Schmidt, 1862) in the south-western Atlantic. Specimens were collected in Maricás Archipelago, Rio de Janeiro State in September 2010 by scuba diving at 10–12 m depth and deposited in the Porifera collection of Museu Nacional, Universidade Federal do Rio de Janeiro. Morphologically, the specimens presently examined are very similar to those described in the beta and gamma growth form from the Mediterranean. The Brazilian and Mediterranean specimens share large and irregular papillae over 2 cm in diameter, megasclere tylostyles up to 500 µm long and microsclere spirasters with up to five twists and 34 µm long. A Maximum Likelihood analysis of 28S rDNA of C. viridis, C. aprica, C. jullieni, C. schmidti and C. varians was performed for a genetic identification of the Brazilian specimens. The Brazilian material is phylogenetically closer to the Mediterranean C. viridis than to the Caribbean and Indian Ocean members of this species complex included in the present analysis. Our results suggest that C. viridis is a cryptogenic species with a distribution extending from the Mediterranean to the eastern Atlantic and in the SE Brazilian coast or further.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Barbieri, M., Bavestrello, G. and Sarà, M. (1995) Morphological and ecological differences in two electrophoretically detected species of Cliona (Porifera, Demospongiae). Biological Journal of the Linnean Society 54, 193200.Google Scholar
Barucca, M., Azzini, F., Bavestrello, G., Biscotti, M.A., Calcinai, B., Canapa, A., Cerrano, C. and Olmo, E. (2007) The systematic position of some boring sponges (Demospongiae, Hadromerida) studied by molecular analysis. Marine Biology 151, 529535.CrossRefGoogle Scholar
Bavestrello, G., Calcinai, B., Cerrano, C., Pansini, M. and Sarà, M. (1996a) The taxonomic status of some Mediterranean clionids (Porifera: Demospongiae) according to morphological and genetic characters. Bulletin de l'Institut Royal des Sciences Naturelles de Belgique, Biologie 66(Suppl.), 185195.Google Scholar
Bavestrello, G., Calcinai, B. and Sarà, M. (1996b) Delectona ciconiae sp. nov. (Porifera, Demospongiae) boring in the scleraxis of Corallium rubrum. Journal of the Marine Biological Association of the United Kingdom 76, 867873.CrossRefGoogle Scholar
Bell, J.J., Barnes, D.K.A. and Turner, J.R. (2002) The importance of micro and macro morphological variation in the adaptation of a sublittoral sponge to the current regime. Marine Biology 140, 7581.Google Scholar
Boury-Esnault, N. (1973) Campagne de la Calypso au large des côtes atlantiques de l’ Amérique du Sud (1961–1962). Résultats Scientifiques des Campagnes de la Calypso 10, 263295.Google Scholar
Bromley, R.G. (1978) Bioerosion of Bermuda reefs. Palaeogeography, Palaeoclimatology, Palaeoecology 23, 169197.CrossRefGoogle Scholar
Bromley, R.G. and D'Alessandro, A. (1984) The ichnogenus Entobia from the Miocene, Pliocene and Pleistocene of Southern Italy. Rivista Italiana di Paleontologia e Stratigrafia 90, 227296.Google Scholar
Bromley, R.G. and D'Alessandro, A. (1990) Comparative analysis of bioerosion in deep and shallow water, Pliocene to recent, Mediterranean Sea. Ichnos 1, 4349.CrossRefGoogle Scholar
Calcinai, B., Arillo, A., Cerrano, C. and Bavestrello, G. (2003) Taxonomy-related differences in the excavating micro-patterns of boring sponges. Journal of the Marine Biological Association of the United Kingdom 83, 3739.CrossRefGoogle Scholar
Calcinai, B., Azzini, F., Bavestrello, G., Gaggero, L. and Cerrano, C. (2007) Excavating rates and boring pattern of Cliona albimarginata (Porifera: Clionaidae) in different substrata. In Custódio, M.R., Hajdu, E., Lôbo-Hajdu, G. and Muricy, G. (eds) Porifera research: biodiversity, innovation and sustainability. Rio de Janeiro: Museu Nacional, pp. 203210.Google Scholar
Calcinai, B., Bavestrello, G. and Cerrano, C. (2004) Bioerosion micro-patterns as diagnostic characteristics in boring sponges. Bollettino dei Musei e degli Istituti Biologici dell'Universitá di Genova 68, 229238.Google Scholar
Calcinai, B., Bavestrello, G., Cuttone, G. and Cerrano, C. (2011) Excavating sponges from the Adriatic Sea: description of Cliona adriatica sp. nov. (Demospongiae: Clionaidae) and estimation of its boring activity. Journal of the Marine Biological Association of the United Kingdom 91, 339346.CrossRefGoogle Scholar
Campos, E.J.D., Velhote, D. and da Silveira, I.C.A. (2000) Shelf break upwelling driven by Brazil Current cyclonic meanders. Geophysical Research Letters 27, 751754.CrossRefGoogle Scholar
Carballo, J.L., Naranjo, S.A. and García-Gómez, J.C. (1997) Where does the Mediterranean Sea begin? Zoogeographical affinities of the littoral sponges of the Strait of Gibraltar. Journal of Biogeography 24, 223232.CrossRefGoogle Scholar
Carballo, J.L., Sánchez-Moyano, J.E. and García-Gómez, J.C. (1994) Taxonomic and ecological remarks on boring sponges (Clionidae) from the Straits of Gibraltar (southern Spain): tentative bioindicators? Zoological Journal of the Linnean Society of London 112, 407424.CrossRefGoogle Scholar
Cárdenas, P., Pérez, T. and Boury-Esnault, N. (2012) Sponge systematics facing new challenges. Advances in Marine Biology 61, 79209.CrossRefGoogle ScholarPubMed
Carter, H.J. (1882) Some sponges from the West Indies and Acapulco in the Liverpool Free Museum described, with general and classificatory remarks. Annals and Magazine of Natural History 9, 266301, 346–368.CrossRefGoogle Scholar
Carter, H.J. (1886) Supplement to the descriptions of Mr. J. Bracebridge Wilson's Australian sponges. Annals and Magazine of Natural History 18, 271290, 369–379, 445–466.CrossRefGoogle Scholar
Corriero, G. and Nonnis Marzano, C. (2006) A new species of Cliona (Demospongiae, Hadromerida) from the Mediterranean Sea. Italian Journal of Zoology 73, 191194.CrossRefGoogle Scholar
Corriero, G. and Scalera-Liaci, L. (1997) Cliona parenzani n. sp. (Porifera, Hadromerida) from the Ionian Sea. Italian Journal of Zoology 64, 6973.CrossRefGoogle Scholar
De Laubenfels, M.W. (1950) The Porifera of the Bermuda Archipelago. Transactions of the Zoological Society of London 27, 1154.CrossRefGoogle Scholar
De Paula, T.S., Zilberberg, C., Hajdu, E. and Lôbo-Hajdu, G. (2012) Morphology and molecules on opposite sides of the diversity gradient: four cryptic species of the Cliona celata (Porifera, Demospongiae) complex in South America revealed by mitochondrial and nuclear markers. Molecular Phylogenetics and Evolution 62, 529541.CrossRefGoogle ScholarPubMed
Duchassaing, F.P. and Michelotti, G. (1864) Spongiaires de la mer Caraïbe. Natuurkundige verhandelingen van de Hollandsche maatschappij der wetenschappen te Haarlem 21, 1124.Google Scholar
Escobar, D., Zea, S. and Sánchez, J.A. (2012) Phylogenetic relationships among the Caribbean members of the Cliona viridis complex (Porifera, Demospongiae, Hadromerida) using nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 64, 271284.CrossRefGoogle ScholarPubMed
Fang, J.H.K., Athayde, M.A.M., Schönberg, C.H.L., Kline, D.I., Hoegh-Guldberg, O. and Dove, S. (2013) Sponge biomass and bioerosion rates under ocean warming and acidification. Global Change Biology 19, 35813591.CrossRefGoogle ScholarPubMed
Friday, S., Poppel, E. and Hill, M. (2013) Cliona tumula sp. nov., a conspicuous, massive Symbiodinium-bearing clionaid from the lower Florida Keys (USA) (Demospongiae: Hadromerida: Clionaidae). Zootaxa 3750, 375382.CrossRefGoogle Scholar
Fromont, J., Craig, R., Rawlinson, L. and Alder, J. (2005) Excavating sponges that are destructive to farmed pearl oysters in Western and Northern Australia. Aquaculture Reaserch 36, 150162.CrossRefGoogle Scholar
Hajdu, E., Peixinho, S. and Fernandez, J.C.C. (2011) Esponjas marinhas da Bahia – guia de campo e laboratório. Série Livros 45. Rio de Janeiro: Museu Nacional.Google Scholar
Hechtel, G.J. (1976) Zoogeography of Brazilian marine Demospongiae. In Harrison, F.W. and Cowden, R.R. (eds) Aspects of sponge biology. New York: Academic Press, pp. 237260.CrossRefGoogle Scholar
Hill, M.S. (1999) Morphological and genetic examination of phenotypic variability in the tropical sponge Anthosigmella varians. Memoirs of the Queensland Museum 44, 239247.Google Scholar
Hill, M.S. and Hill, A.L. (2002) Morphological plasticity in the tropical sponge Anthosigmella varians, responses to predators and wave energy. Biological Bulletin 202, 8695.CrossRefGoogle ScholarPubMed
Holmes, K.E. (2000) Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invertebrate Biology 119, 125138.CrossRefGoogle Scholar
Hooper, J.N.A. and Wiedenmayer, F. (1994) Porifera. In Wells, A. (ed.) Zoological catalogue of Australia 12. Melbourne: CSIRO Information Service, pp. 130134.Google Scholar
Ignacio, B.L., Julio, L.M., Junqueira, A.O.R. and Ferreira-Silva, M.A.G. (2010) Bioinvasion in a Brazilian Bay: filling gaps in the knowledge of Southwestern Atlantic Biota. PLoS ONE 5, e13065.CrossRefGoogle Scholar
Katoh, K., Kuma, K., Toh, H. and Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511518.CrossRefGoogle ScholarPubMed
Kjerfv, B., Ribeiro, C.H.A., Dias, G.T.M., Filippo, A.M. and Quaresma, V.S. (1997) Oceanographic characteristics of an impacted coastal bay: Baía de Guanabara, Rio de Janeiro, Brazil. Continental Shelf Research 17, 16091643.CrossRefGoogle Scholar
Klautau, M., Monteiro, L. and Borojevic, R. (2004) First record of the genus Paraleucilla (Calcarea, Porifera) in the Atlantic Ocean: P. magna sp. nov. Zootaxa 710, 18.CrossRefGoogle Scholar
Leidy, J. (1889) The boring sponge, Cliona. Proceedings of the Academy of Natural Sciences of Philadelphia 41, 7075.Google Scholar
Longo, C., Mastrototaro, F. and Corriero, G. (2007) Occurrence of Paraleucilla magna (Porifera: Calcarea) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 87, 17491755.CrossRefGoogle Scholar
López-Victoria, M., Zea, S. and Weil, E. (2006) Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Marine Ecology Progress Series 312, 113121.CrossRefGoogle Scholar
MacGeachy, J.K. (1977) Factors controlling sponge boring in Barbados reef corals. In Taylor, D.L. (ed.) Proceedings of the Third International Coral Reef Symposium, Rosenstiel School of Marine and Atmospheric Science: Volume 1 Biology. Miami: University of Miami, pp. 477483.Google Scholar
Mallela, J. and Perry, C.T. (2007) Calcium carbonate budgets for two coral reefs affected by different terrestrial runoff regimes, Rio Bueno, Jamaica. Coral Reefs 26, 129145.CrossRefGoogle Scholar
Márquez, J.C. and Zea, S. (2012) Parrotfish mediation in coral mortality and bioerosion by the encrusting, excavating sponge Cliona tenuis. Marine Ecology 23, 41426.Google Scholar
Miloslavich, P., Díaz, J.M., Klein, E., Alvarado, J.J., Díaz, C., Gobin, J., Escobar-Briones, E., Cruz-Motta, J.J., Weil, E., Cortés, J., Bastidas, A.C., Robertson, R., Zapata, F., Martín, A., Castill, J., Kazandjian, A. and Ortiz, M. (2010) Marine biodiversity in the Caribbean: regional estimates and distribution patterns. PloS ONE 5, e11916.CrossRefGoogle ScholarPubMed
Monteiro-Neto, C., Bertoncini, A.A., Chaves, L.C.T., Noguchi, R., Mendonça-Neto, J.P. and Rangel, C.A. (2013) Checklist of marine fishes from coastal islands of Rio de Janeiro, with remarks on marine conservation. Marine Biodiversity Records 6, e139.CrossRefGoogle Scholar
Morrow, C. and Cárdenas, P. (2015) Proposal for a revised classification of the Demospongiae (Porifera). Frontiers in Zoology 12, 127.CrossRefGoogle ScholarPubMed
Morrow, C.C., Picton, B.E., Erpenbeck, D., Boury-Esnault, N., Maggs, C.A. and Allcock, A.L. (2012) Congruence between nuclear and mitochondrial genes in Demospongiae: a new hypothesis for relationships within the G4 clade (Porifera: Demospongiae). Molecular Phylogenetics and Evolution 62, 174190.CrossRefGoogle ScholarPubMed
Muricy, G., Esteves, E.L., Moraes, F.C., Santos, J.P., Silva, S.M., Almeida, E.V.R., Klautau, M. and Lanna, E. (2008) Biodiversidade Marinha da Bacia Potiguar: Porifera. Série Livros 29. Rio de Janeiro: Museu Nacional.Google Scholar
Muricy, G. and Hajdu, E. (2006) Porifera Brasilis: guia de identificação das esponjas marinhas mais comuns do sudeste do Brasil. Série Livros, 17. Rio de Janeiro: Museu Nacional.Google Scholar
Pang, R.K. (1973) The systematics of some Jamaican excavating sponges (Porifera). Postilla 161, 175.CrossRefGoogle Scholar
Ridley, S.O. (1881) XI. Spongida. Horny and siliceous sponges of Magellan Straits, S.W. Chily, and Atlantic off S.W. In Günther, A. (ed.) Account of the Zoological Collections made during the Survey of H.M.S. ‘Alert’ in the Straits of Magellan and on the Coast of Patagonia. London: Proceedings of the Zoological Society of London, pp. 107141.Google Scholar
Rosell, D. (1994) Morphological and ecological relationships of two clionid sponges. Ophelia 40, 3750.CrossRefGoogle Scholar
Rosell, D. and Uriz, M.J. (1997) Phylogenetic relationships within the excavating Hadromerida (Porifera), with a systematic revision. Cladistics 13, 349366.CrossRefGoogle ScholarPubMed
Rosell, D. and Uriz, M.J. (2002) Excavating and endolithic sponge species (Porifera) from the Mediterranean: species descriptions and identification key. Organisms, Diversity & Evolution 1, 132.Google Scholar
Rützler, K. (1974) The burrowing sponges of Bermuda. Smithsonian Contributions to Zoology 165, 132.CrossRefGoogle Scholar
Rützler, K. (1978) Sponges in coral reefs. In Stoddart, D.R. and Johannes, R.E. (eds) Coral reefs: research methods. Paris: UNESCO, pp. 299313.Google Scholar
Rützler, K. (2002) Family Clionaidae D'Orbigny, 1851. In Hooper, J.N.A. and Van Soest, R.W.M. (eds) Systema Porifera: a guide to the classification of sponges. New York: Kluwer Academic/Plenum Publishers, pp. 173185.CrossRefGoogle Scholar
Rützler, K. and Bromley, R.G. (1981) Cliona rhodensis, new species (Porifera: Hadromerida) from the Mediterranean. Proceedings of the Biological Society of Washington 94, 12191225.Google Scholar
Schönberg, C.H.L. (2000a) Bioeroding sponges common to the Central Great Barrier Reef: descriptions of three new species, two new records, and additions to two previously described species. Senckenbergiana maritima 30, 161221.CrossRefGoogle Scholar
Schönberg, C.H.L. (2000b) Sponges of the ‘Cliona viridis complex’ – a key for species identification. In Moosa, M.K., Soegiarto, A., Romimohtarto, K., Nontji, A., Soekarno, and Suharsono, (eds) Proceedings of the Ninth International Coral Reef Symposium. Bali, Indonesia 23–27 October 2000, pp. 295300.Google Scholar
Schönberg, C.H.L. (2001) Small-scale distribution of Great Barrier Reef bioeroding sponges in shallow water. Ophelia 55, 3954.CrossRefGoogle Scholar
Schönberg, C.H.L. (2008) A history of sponge erosion: from past myths and hypotheses to recent approaches. In Wisshak, M. and Tapanila, L. (eds) Erlangen earth conference series. Current developments in bioerosion. Berlin: Springer-Verlag, pp. 165202.CrossRefGoogle Scholar
Schönberg, C.H.L. (2015) Monitoring bioeroding sponges: using rubble, quadrat or intercept surveys? Biological Bulletin 228, 137155.CrossRefGoogle ScholarPubMed
Schönberg, C.H.L. and Beuck, L. (2007) Where Topsent went wrong: Aka infesta a.k.a. Aka labyrinthica (Demospongiae: Hadromerida) and implications for other Aka spp. Journal of the Marine Biological Association of the United Kingdom 87, 14591476.CrossRefGoogle Scholar
Schönberg, C.H.L., Grass, S. and Heiermann, A.T. (2006) Cliona minuscula, sp. nov. (Hadromerida: Clionaidae) and other bioeroding sponges that only contain tylostyles. Zootaxa 1312, 124.CrossRefGoogle Scholar
Schönberg, C.H.L. and Ortiz, J.-C. (2009) Is sponge bioerosion increasing? Proceedings of the 11th International Coral Reef Symposium, Ft. Lauderdale, Florida, 7–11 July 2008, pp. 520523.Google Scholar
Schönberg, C.H.L. and Shields, G. (2008) Micro-computed tomography for studies on Entobia: transparent substrate versus modern technology. In Wisshak, M. and Tapanila, L. (eds) Erlangen earth conference series. Current developments in bioerosion. Berlin: Springer-Verlag, pp. 147164.CrossRefGoogle Scholar
Schönberg, C.H.L. and Suwa, R. (2007) Why bioeroding sponges may be better hosts for symbiotic dinoflagellates than many corals. In Custódio, M.R., Lôbo-Hajdu, G., Hajdu, E. and Muricy, G. (eds) Porifera research. Biodiversity, innovation and sustainability. Rio de Janeiro: National Museum, pp. 569580.Google Scholar
Schönberg, C.H.L. and Wilkinson, C.R. (2001) Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20, 6976.Google Scholar
Sollas, W.J. (1878) On two new and remarkable species of Cliona. Annals and Magazine of Natural History 1, 5466.CrossRefGoogle Scholar
Spalding, M.D., Fox, H.E., Gerald, R.A., Davidson, N., Ferdana, Z.A., Finlayson, M., Halpern, B.S., Jorge, M.A., Lombana, A., Lourie, S.A., Martin, K.D., McManus, E., Molnar, J., Recchia, C.A. and Robertson, J. (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573583.CrossRefGoogle Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 8890.CrossRefGoogle ScholarPubMed
Stubler, A.D., Furman, B.T. and Peterson, B.J. (2014) Effects of pCO2 on the interaction between an excavating sponge, Cliona varians, and a hermatypic coral, Porites furcata. Marine Biology 161, 18511859.CrossRefGoogle Scholar
Topsent, E. (1888) Contribution à l’Étude des Clionides. Archives de Zoologie expérimentale et générale 5, 1165.Google Scholar
Topsent, E. (1932) Notes sur des Clionides. Archives de Zoologie expérimentale et générale 74, 549579.Google Scholar
Van Soest, R.W.M. (1993) Affinities of the marine Demospongiae fauna of the Cape Verde Islands and Tropical West Africa. Courier Forschungsinstitut Senckenberg 159, 205219.Google Scholar
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., Schönberg, C., Janussen, D., Tabachnick, K.R., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, C.M. and Cárdenas, P. (2015) World Porifera database at http://www.marinespecies.org/porifera (accessed 7 July 2015).Google Scholar
Von Lendenfeld, R. (1897) Die Clavulina der Adria. Nova Acta Academiae Caesareae Leopoldino Carolinae Germanicae Naturaecuriosorum 69, 1251.Google Scholar
White, G.B. (1977) The place of morphological studies in the investigation of Anopheles species complexes. Mosquito Systematics 9, 124.Google Scholar
Wiedenmayer, F. (1977) Shallow-water sponges of the western Bahamas. Experientia Supplementum 28, 1287.Google Scholar
Wisshak, M., Schönberg, C.H.L., Form, A. and Freiwald, A. (2012) Ocean acidification accelerates reef bioerosion. PloS ONE 7, e45124.CrossRefGoogle ScholarPubMed
Wisshak, M., Schönberg, C.H.L., Form, A. and Freiwald, A. (2013) Effects of ocean acidification and global warming on bioerosion – lessons from a clionaid sponge. Aquatic Biology 19, 111127.CrossRefGoogle Scholar
Wisshak, M., Schönberg, C.H.L., Form, A. and Freiwald, A. (2014) Sponge bioerosion accelerated by ocean acidification across species and latitudes? Helgoland Marine Research 68, 253263.CrossRefGoogle Scholar
Xavier, J.R., Rachello-Dolmen, P.G., Parra-Velandia, F., Schönberg, C.H.L., Breeuwer, J.A.J. and Van Soest, R.W.M. (2010) Molecular evidence of cryptic speciation in the ‘cosmopolitan’ excavating sponge Cliona celata (Porifera, Clionaidae). Molecular Phylogenetics and Evolution 56, 1320.CrossRefGoogle ScholarPubMed
Zea, S. and Weil, E. (2003) Taxonomy of the Caribbean excavating sponge species complex Cliona caribbaea – C. aprica – C. langae (Porifera, Hadromerida, Clionaidae). Caribbean Journal of Science 39, 348370.Google Scholar