Adriatic calcarean sponges (Porifera, Calcarea), with the description of six new species and a richness analysis

Michelle Klautau, Mirna Imešek, Fernanda Azevedo, Bruna Pleše, Vedran Nikolić, Helena Ćetković

Abstract


In this study we analyze the calcarean sponge diversity of the Adriatic Sea, the type locality of some of the first described species of calcarean sponges. Morphological and molecular approaches are combined for the taxonomic identification. Our results reveal six species new to science and provisionally endemic to the Adriatic Sea (Ascandra spalatensis sp. nov., Borojevia croatica sp. nov., Leucandra falakra sp. nov., L. spinifera sp. nov., Paraleucilla dalmatica sp. nov., and Sycon ancora sp. nov.), one species previously known only from the Southwestern Atlantic (Clathrina conifera), and three already known from the Adriatic Sea (Ascaltis reticulum, Borojevia cerebrum, and Clathrina primordialis). We confirm the presence of the alien species Paraleucilla magna in the Adriatic and again record Clathrina blanca, C. clathrus, and C. rubra. We emend the description of the genus Ascaltis, propose a lectotype for Borojevia cerebrum and synonymise B. decipiens with B. cerebrum. A checklist of all calcarean species previously and currently known from the Adriatic Sea (39 species) is given. The Central Adriatic is indicated as the richest calcarean sponge fauna sector; however, the biodiversity of this class is underestimated in the whole Adriatic Sea and new systematic surveys are desirable.

Keywords


Porifera; Calcarea; Adriatic Sea; molecular taxonomy; morphological taxonomy

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DOI: https://doi.org/10.5852/ejt.2016.178

References


Arndt W. 1941. Eine neuere Ausbeute von Meeresschwämmen der West- und Südküste Portugals. Memórias do Museu de Zoologia da Universidade de Coimbra 116: 1–75.

Arnesen E. 1901. Spongier fra den norske kyst. I. Calcarea. Systematisk katalog med bemerkninger og bestemmelsestabell. Bergen Museums Ǻrbok 1900: 1–44.

Bianchi C.N. & Morri C. 2000. Marine biodiversity of the Mediterranean Sea: Situation, problems and prospects for future research. Marine Pollution Bulletin 40: 367–376. http://dx.doi.org/10.1016/S0025-326X(00)00027-8

Bianchi C.N., Morri C., Chiantore M., Montefalcone M., Parravicini V. & Rovere, A. 2012. Mediterranean Sea biodiversity between the legacy from the past and a future of change. In: Stambler N. (ed.) Life in the Mediterranean Sea: A Look at Habitat Changes: 1–55. Nova Science Publishers, Inc., New York.

Bianco S.L.O. 1888. Notizie biologiche riguardanti specialmente il periodo di maturità sessuale degli animali del golfo di Napoli. Mitteilungen aus der Zoologischen Station zu Neapel 8: 385–440.

Bidder G.P. 1891. Review of “A Monograph of Victorian Sponges”. Quarterly Journal of Microscopical Science 32: 625–632.

Borojević R. 1967. Spongiaires d’Afrique du Sud (2) Calcarea. Transactions of the Royal Society of South Africa 37: 183–226.

Borojević R. 1971. Éponges calcaires des côtes du Sud-Est du Brésil, épibiontes sur Laminaria brasiliensis et Sargassum cymosum. Revista Brasileira de Biologia 31: 525–530.

Borojević R. & Peixinho S. 1976. Éponges calcaires du nord-nord-est du Brésil. Bulletin du Muséum national d’Histoire naturelle 3(402): 987–1036.

Borojević R. & Boury-Esnault N. 1987. Calcareous sponges collected by N.O. Thalassa on the continental margin of the Bay of Biscaye: I. Calcinea. In: Vacelet J. & Boury-Esnault N. (eds) Taxonomy of Porifera from the NE Atlantic and Mediterranean Sea: 1–27. NATO Asi Series G13.

Borojević R., Cabioch L. & Lévi C. 1968. Inventaire de la Faune marine de Roscoff: Spongiaires. Éditions de la Station Biologique de Roscoff, France.

Bouzon J.L., Brandini F.P & Rocha R.M. 2012. Biodiversity of sessile fauna on rocky shores of coastal islands in Santa Catarina, Southern Brazil. Marine Science 2(5): 39–47. http://dx.doi.org/ 10.5923/j.ms.20120205.01

Breitfuss L.L. 1897a. Ascandra hermesi, ein neuer homocoeler Kalkschwamm aus der Adria. Zeitschrift für Wissenschaftliche Zoologie 63(1): 39–42.

Breitfuss L.L. 1897b. Catalog der Calcarea der zoologischen Sammlung des königlichen Museums für Naturkunde zu Berlin. Archiv für Naturgeschichte 63: 205–226.

Breitfuss L.L. 1898a. Kalkschwammfauna des Weissen Meeres und der Eismeerküsten des europäischen Russlands. Mémoires de l’Académie Imperiale des Sciences de St. Pétersbourg 6(2): 1–41.

Breitfuss L.L. 1898b. Kalkschwammfauna der Westküste Portugals. Zoologische Jahrbücher 2: 89–102.

Breitfuss L.L. 1898c. Kalkschwämme von Ternate. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 24: 169–178.

Breitfuss L.L. 1930. Biogeographischer Beitrag zur Kenntniss der Spongienfauna der Arktis. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 1929: 274–282.

Breitfuss L.L. 1932. Die Kalkschwammfauna des arktischen Gebietes. Fauna Arctica 6: 235–252.

Breitfuss L.L. 1935. La spugne calcarea dell’Adriatico con riflesso a tutto i1 Mediterraneo. Memorie Reale Comitato Talassographico Italiano 2223: 1–45.

Brøndsted H.V. 1914. Catalogue of the Porifera of Greenland. Meddelelser Om Grönland 23: 457–544.

Brøndsted H.V. 1931. Die Kalkschwämme. Deutsche Südpolar Expedition 1901–03 20: 1–47.

Burton M. 1926. Report on the sponges. Transactions of the Zoological Society of London 22: 71–83. http://dx.doi.org/10.1111/j.1096-3642.1926.tb00322.x

Burton M. 1933. Report on a small collection of sponges from Still Bay, S. Africa. Annals and Magazine of Natural History 12: 235–244.

Burton M. 1963. A Revision of the Classification of the Calcareous Sponges. British Museum, London.

Carter H.J. 1886. Descriptions of the sponges from the neighbourhood of Port Philip Heads, South Australia. Annals and Magazine of Natural History 5(18): 502–516.

Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17: 540-552. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334

Custódio M.R. & Hajdu E. 2011. Checklist de Porifera do Estado de São Paulo, Brasil. Biota Neotropica 11(1a): 1–17.

Cvitković I., Despalatović M., Grubelić I., Nikolić V., Pleše B. & Žuljević A. 2013. Occurrence of Paraleucilla magna (Porifera: Calcarea) in the eastern Adriatic Sea. Acta Adriatica: International Journal of Marine Sciences 54(1): 93–99.

Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9 (8): 772. http://dx.doi.org/10.1038/nmeth.2109

Dendy A. & Row H. 1913. The classification and phylogeny of the calcareous sponges, with a reference list of all the described species, systematically arranged. Proceedings of the Zoological Society of London 47: 704–813. http://dx.doi.org/10.1111/j.1469-7998.1913.tb06152.x

Dohrmann M., Voigt O., Erpenbeck D. & Wörheide G. 2006. Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Molecular Phylogenetics and Evolution 40: 830–843. http://dx.doi.org/10.1016/j.ympev.2006.04.016

Ferrer Hernández F. 1918. Esponjas del litoral de Asturias. Trabajos del Museo nacional de ciencias de Madri (Zoológica) 36: 1–39.

Guindon S. & Gascuel O. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology 52: 696–704. http://dx.doi.org/10.1080/10635150390235520

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. http://dx.doi.org/10.1093/sysbio/syq010

Haeckel E. 1870. Prodromus eines Systems der Kalkschwämme. Jenaische Zeitschrift für Medicin und Naturwissenschaft 5: 236–254.

Haeckel E. 1872. Die Kalkschwämme, eine Monographie. Vols 1–3. Reimer, Berlin.

Harcet M., Bilandžija H., Bruvo-Mađarić B. & Ćetković H. 2010. Taxonomic position of Eunapius subterraneus (Porifera, Spongillidae) inferred from molecular data—a revised classification needed? Molecular Phylogenetics and Evolution 54: 1021–1027. http://dx.doi.org/10.1016/j.ympev.2009.12.019

Heller C. 1864. Horae dalmatinae. Bericht über eine Reise nach der Ostküste des adriatischen Meeres. Verhandlungen der zoologisch-botanischen Gesellschaft in Wien 14: 17–64.

Hijmans R.J., Guarino L. & Mathur P. 2012. DIVAGIS, Version 7.5. A geographic information system for the management and analysis of genetic resources data. Manual. International Potato Center, Lima, Peru.

Hôzawa S. 1940. On some calcareous sponges from Japan. Science Reports of the Tôhoku Imperial University 15: 29–58.

Huelsenbeck J.P. & Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. http://dx.doi.org/10.1093/bioinformatics/17.8.754

Imešek M., Pleše B., Pfannkuchen M., Godrijan J., Pfannkuchen D.M., Klautau M. & Ćetković H. 2014. Integrative taxonomy of four Clathrina species of the Adriatic Sea, with the first formal description of Clathrina rubra Sarà, 1958. Organisms Diversity & Evolution 14(1): 21–29. http://dx.doi.org/10.1007/s13127-013-0156-0

Jenkin C.F. 1908. The marine fauna of Zanzibar and British East Africa from collections made by Cyril Crossland, M.A., in the years 1901 and 1902. Proceedings of the Zoological Society of London 434–456. http://www.biodiversitylibrary.org/item/99643#

Katoh S. & Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. http://dx.doi.org/10.1093/molbev/mst010

Kirk H.B. 1896. New Zealand sponges. Third paper. Transactions of the New Zealand Institute 28: 205–210. http://www.biodiversitylibrary.org/item/22752#

Klautau M. & Borojević R. 2001. Calcareous sponges from Arraial do Cabo – Brazil (I: the genus Clathrina). Zoosystema 23: 395–410.

Klautau M. & Valentine C. 2003. Revision of the genus Clathrina (Porifera, Calcarea). Zoological Journal of the Linnean Society 139: 1–62. http://dx.doi.org/10.1046/j.0024-4082.2003.00063.x

Klautau M., Solé-Cava A.M. & Borojević R. 1994. Biochemical systematics of sibling sympatric species of Clathrina (Porifera: Calcarea). Biochemical Systematics and Ecology 22: 367–375. http://dx.doi.org/10.1016/0305-1978(94)90027-2

Klautau M., Azevedo F., Báslavi C.-L., Rapp H.T., Collins A. & Russo C.A.M. 2013. A molecular phylogeny for the order Clathrinida rekindles and refines Haeckel’s taxonomic proposal for calcareous sponges. Integrative and Comparative Biology 53 (3): 447–461. http://dx.doi.org/10.1093/icb/ict039

Lackschewitz P. 1886. Über die Kalkschwämme Menorcas. Zoologische Jahrbücher 1: 297–310. http://www.biodiversitylibrary.org/item/38121#

Lanna E., Rossi A.L., Cavalcanti F.F., Hajdu E. & Klautau M. 2007. Calcareous sponges from São Paulo State, Brazil (Porifera: Calcarea: Calcinea) with the description of two new species. Journal of the Marine Biological Association of the United Kingdom 87: 1553–1561. http://dx.doi.org/10.1017/S0025315407056871

Lendenfeld R. von 1885. The Homocoela of Australia and the new family Homodermidae. Proceedings of the Linnean Society of New South Wales 9: 896–907. http://www.biodiversitylibrary.org/item/82331#

Lendenfeld R. von 1891. Die Spongien der Adria. I. Die Kalkschwämme. Wilhelm Engelmann, Leipzig.

Lieberkühn N. 1859. Neue Beiträge zur Anatomie der Spongien. Archiv für Anatomie und Physiologie 30 (3): 353–382, 515–529.

Lôbo-Hajdu G., Guimarães A.C.R., Salgado A., Lamarão F.R.M., Vieiralves T., Mansure J.J. & Albano R.M. 2004. Intragenomic, intra- and interspecific variation in the rDNA ITS of Porifera revealed by PCR single-strand conformation polymorphism (PCR-SSCP). Bollettino dei Musei e degli Istituti Biologici dell’Universitá di Genova 68: 413–423.

Longo C. & Pronzato R. 2011. Class Calcarea. In: Pansini M., Manconi R. & Pronzato R. (eds) Fauna d’Italia - Porifera I - Calcarea, Demospongiae (partim), Hexactinellida, Homoscleromorpha: 117–244. Calderini, Bologna.

Longo C., Mastrototaro F. & Corriero G. 2007. Occurrence of Paraleucilla magna (Porifera: Calcarea) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 87: 1749–1755. http://dx.doi.org/10.1017/S0025315407057748

Martens G.M. von. 1824. Reise nach Venedig. 2 Volumes. Stettin’sche Buchhandlung, Ulm.

Minchin E.A. 1896. Suggestions for a natural classification of the Asconidae. Annals and Magazine of Natural History 18: 349–362.

Minchin E.A. 1905. On the sponges Leucosolenia contorta Bowerbank, Ascandra contorta Haeckel, and Ascetta spinosa Lendenfeld. Proceedings of the Zoological Society of London 2: 1–20.

Monteiro L.C. & Muricy G. 2004. Patterns of sponge distribution in Cagarras Arquipelago, Rio de Janeiro, Brazil. Journal of the Marine Biological Association of the United Kingdom 84 (4): 681–687. http://dx.doi.org/10.1017/S0025315404009750h

Mothes-de-Moraes B. 1985. Sponges collected by the Oxford diving expedition to the Cabo Frio upwelling area (Rio de Janeiro, Brasil). Studies on Neotropical Fauna and Environment 20 (4): 227–237. http://dx.doi.org/10.1080/01650528509360694

Muricy G. & Hajdu E. 2006. Porifera Brasilis: Guia de Identificação das Esponjas mais comuns do Sudeste do Brasil. Série Livros 17, Museu Nacional, Rio de Janeiro.

Muricy G. & Silva O.C. 1999. Esponjas marinhas do Estado do Rio de Janeiro: um recurso renovável inexplorado. In: Silva S.H.G & Lavrado H.P. (eds) Ecologia dos Ambientes Costeiros do Estado do Rio de Janeiro. Série Oecologia Brasiliensis 7: 155–178.

Muricy G., Lopes D.A., Hajdu E., Carvalho M.S., Moraes F.C., Klautau M., Menegola C. & Pinheiro U. 2011. Catalogue of Brazilian Porifera. Museu Nacional, Rio de Janeiro.

Nichols S.A. 2005. An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution 34 (1): 81–96. http://dx.doi.org/10.1016/j.ympev.2004.08.019

Pansini M. & Longo C. 2008. Porifera. In: Relini G. (ed.) Checklist della Flora e della Fauna dei Mari Italiani (Parte I): 42–66. Biologia Marina Mediterranea 15 suppl. (1).

Rossi A.L., Russo C.A.M., Solé-Cava A.M., Rapp H.T. & Klautau M. 2011. Phylogenetic signal in the evolution of body colour and spicule skeleton in calcareous sponges. Zoological Journal of the Linnean Society 163: 1026–34. http://dx.doi.org/10.1111/j.1096-3642.2011.00739.x

Row R.W.H. 1909. Reports on the marine biology of the Sudanese Red Sea. XIX. Report on the Sponges collected by Mr Cyril Crossland in 1904–05. Journal of the Linnean Society of London, Zoology 31: 182–214. http://www.biodiversitylibrary.org/item/98662#

Row R.W.H. & Hôzawa S. 1931. Report on the Calcarea obtained by the Hamburg South-West Australian Expedition of 1905. Science Reports of the Tôhoku University 6: 727–809.

Sarà M. 1961. La fauna di poriferi delle grotte delle isole Tremiti. Studio ecologico e sistematico. Archivo Zoologico Italiano 46: 1–59.

Schmidt O. 1862. Die Spongien des Adriatischen Meeres, enthaltend die Histologie und systematiche Ergänzungen. Wilhelm Engelmann, Leipzig.

Schmidt O. 1864. Supplement der Spongien des Adriatischen Meeres, enthaltend die Histologie und systematische Ergänzungen. Wilhelm Engelmann, Leipzig.

Schmidt O. 1866. Zweites Supplement der Spongien des Adriatischen Meeres, enthaltend die Vergleichung der Adriatischen und Britischen Spongiengattungen. Wilhelm Engelmann, Leipzig.

Schmidt O. 1868. Die Spongien der Küste von Algier (Drittes Supplement). Wilhelm Engelmann, Leipzig.

Schmidt O. 1869. Vorläufige Mitteilungen über die Spongien der Grönländischen Küste. Mitteilungen des naturwissenschaftlichen Vereins für Steiermark 2: 89–97.

Schmidt O. 1870. Grundzüge einer Spongienfauna des atlantischen Gebietes. Wilhelm Engelmann, Leipzig.

Solé-Cava A.M., Klautau M., Boury-Esnault N., Borojević R. & Thorpe J.P. 1991. Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Marine Biology 111 (3): 381–386. http://dx.doi.org/10.1007/BF01319410

Spalding M.D., Fox H.E., Allen G.R., Davidson N., Ferdaña 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. & Robertson J. 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57: 573–583. http://dx.doi.org/10.1641/B570707

Tanita S. 1942. Key to all the described species of the genus Leucosolenia and their distribution. Science Reports of the Tôhoku Imperial University 17: 71–93.

Tanita S. 1943. Studies on the Calcarea of Japan. Science Reports of the Tôhoku Imperial University 17 (4): 353–490.

Topsent E. 1934. Aperçu de la faune des éponges calcaires de la Mediterranée. Bulletin de l’Institut Océanographique de Monaco 659: 1–20.

Topsent E. 1936. Étude sur les Leucosolenia. Bulletin de l’Institut Océanographique de Monaco 711: 1–47.

Voigt O., Wülfing E. & Wörheide G. 2012. Molecular phylogenetic evaluation of classification and scenarios of character evolution in calcareous sponges (Porifera, Class Calcarea). PLoS ONE 7(3): e33417. http://dx.doi.org/10.1371/journal.pone.0033417

Wörheide G. & Hooper J.N.A. 1999. Calcarea from the Great Barrier Reef. I: Cryptic Calcinea from Heron Island and Wistari Reef (Capricorn-Bunker group). Memoirs of the Queensland Museum 43: 859–891.


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