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Type: Article
Published: 2016-12-18
Page range: 349–364
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Coping with brackish water: A new species of cave-dwelling Protosuberites Porifera: Demospongiae: Suberitidae) from the Western Mediterranean and a first contribution to the phylogenetic relationships within the genus

Department of Science for Nature and Environmental Resources (DIPNET), University of Sassari, Via Muroni 25, Sassari, Italy.
Department of Life Sciences, The Natural History Museum of London, Cromwell Rd, London, UK.
Department of Life Sciences, The Natural History Museum of London, Cromwell Rd, London, UK.
Department of Science for Nature and Environmental Resources (DIPNET), University of Sassari, Via Muroni 25, Sassari, Italy.
Porifera sponges integrative taxonomy Sardinia Bue Marino Cave estuarine/anchialine karstic caves

Abstract

We used both morphological and genetic approaches to investigate and to describe a new Mediterranean sponge species of the genus Protosuberites from the estuarine-anchialine Bue Marino Cave of Sardinia (Tyrrhenian Sea). The morphotraits of the specimens were compared versus congeneric species with the strongest affinities, covering the genus geographic range worldwide. Protosuberites mereui sp. nov. is light yellow, thinly encrusting, devoid of any special ectosomal skeleton, with spicular complement of tylostyles of three size classes, single or arranged in bundles/tufts, with round to suboval heads. The new species is characterized by an exclusive diagnostic trait recorded for any cave-dwelling Protosuberites i.e. suboval and basally plated resting bodies with a foraminal aperture ornate by a collar. Resting bodies were found in the basal spongin plate firmly adhering to the substratum singly or in small groups. Also the rare, small tylostyles with a sinuous shaft and a typical mushroom-like head were never recorded in the Western Mediterranean and Atlantic species of the genus. The phylogenetic reconstruction using maximum likelihood (ML) and Bayesian Inference (BI) analyses (COI, 18S rRNA, and 28S rRNA) recovered a robustly supported sister relationship between the Mediterranean P. mereui sp. nov. and Protosuberites sp. ‘Panama’ from the Eastern Pacific Ocean. The genetic distances based on COI sequences between all compared Protosuberites species were always higher than 2%, a value sufficient to confirm that P. mereui sp. nov. is a distinct species within the genus. Morphological and genetic analyses confirm unanimously P. mereui sp. nov. as a new species. Our results contribute to the assessment of biodiversity in anchialine/estuarine caves and increase data on sponge adaptive strategies in these extreme ecosystems.

 

References

  1. Ackers, R.G.A., Moss, D. & Picton, B.E. (1992) Sponges of the British Isles (Sponge V), a colour guide and working document. Marine Conservation Society, 175.

    Annandale, N. (1914) Fauna symbiotica indica. 5. Some sponges commonly associated with oysters and mussels in Madras Harbour and the Chilka Lake. Records of the Indian Museum, 10 (7), 149–158.
    https://doi.org/10.5962/bhl.part.5625

    Annandale, N. (1915) Fauna of the Chilka Lake: Sponges. Memoirs of the Indian Museum, 5 (1), 21–54.

    Annandale, N. (1924) Sponges from Brackish water on Verlaten Island near Krakatau. Treubia, 5 (4), 402–407.

    Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI–BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25 (17), 3389–3402.
    https://doi.org/10.1093/nar/25.17.3389

    Blanquer, A. & Uriz, M.J. (2007) Cryptic speciation in marine sponges evidenced by mitochondrial and nuclear genes: a phylogenetic approach. Molecular Phylogenetics and Evolution, 45, 392–397.
    https://doi.org/10.1016/j.ympev.2007.03.004

    Blanquer, A. & Uriz, M.J. (2008) 'A posteriori' searching for phenotypic characters to described new cryptic species of sponges revealed by molecular markers (Scopalina: Dictyonellidae). Invertebrate Systematics, 22 (5), 489–502.
    https://doi.org/10.1071/IS07004

    Boury-Esnault, N. & Lopes, M.T. (1985) Les Démosponges littorales de l’Archipel des Açores. Annales de l’Institut océanographique, 61 (2),149–225.

    Cárdenas, P., Menegola, C., Rapp, H.T. & Díaz, M.C. (2009) Morphological description and DNA barcodes of shallow–water Tetractinellida (Porifera: Demospongiae) from Bocas del Toro, Panama, with description of a new species. Zootaxa, 2276, 1–39.

    Chelossi, E., Milanese, M., Milano, A., Pronzato, R. & Riccardi, G. (2004) Characterisation and antimicrobial activity of epibiotic bacteria from Petrosia ficiformis (Porifera, Demospongiae). Journal of Experimental Marine Biology and Ecology, 309, 21–33.
    https://doi.org/10.1016/j.jembe.2004.03.006

    Chombard, C., Boury–Esnault, N. & Tillier, S. (1998) Reassessment of homology of morphological characters in tetractinellid sponges based on molecular data. Systematic Biology, 47 (3), 351–366.
    https://doi.org/10.1080/106351598260761

    Corriero, G., Scalera Liaci, L., Ruggiero, D. & Pansini, M. (2000) The sponge community of a semi–submerged Mediterranean cave. Marine Ecology, 21 (1), 85–96.
    https://doi.org/10.1046/j.1439-0485.2000.00655.x

    Cottarellï, V. & Bruno, M.C. (1993) Harpacticoida (Crustacea, Copepoda) from subterranean waters of Bue Marino cave, Sardinia, and St. Barthélémy cave, Corsica, and description of three new species. International Journal of speleology, 22 (1), 1–3.

    De Waele, J. & Forti, P. (2003) Estuari sotterranei. In: Cicogna, F., C.N. Bianchi, G. Ferrari & P. Forti (Eds), Grotte Marine: cinquant’anni di ricerca in Italia. Rapallo, Ministero per la Difesa dell’Ambiente, pp. 91–104.

    Díaz, M.C., Alvarez, B. & van Soest, R.W.M. (1987) New species of Demospongiae (Porifera) from the National Park "Archipiélago de Los Roques", Venezuela. Bijdragen tot de Dierkunde, 57 (1), 31–41.

    Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC bioinformatics, 5 (1), 1–113.
    https://doi.org/10.1186/1471-2105-5-113

    Erpenbeck, D., Breeuwer, J., van der Velde, H. & van Soest, R.W.M. (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Marine Biology, 141 (2), 377–386.
    https://doi.org/10.1007/s00227-002-0785-x

    Erpenbeck, D., Hall, K., Alvarez, B., Büttner, G., Sacher, K., Schätzle, S., Schuster, A., Vargas, S., Hooper J.N.A. & Wörheide, G. (2012) The phylogeny of halichondrid demosponges: past and present re–visited with DNA–barcoding data. Organisms Diversity and Evolution, 12 (1), 57–70.
    https://doi.org/10.1007/s13127-011-0068-9

    Escobar, D., Zea, S. & 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, 271–284.
    https://doi.org/10.1016/j.ympev.2012.03.021

    Fancello, L. (2009) La grotta del Bue Marino. Sardegna Speleologica, 24, 59–72.

    Geller, J., Meyer, C., Parker, M. & Hawk, H. (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all–taxa biotic surveys. Molecular ecology resources, 13 (5), 851–861.
    https://doi.org/10.1111/1755-0998.12138

    Giribet, G., Carranza, S., Baguñá, J., Riutort, M. & Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada+ Arthropoda clade. Molecular Biology and Evolution, 13 (1), 76–84.
    https://doi.org/10.1093/oxfordjournals.molbev.a025573

    Giribet, G., Okies, A., Lindgren, A.R., Huff, S.W., Schrödl, M. & Nishiguchi, M.K. (2006) Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences, 103 (20), 7723–7728.
    https://doi.org/10.1073/pnas.0602578103

    Kumar, S., Nei, M., Dudley, J. & Tamura, K. (2008) MEGA: a biologist–centric software for evolutionary analysis of DNA and protein sequences. Briefings in bioinformatics, 9 (4), 299–306.
    https://doi.org/10.1093/bib/bbn017

    Hansen, G.A. (1885) Spongiadae. The Norwegian North-Atlantic Expedition 1876-1878. Zoology, 13, 1–26.

    Holthuis, L.B. (1973) Caridean Shrimps Found in Land–locked Saltwater Pools at Four Indo–West Pacific Localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawaii Islands): With the Description of One New Genus and Four New Species. Zoologische Verhandelingen 128, 1–48.

    Hooper, N.J.A. & van Soest, R.W.M. (2002) Systema Porifera: a guide to the classification of sponges. Kluwer Academic / Plenum Publisher, New York.
    https://doi.org/10.1007/978-1-4615-0747-5

    Humphreys, W.F. (2006) Aquifers: the ultimate groundwater–dependent ecosystems, Australian Journal of Botany, 54 (2), 115–132.
    https://doi.org/10.1071/BT04151

    Humphreys, W.F., Watts, C.H., Cooper, S.J.B. & Leijs, R. (2009) Groundwater estuaries of salt lakes: buried pools of endemic biodiversity on the western plateau, Australia. Hydrobiologia, 626 (1), 79–95.
    https://doi.org/10.1007/s10750-009-9738-4

    Lévi, C. (1973) Systématique de la classe des Demospongiaria (Demosponges) Spongiaires, 3, 577–631.

    Klautau, M., Russo, C.A., Lazoski, C., Boury–Esnault, N., Thorpe, J.P. & Solé–Cava, A.M. (1999) Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution, pp. 1414–1422.
    https://doi.org/10.2307/2640888

    Manconi, R. & Pronzato, R. (2000) Rediscovery of the type material of Spongilla lacustris (L., 1759) from the Linnean Herbarium. Italian Journal of Zoology, 67 (1), 89–92.
    https://doi.org/10.1080/11250000009356300

    Manconi, R. & Pronzato, R. (2002) Spongillina subord. nov.: Freshwater Sponges. In: Hooper J.N.A. & van Soest R.W.M. (Eds), Systema Porifera: A guide to the Classification of Sponges. Kluwer Academic / Plenum Publisher, New York, pp. 921–1019.
    https://doi.org/10.1007/978-1-4615-0747-5_97

    Manconi, R. & Pronzato, R. (2007) Gemmules as a key structure for the adaptive radiation of freshwater sponges: A morpho–functional and biogeographical study. In: Custódio, M.R., Lôbo–Hajdu, G., Hajdu, E. & Muricy, M. (Eds), Porifera Research: Biodiversity, Innovation, Sustainability, Serie Livros 28. Rio de Janeiro: Museu Nacional, pp. 61–77.

    Manconi, R. & Pronzato, R. (2016) How to survive and persist in temporary freshwater ? Adaptive traits of sponges (Porifera: Spongillida): A review. Hydrobiologia, pp. 1–12. [in press]
    https://doi.org/10.1007/s10750-016-2714-x 1

    Manconi, R. & Pronzato, R. (2015) Phylum Porifera. In: Thorp, J., Rogers, D.C. (Eds), Ecology and General Biology: Thorp and Covich's Freshwater Invertebrates, Academic Press, pp. 133–157.
    https://doi.org/10.1016/b978-0-12-385026-3.00008-5

    Manconi, R., Melis, P., Cadeddu, B., Manca, B. & Ledda, F.D. (2012) How many sponges live in anchialine caves? Natura Croatica, 21 (suppl. 1), 77–79.

    McDonald, J.I., Hooper, J.N. & McGuinness, K.A. (2002) Environmentally influenced variability in the morphology of Cinachyrella australiensis (Carter 1886) (Porifera: Spirophorida: Tetillidae). Marine and Freshwater Research, 53 (1), 79–84.
    https://doi.org/10.1071/MF00153

    Melis, P., Cadeddu, B., Demurtas, D., Ferretti, C. & Ledda, F.D. (2013) Fauna bentonica di una grotta d’estuario: il caso della Grotta del Bue Marino (Golfo di Orosei). 44° Congresso della Società Italiana di Biologia Marina, Roma, 14–16 maggio 2013.

    Melis, P. (2015) Conservation of marine biodiversity: biology, taxonomy, biogeography and sustainable development of target sponges. PhD Thesis, University of Sassari, Italy.

    Morrow C. & Cárdenas P. (2015) Proposal for a revised classification of the Demospongiae (Porifera). Frontiers in Zoology 12, 1–27.
    https://doi.org/10.1186/s12983-015-0099-8

    Muricy, G., Solé–Cava, A.M., Thorpe, J.P. & Boury–Esnault, N. (1996) Genetic evidence for extensive cryptic speciation in the subtidal sponge Plakina trilopha (Porifera: Demospongiae: Homoscleromorpha) from the Western Mediterranean. Marine Ecology Progress Series, 138 (1), 181–187.
    https://doi.org/10.3354/meps138181

    Nichols, S.A. & Barnes, P.A. (2005) A molecular phylogeny and historical biogeography of the marine sponge genus Placospongia (Phylum Porifera) indicate low dispersal capabilities and widespread crypsis. Journal of Experimental Marine Biology and Ecology, 323 (1), 1–15.
    https://doi.org/10.1016/j.jembe.2005.02.012

    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.
    https://doi.org/10.1016/j.ympev.2004.08.019

    Olivi, G. (1792) Zoologia Adriatica, ossia catalogo ragionato degli animali del golfo e della lagune di Venezia. Bassano. G. Remondini e fl., 334 (9), 1–23.

    Pansini, M. & Pesce, G.L. (1998) Higginsia ciccaresei sp. nov. (Porifera: Demospongiae) from a marine cave on the Apulian coast (Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom, 78 (04), 1083–1091.
    https://doi.org/10.1017/S0025315400044337

    Pöppe, J., Sutcliffe, P., Hooper, J.N., Wörheide, G. & Erpenbeck, D. (2010) COI barcoding reveals new clades and radiation patterns of Indo–Pacific sponges of the family Irciniidae (Demospongiae: Dictyoceratida). PLoS ONE, 5 (4), e9950.
    https://doi.org/10.1371/journal.pone.0009950

    Posada, D. & Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology, 53 (5), 793–808.
    https://doi.org/10.1080/10635150490522304

    Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular biology and evolution, 25 (7), 1253–1256.
    https://doi.org/10.1093/molbev/msn083

    Pouliquen, L. (1972) Les spongiaires des grottes sous–marines de la région de Marseille: écologie et systématique. Tethys, 3 (4), 717–758.

    Pronzato, R. & Manconi, R. (1994) Adaptive strategies of sponges in inland waters. Bollettino di Zoologia, 61 (4), 395–401.
    https://doi.org/10.1080/11250009409355912

    Pronzato, R. & Manconi, R. (1995) Long–term dynamics of a freshwater sponge population. Freshwater Biology, 33 (3), 485–495.
    https://doi.org/10.1111/j.1365-2427.1995.tb00408.x

    Pulitzer–Finali, G. (1978) Report on a collection of sponges from the Bay of Naples. III. Hadromerida, Axinellida, Poecilosclerida, Halichondrida, Haplosclerida. Bollettino dei Musei e degli Istituti Biologici della Università di Genova, 45, 7–89.

    Pulitzer–Finali, G. (1983) A collection of Mediterranean Demospongiae (Porifera) with, in appendix, a list of the Demospongiae hitherto recorded from the Mediterranean Sea. Annali del Museo civico di Storia Naturale Giacomo Doria, 84, 445–621.

    Rambaut, A. & Drummond, A.J. (2007) Tracer v1. 4.

    Rohlf, F.J. (2010) TPSDig2 Version 2.16. Department of Ecology and Evolution, Stony Brook University, NY, USA.

    Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.
    https://doi.org/10.1093/sysbio/sys029

    Rua, C.P., Zilberberg, C. & Solé–Cava, A.M. (2011) New polymorphic mitochondrial markers for sponge phylogeography. Journal of the Marine Biological Association of the United Kingdom, 91, 1015–1022.
    https://doi.org/10.1017/S0025315410002122

    Schulmeister, S. (2003) Simultaneous analysis of basal Hymenoptera (Insecta): introducing robust–choice sensitivity analysis. Biological Journal of the Linnean Society, 79 (2), 245–275.
    https://doi.org/10.1046/j.1095-8312.2003.00233.x

    Shearer, T.L., Van Oppen, M.J.H., Romano, S.L. & Wörheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology, 11 (12), 2475–2487.
    https://doi.org/10.1046/j.1365-294X.2002.01652.x

    Simpson, T.L. & Fell, P.E. (1974) Dormancy among the Porifera: gemmule formation and germination in fresh–water and marine sponges. Transactions of the American Microscopical Society, 544–577.
    https://doi.org/10.2307/3225157

    Sket, B. (1996) The ecology of anchihaline caves. Trends in Ecology and Evolution, 11 (5), 221–225.
    https://doi.org/10.1016/0169-5347(96)20031-X

    Solé-Cava, A.M. & Thorpe, J.P. (1986) Genetic differentiation between morphotypes of the marine sponge Suberites ficus (Demospongiae: Hadromerida). Marine Biology, 93, 247–253.
    https://doi.org/10.1007/BF00508262

    Solé-Cava, A.M., Klautau, M., Boury-Esnault, N., Borojevic, 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.
    https://doi.org/10.1007/BF01319410

    Stamatakis, A. (2006) RAxML–VI–HPC: maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.
    https://doi.org/10.1093/bioinformatics/btl446

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic biology, 57 (5), 758–771.
    https://doi.org/10.1080/10635150802429642

    Swartschewsky, B. (1905) Materialui faunui ghubok Chernaghomorya (Monaxonida). (Beitrag zur Kenntniss der Schwamm-Fauna des Schwarzen Meeres). Zapiski Kïevskago obshchestva estestvoispÿtatelei. Mémoires de la Société des Naturalistes de Kiew, 20 (1), 1-48.

    Tavaré, S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on mathematics in the life sciences, 17, 57–86.

    Thiele, J. (1898) Studien über pazifische Spongien. I. Japanische Demospongien. Zoologica. Original-Abhandlungen aus dem Gesamtgebiete der Zoologie, 24 (1), 1–72.

    Topsent, E. (1893) Nouvelle série de diagnoses d’éponges de Roscoff et de Banyuls. Archives de Zoologie expérimentale et générale, 1 (3), 33–43.

    Topsent, E. (1900) Etude monographique des spongiaires de France. Monaxonida (Hadromerina). Archives de Zoologie expérimentale et générale, 8 (3), 1–331.

    van Soest, R.W.M. (1977) Marine and freshwater sponges (Porifera) of the Netherlands. Zoologische Mededelingen, 50 (16), 261–273.

    van Soest, R.W.M. & Sass. D.B. (1981) Amsterdam expeditions to the West Indian Islands, report 13. Marine sponges from an island cave on San Salvador Island, Bahamas. Bijdragen tot de Dierkunde, 51 (2), 332–344.

    van Soest, R.W.M. & De Kluijver, M.J. (2003) Protosuberites denhartogi spec. nov., a new name for European Prosuberites epiphytum (Demospongiae, Hadromerida). Zoologische Verhandelingen, 345, 401–407.

    van Soest, R.W.M. (2002) Family Suberitidae Schmidt, 1870. 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. 227–244.
    https://doi.org/10.1007/978-1-4615-0747-5_25

    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, M.–C. & Cárdenas, P. (2016) World Porifera database. Available from http://www.marinespecies.org/porifera (2016–02–28)

    Vargas, S., Schuster, A., Sacher, K., Büttner, G., Schätzle, S., Läuchli, B. & Wörheide, G. (2012) Barcoding sponges: an overview based on comprehensive sampling. PloS ONE, 7 (7), e39345.
    https://doi.org/10.1371/journal.pone.0039345

    Webster, N.S. & Taylor, M.W. (2012) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology, 14 (2), 335–346.
    https://doi.org/10.1111/j.1462-2920.2011.02460.x

    Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46 (1), 1–68.
    https://doi.org/10.1093/sysbio/46.1.1

    Wörheide, G. (2006) Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo–Pacific. Marine Biology, 148 (5), 907–912.

    Wörheide, G. & Erpenbeck, D. (2007) DNA taxonomy of sponges—progress and perspectives. Journal of the Marine Biological Association of the United Kingdom, 87, 1–6.

    Wulff, J.L. (2006) Sponge systematics by starfish: predators distinguish cryptic sympatric species of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). The Biological Bulletin, 211 (1), 83–94.

    Xavier, J.R., Rachello–Dolmen, P.G., Parra–Velandia, F., Schönberg, C.H.L., Breeuwer, J.A.J. & 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 (1), 13–20.

    Yang, Z. (1996) Maximum–likelihood models for combined analyses of multiple sequence data. Journal of Molecular Evolution, 42 (5), 587–596.