Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Relevance of an integrative approach for taxonomic revision in sponge taxa: case study of the shallow-water Atlanto-Mediterranean Hexadella species (Porifera : Ianthellidae : Verongida)

Julie Reveillaud A B H , Céline Allewaert C , Thierry Pérez D E F , Jean Vacelet D E F , Bernard Banaigs G and Ann Vanreusel A B
+ Author Affiliations
- Author Affiliations

A Marine Biology Section, Biology Department, Ghent University, Krijgslaan 281–S8, 9000 Ghent, Belgium.

B CeMoFE, Center for Molecular Phylogeny and Evolution, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium.

C Protistology and Aquatic Ecology, Biology Department, Ghent University, Krijgslaan 281–S8, 9000 Ghent, Belgium.

D Université d’Aix-Marseille, 13007, Marseille, France.

E CNRS UMR 7263 Institut Méditerranéen de Biodiversité et d’Ecologie Marine et continentale (IMBE), 13007, Marseille, France.

F Station Marine d’Endoume, rue Batterie des Lions, 13007 Marseille, France.

G Université de Perpignan, Laboratoire de Chimie des Biomolécules & de l’Environnement, 52 Avenue Paul Alduy, 66860 Perpignan, France.

H Corresponding author. Email: julie.reveillaud@ugent.be

Invertebrate Systematics 26(3) 230-248 https://doi.org/10.1071/IS11044
Submitted: 1 November 2011  Accepted: 20 February 2012   Published: 21 September 2012

Abstract

The identification of sponges that lack a mineral skeleton is always highly challenging, especially for Hexadella species, which are also fibreless. Recently, the yellow species Hexadella pruvoti Topsent was identified as a cryptic species complex while the pink coloured Hexadella racovitzai Topsent showed two highly divergent lineages. We performed a COI phylogenetic reconstruction using 27 new Mediterranean Hexadella samples in order to confirm the presence of divergent lineages within both shallow-water species. Specimens were described with an integrative approach combining morphological and cytological investigations, biochemical profiling and assessment of natural toxicity in order to identify diagnostic characters for each taxon. H. topsenti, sp. nov. is distinguished from H. racovitzai by its colour, its surface network shape, divergent secondary metabolite patterns and toxicity values. H. crypta, sp. nov. differs from H. pruvoti by a different encrusting growth form when alive, and by distinctively colouring the ethanol fixative solution. In addition, H. pruvoti and H. crypta show different types of cells with inclusions as well as distinct metabolic fingerprints. Natural toxicity values, however, do not permit the separation of H. pruvoti and H. crypta. Our work shows that only the use of a combination of complementary tools can provide relevant descriptions for some problematic taxa.

Additional keywords: biochemistry, cytology, Hexadella, morphology, phylogeny, taxonomy, toxicity.


References

Becerro, M. A., Uriz, M. J., and Turon, X. (1995). Measuring toxicity in marine environments: critical appraisal of three commonly used methods. Experientia 51, 414–418.
Measuring toxicity in marine environments: critical appraisal of three commonly used methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXls1Onsbs%3D&md5=c77791fe443e45dec9540ce5023dc7ccCAS |

Bergquist, P. R. (1978). Sponges. Hutchinson University Library, London.

Bergquist, P. R. (1980). A revision of the supraspecific classification of the orders Dictyoceratida, Dendroceratida and Verongida (Class Demospongia). New Zealand Journal of Zoology 7, 443–503.

Bergquist, P. R., and Cook, S. D. C. (2002). Order Verongida Bergquist, 1978. In ‘Systema Porifera: A Guide to the Classification of Sponges. Vol. I.’ (Eds J. N. A. Hooper and R. W. M. Van Soest.) pp. 1081–1096. (Kluwer Academic/Plenum Publishers: New York.)

Blanquer, A., and Uriz, M. J. (2008). ‘A posteriori’ searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Dictyonellidae: Scopalina). Invertebrate Systematics 22, 489–502.
‘A posteriori’ searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Dictyonellidae: Scopalina).Crossref | GoogleScholarGoogle Scholar |

Borojevic, R., Cabioch, L., and Lévi, C. (1968). ‘Inventaire de la Faune Marine de Roscoff. Spongiaires’. (Editions de la Station Biologique de Roscoff: Roscoff.)

Boury-Esnault, N., and Lopez, M. T. (1985). Les démosponges littorales de l’Archipel des Açores. Annales de l’Institut Océanographique, Paris, France 61, 149–225.

Boury-Esnault, N., Muricy, G., Gallissian, M. F., and Vacelet, J. (1995). Sponges without skeleton: a new Mediterranean genus of Homoscleromorpha (Porifera, Demospongiae). Ophelia 43, 25–43.

Burton, M. (1926). Description of South African sponges collected in the South African Marine Survey. Part I. Myxospongia and Astrotetraxonida. Fisheries Bulletin. Fisheries and Marine Biological Survey Division, Union of South Africa Rept. 4 (Special Rept. 9), 1–29, pls I–VI.

Burton, M. (1937). Supplement to The Littoral Fauna of Krusadai Island in the Gulf of Manaar. Porifera. Bulletin of the Madras Government Museum (New Series, Natural History Section) 1, 1–58, pls I–IX.

Cruz, T., and Bacallado, J. J. (1985). Introduccion a los poblamientos de espongiarios de las islas Canarias. In ‘Actas do IV° Simposio Iberico do Estudios do Benthos Marino Mayo, 1984’. pp. 141–150 (Lisboa)

Darwin, C. (1859 [1964]). ‘On the Origin of Species: a Facsimile of the First Edition.’ (Harvard University Press: Cambridge, MA.)

De Laubenfels, M. W. (1950). The sponges of Kaneohe Bay, Oahu. Pacific Science 4, 1–36.

Dendy, A. (1905). Report on the sponges collected by Professor Herdman at Ceylon, in 1902. In ‘Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar’. (Ed. W. A. Herdman.) pp. 57–246, pls I–XVI (Royal Society: London.)

Ereskovsky, A. V., Borchiellini, C., Gazave, E., Ivanišević, J., Lapébie, P., Pérez, T., Renard, E., and Vacelet, J. (2009). The homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology. BioEssays 31, 89–97.
The homoscleromorph sponge Oscarella lobularis, a promising sponge model in evolutionary and developmental biology.Crossref | GoogleScholarGoogle Scholar |

Erpenbeck, D., and Van Soest, R. W. M. (2007). Status and perspective of sponge chemosystematics. Marine Biotechnology (New York, N.Y.) 9, 2–19.
Status and perspective of sponge chemosystematics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlCrsLs%3D&md5=9de69639df97eb7521e08acde293ed24CAS |

Erwin, P. M., and Thacker, R. W. (2007). Phylogenetic analyses of marine sponges within the order Verongida: a comparison of morphological and molecular data. Invertebrate Biology 126, 220–234.
Phylogenetic analyses of marine sponges within the order Verongida: a comparison of morphological and molecular data.Crossref | GoogleScholarGoogle Scholar |

Ivanišević, J., Thomas, O., Lejeusne, C., Chevaldonné, P., and Pérez, T. (2011). Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 7, 289–304.
Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges.Crossref | GoogleScholarGoogle Scholar |

Klautau, M., Russo, C. A. M., Lazoski, C., Boury-Esnault, N., Thorpe, J. P., and Sole-Cava, A. M. (1999). Does cosmopolitanism result from overconservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53, 1414–1422.

Longo, C., Mastrototaro, F., and Corriero, G. (2005). Sponge fauna associated with a Mediterranean deep-sea coral bank. Journal of the Marine Biological Association of the United Kingdom 85, 1341–1352.
Sponge fauna associated with a Mediterranean deep-sea coral bank.Crossref | GoogleScholarGoogle Scholar |

Martí, R., Fontana, A., Uriz, M. J., and Cimino, G. (2003). Quantitative assessment of natural toxicity in sponges: toxicity bioassay versus compound quantification. Journal of Chemical Ecology 29, 1307–1318.
Quantitative assessment of natural toxicity in sponges: toxicity bioassay versus compound quantification.Crossref | GoogleScholarGoogle Scholar |

Matsunaga, S., Kobayashi, H., van Soest, R. W. M., and Fusetani, N. (2005). Novel bromotyrosine derivatives that inhibit growth of the fish pathogenic bacterium Aeromonas hydrophila, from a marine sponge Hexadella sp. The Journal of Organic Chemistry 70, 1893–1896.
Novel bromotyrosine derivatives that inhibit growth of the fish pathogenic bacterium Aeromonas hydrophila, from a marine sponge Hexadella sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnvVemtg%3D%3D&md5=bb25647c94aea578a52687db57df2ea8CAS |

Morris, S. A., and Andersen, R. J. (1989). Nitrogenous metabolites from the deep water sponge Hexadella sp. Canadian Journal of Chemistry 67, 677.
Nitrogenous metabolites from the deep water sponge Hexadella sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVCmtL0%3D&md5=73614b6e7956d5035e380a8fea5f3c09CAS |

Morrow, C. C., and Picton, B. E. (1996). An aplysillid sponge Hexadella racovitzai Topsent, 1896, new to the British Isles with notes on its habitat and distribution. Irish Naturalists’ Journal 25, 218–221.

Muricy, G., Boury-Esnault, N., Bézac, C., and Vacelet, J. (1996). Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha). Canadian Journal of Zoology-Revue Canadienne de Zoologie 74, 881–896.
Cytological evidence for cryptic speciation in Mediterranean Oscarella species (Porifera, Homoscleromorpha).Crossref | GoogleScholarGoogle Scholar |

Picton, B. E., and Costello, M. J. (1999). BioMar biotope viewer: a guide to marine habitats, fauna and flora of Britain and Ireland. Environmental Sciences Unit, Trinity College, Dublin.

Picton, B. E., and Goodwin, C. E. (2007). Sponge biodiversity of Rathlin Island, Northern Ireland. Journal of the Marine Biological Association of the United Kingdom 87, 1441–1458.
Sponge biodiversity of Rathlin Island, Northern Ireland.Crossref | GoogleScholarGoogle Scholar |

Reveillaud, J., Remerie, T., van Soest, R., Erpenbeck, D., Cárdenas, P., Derycke, S., Xavier, J. R., Rigaux, A., and Vanreusel, A. (2010). Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae). Molecular Phylogenetics and Evolution 56, 104–114.
Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae).Crossref | GoogleScholarGoogle Scholar |

Reveillaud, J., van Soest, R., Derycke, S., Picton, B., Rigaux, A., and Vanreusel, A. (2011). Phylogenetic relationships among NE Atlantic Plocamionida Topsent (1927) (Porifera, Poecilosclerida): under-estimated diversity in reef ecosystems. PLoS ONE 6, e16533.
Phylogenetic relationships among NE Atlantic Plocamionida Topsent (1927) (Porifera, Poecilosclerida): under-estimated diversity in reef ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlSgsbo%3D&md5=64adbf9a9afee110a85442eb4e80bae9CAS |

Ribo, J. M., and Kaiser, K. L. E. (1987). Photobacterium–phosphoreum toxicity bioassay. 1. Test procedures and applications. Toxicity Assessment 2, 305–323.
Photobacterium–phosphoreum toxicity bioassay. 1. Test procedures and applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlt1yms7Y%3D&md5=13c4cb28178066eedde01f01dfa11fa9CAS |

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.

Topsent, E. (1913). Spongiaires provenant des campagnes scientifiques de la ‘Princesse Alice’ dans les Mers du Nord (1898–1899 – 1906–1907). Résultats des campagnes scientifiques accomplies par le Prince Albert I. Monaco 45, 1–67.

Vacelet, J. (1967). Les cellules à inclusions de l’éponge cornée Verongia cavernicola Vacelet. Journal of Microscopy 6, 237–240.

Vacelet, J. (1969). Éponges de la Roche du Large et de l’étage bathyal de Méditerranée (récoltes de la soucoupe plongeante Cousteau et dragages). Mémoires du Muséum national d’Histoire naturelle (A, Zoologie) 59, 145–219.

Vacelet, J., Vasseur, P., and Lévi, C. (1976). Spongiaires de la pente externe des récifs coralliens de Tulear Sud-Ouest de Madagascar. Mémoires du Muséum national d’Histoire naturelle 49, 1–116.

Van Soest, R. W. M., and Braekman, J. C. (1999). Chemosystematics of Porifera: a review. Memoirs of the Queensland Museum 44, 569–589.

Van Soest, R. W. M., and Lavaleye, M. S. S. (2005). Diversity and abundance of sponges in bathyal coral reefs of Rockall Bank, NE Atlantic, from boxcore samples. Marine Biology Research 1, 338–349.
Diversity and abundance of sponges in bathyal coral reefs of Rockall Bank, NE Atlantic, from boxcore samples.Crossref | GoogleScholarGoogle Scholar |

Van Soest, R. W. M., Van Duyl, F. C., Maier, C., Lavaleye, M. S. S., Beglinger, E., and Tabachnick, K. R. (2007). Mass occurrence of the hexactinellid Rossella nodastrella Topsent in bathyal coral reefs of Rockall Bank, W of Ireland. In ‘Trends in Porifera Research-Biodiversity, Innovation, Sustainability. Proceedings 7th International Sponge Conference, Buzios 6–13 May 2006’. (Eds M. R. Custódio, G. Lôbo-Hajdu, E. Hajdu and G. Muricy.) pp. 645–652. (Universidade de Sao Paulo: Brazil.)

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., Janussen, D., Tabachnick, K. R., Klautau, M., Picton, B., Kelly, M., and Vacelet, J. (2011) World Porifera database. Available online at http://www.marinespecies.org/porifera.

Williams, S. T. (2000). Species boundaries in the starfish genus Linckia. Marine Biology 136, 137–148.

Wu, H., Nakamura, H., Kobayashi, J., Ohizumi, Y., and Hirata, Y. (1986). Lipopurealins, novel bromotyrosine derivatives with long-chain acyl-groups, from the marine sponge Psammaplysilla purea. Experientia 42, 855–856.
Lipopurealins, novel bromotyrosine derivatives with long-chain acyl-groups, from the marine sponge Psammaplysilla purea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xls12hsrk%3D&md5=ec9785fdbbd18408751c9ae24fc2164dCAS |

Xavier, J. R., and Van Soest, R. W. M. (2007). Demosponge fauna of Ormonde and Gettysburg Seamounts (Gorringe Bank, north-east Atlantic): diversity and zoogeographical affinities. Journal of the Marine Biological Association of the United Kingdom 87, 1643–1653.
Demosponge fauna of Ormonde and Gettysburg Seamounts (Gorringe Bank, north-east Atlantic): diversity and zoogeographical affinities.Crossref | GoogleScholarGoogle 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, 13–20.
Molecular evidence of cryptic speciation in the “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czns1CqsA%3D%3D&md5=1bbacab3d4804c46d1c3ba040411cebcCAS |