‘A posteriori’ searching for phenotypic characters to describe new cryptic species of sponges revealed by molecular markers (Dictyonellidae : Scopalina)
Andrea Blanquer A B and Maria-J. Uriz AA Centre d’Estudis Avançats de Blanes CSIC, c/ accés cala St Francesc 14, 17300 Blanes, Girona, Spain.
B Corresponding author. Email: andrea@ceab.csic.es
Invertebrate Systematics 22(5) 489-502 https://doi.org/10.1071/IS07004
Submitted: 15 February 2007 Accepted: 29 July 2008 Published: 4 December 2008
Abstract
Cryptic speciation is repeatedly reported in sponge taxonomic studies. Most of the cryptic species, which were revealed by molecular markers, have never been formally described owing to the difficulty in finding diagnostic phenotypic characters. A previous molecular study revealed four genetically distinct species that had been misidentified as Scopalina lophyropoda Schmidt. One species was S. lophyropoda sensu stricto, whereas the other three were new species. Here, the three new species are formally described after careful searching for discriminatory phenotypic characters. The new species are Scopalina blanensis, sp. nov. from the north-western Mediterranean, S. ceutensis, sp. nov. from the Mediterranean coasts of Africa (Atlantic waters) and S. canariensis, sp. nov. from the Canary Islands, Atlantic Ocean. All of them are at first sight morphologically similar and inhabit shallow environments with resuspended sediment. However, a closer examination allowed us to find some differential features: e.g. the amount of spongin embedding the spicules, the degree of complexity of the skeletal tracts, the size and curvature of the styles, the growth habit and the colour tinge. Furthermore, an identification key to the Atlanto-Mediterranean Scopalina species is presented. The differences between the genera Scopalina, Ulosa and Dictyonella are also discussed.
Acknowledgements
We thank X. Turon and C. Palacín for the specimens of S. ceutensis; S. Duran, K. Rützler and S. Mariani for specimens and pictures of S. ruetzleri from Belize (North-west Atlantic) and S. Mariani for helping in larval collection. We also thank C. Marschal and N. Boury-Esnault from the Centre d’Océanologie de Marseille for performing the thick sections and J. M. Fortuño from CMIMA-CSIC for helping with the SEM pictures. Comments and suggestions by two anonymous reviewers substantially improved the final version of this paper. The study has benefited from an I3P pre-doctoral fellowship from the CSIC to AB and project INTERGEN, CTM 2004–05265-CO2/MAR, and MARMOL, CTM2007–66635-C02/MAR to MJU.
Alvarez B.,
Bergquist P. R., Battershill C. N.
(2002) Taxonomic revision of the genus Latrunculia Du Bocage (Porifera: Demospongiae: Latrunculiidae) in New Zealand. New Zealand Journal of Marine and Freshwater Research 36, 151–184.
Barbieri M.,
Bavestrello G., Sarà M.
(1995) Morphological and ecological differences in two electrophoretically detected species of Cliona (Porifera, Demospongiae). Biological Journal of the Linnean Society 54, 193–200.
Bavestrello G., Sarà M.
(1992) Morphological and genetic differences in ecologically distinct populations of Petrosia (Porifera, Demospongiae). Biological Journal of the Linnean Society 47, 49–60.
| Crossref | GoogleScholarGoogle Scholar |
Benzie J. A. H.,
Sandusky C., Wilkinson C. R.
(1994) Genetic structure of dictyoceratid sponge populations on the western Coral Sea reefs. Marine Biology 119, 335–345.
| Crossref | GoogleScholarGoogle Scholar |
Bibiloni M. A.
(1993) Some new or poorly known sponges of the Balearic Islands (western Mediterranean). Scientia Marina 57, 307–318.
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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, 271–284.
| Crossref | GoogleScholarGoogle Scholar |
Boury-Esnault N.,
Klautau M.,
Bezac C.,
Wulff J., Solé-Cava A. M.
(1999) Comparative study of putative conspecific sponge populations from both sides of the Isthmus of Panama. Journal of the Marine Biological Association of the United Kingdom 79, 39–50.
| Crossref | GoogleScholarGoogle Scholar |
Carballo J. L.,
Uriz M. J., García-Gomez J. C.
(1996) Halichondrids or Axinellids? Some problematic genera of sponges with descriptions of new species from the Strait of Gibraltar (southern Iberian Peninsula). Journal of Zoology 238, 725–741.
Cebrian E., Uriz M. J.
(2007a) Contrasting effects of heavy metals on sponge cell behaviour. Archives of Environmental Contamination and Toxicology 53, 552–558.
|
CAS |
Crossref |
PubMed |
Cebrian E., Uriz M. J.
(2007b) Do heavy metals play an active role in sponge cell behaviour in the absence of calcium? Consequences in larval settlement. Journal of Experimental Marine Biology and Ecology 346, 60–65.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Cocito S.,
Bedulli D., Sgorbini S.
(2002) Distribution patterns of the sublittoral epibenthic assemblages on a rocky shoal in the Ligurian sea (NW Mediterranean). Scientia Marina 66, 175–181.
| Crossref |
Duran S., Rützler K.
(2006) Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution 40, 292–297.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hechtel G. J.
(1965) A systematic study of the Demospongiae of Port Royal, Jamaica. Bulletin of the Peabody Museum of Natural History 20, 1–103.
Hoshino S.,
Takeda M., Watanabe Y.
(2004) Systematics of the Halichondria japonica (Kadota) (Demospongiae, Halichondrida) from Japan. Bollettino dei Musei e degli Instituti Biologici dell’Universitá di Genova 68, 373–379.
Klautau M., Borojevic R.
(2001) Sponges of the genus Clathrina Gray 1867 from Arrayal do Cabo, Brrazil. Zoosystema 23, 395–410.
Klautau M.,
Solé-Cava A. M., Borojevic R.
(1994) Biochemical systematics of sibling sympatric species of Clathrina (Porifera: Clacarea). Biochemical Systematics and Ecology 22, 367–375.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Klautau M.,
Russo C. A. M.,
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 53, 1414–1422.
| Crossref | GoogleScholarGoogle Scholar |
Knowlton N.
(1993) Sibling species in the sea. Annual Review of Ecology and Systematics 24, 189–216.
| Crossref | GoogleScholarGoogle Scholar |
Knowlton N., Mills D. E. K.
(1992) The systematic importance of color and color pattern: evidence for complexes of sibling species of snapping shrimp (Caridea: Alpheidae: Alpheus) from the Caribbean and Pacific coasts of Panama. Proceedings of the San Diego Society of Natural History 18, 1–5.
Lazoski C.,
Solé-Cava A. M.,
Boury-Esnault N.,
Klautau M., Russo C. A. M.
(2001) Cryptic speciation in a high gene flow scenario in the oviparous marine sponge Chondrosia reniformis. Marine Biology 139, 421–429.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lee M. S. Y.
(2004) The molecularisation of taxonomy. Invertebrate Systematics 18, 1–6.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Manchenko G. P., Kulikova V. I.
(1996) Allozyme and colour differences between two sibling species of the heteronemertean Lineus torquatus from the Sea of Japan. Marine Biology 125, 687–691.
| Crossref | GoogleScholarGoogle Scholar |
Mariani S.,
Uriz M. J.,
Turon X., Alcoverro T.
(2006) Dispersal strategies in sponge larvae: integrating the life history of larvae and the hydrologic component. Oecologia 149, 174–184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marschal C.,
Garrabou J.,
Harmelin J. G., Pichon M.
(2004) A new method for measuring growth and age in the precious red coral Corallium rubrum (L.). Coral Reefs 23, 423–432.
| Crossref | GoogleScholarGoogle Scholar |
Miller K.,
Alvarez B.,
Battershill C.,
Northcote P., Parthasarathy H.
(2001) Genetic, morphological and chemical divergence in the sponge genus Latrunculia (Porifera: Demospongiae) from New Zealand. Marine Biology 139, 235–250.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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, Demospngiae, Homoscleromorpha) from the Western Mediterranean. Marine Ecology Progress Series 138, 181–187.
| Crossref | GoogleScholarGoogle Scholar |
Muricy G.,
Boury-Esnault N.,
Bézac C., Vacelet J.
(1998) Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, homoscleromorpha). Zoological Journal of the Linnean Society 124, 169–203.
| Crossref | GoogleScholarGoogle Scholar |
Mustapha K. B.,
Zarrouk S.,
Souissi A., Abed A. E.
(2003) Diversite des demosponges tunisiennes. Bulletin Institut National Sciences et Technologie de la Mer de Salammbo 30, 55–77.
Nichols S. A., Barnes P. A. G.
(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, 1–15.
| Crossref | GoogleScholarGoogle Scholar |
Pulitzer-Finali G.
(1981) Some new or litle known sponges from the Great Barrier reef of Australia. Bolletino dei Musei e degli Instituti Biologici della (R.) Università di Genova 48–49, 87–141.
Rützler K.
(1981) An unusual bluegreen alga symbiotic with two new species of Ulosa (Porifera: Hymeniacidonidae) from Carrie BowCay Belize. Marine Ecology 2, 35–50.
| Crossref | GoogleScholarGoogle Scholar |
Rützler K.,
van Soest R. W. M., Alvarez B.
(2003) Svenzeai zeai, a Caribbean reef sponge with giant larva, and Scopalina ruetzleri: a comparative fine-structural approach to classification (Demospongiae, Halichondrida, Dictyonellidae). Invertebrate Biology 122, 203–222.
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.
| Crossref | GoogleScholarGoogle Scholar |
Solé-Cava A. M., Thorpe J. P.
(1992) Genetic divergence between colour morphs in populations of the common intertidal sea anemone Actinia equina and A. prasina (Anthozoa: Actiniaria) in the Isle of Man. Marine Biology 112, 243–252.
| Crossref | GoogleScholarGoogle Scholar |
Solé-Cava A. M.,
Klautau M.,
Boury-Esnault N.,
Borojevic R., Thorpe J. P.
(1991a) Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge Clathrina. Marine Biology 111, 381–386.
| Crossref | GoogleScholarGoogle Scholar |
Tarjuelo I.,
Posada D.,
Crandall K. A.,
Pascual M., Turon X.
(2004) Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Molecular Ecology 13, 3125–3136.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Topsent E.
(1934) Éponges observees dans les parages de Monaco. 1er Partie. Bulletin Institute d’Océanographie Monaco 650, 1–42.
Uriz M. J.
(1982) Morfología y comportamiento de la larva parenquímula de Scopalina lophyropoda Schmidt 1862 (Demospongia, Halichondrida) y formación del raghon. Investigaciones Pesqueras 42, 313–322.
Uriz M. J.,
Maldonado M.,
Turon X., Marti R.
(1998) How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges? Marine Ecology Progress Series 167, 137–148.
| Crossref | GoogleScholarGoogle Scholar |
Usher K. M.,
Sutton D. C.,
Toze S.,
Kuo J., Fromont J.
(2004) Biogeography and phylogeny of Chondrilla species (Demospongiae) in Australia. Marine Ecology Progress Series 270, 117–127.
| Crossref | GoogleScholarGoogle Scholar |
Vacelet J., Vasseur P.
(1971) Éponges des récifs corallines du Tuléar (Madagascar). Tethys (Marseilles) 1(Suppl.), 51–126.
Voultsiadou E.
(2005) Demosponge distribution in the eastern Mediterranean: a NW-SE gradient. Helgoland Marine Research 59, 237–251.
| Crossref | GoogleScholarGoogle Scholar |
Williams S. T.
(2000) Species boundaries in the starfish genus Linckia. Marine Biology 136, 137–148.
| Crossref | GoogleScholarGoogle Scholar |
Wulff J.
(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, 83–94.
| Crossref | GoogleScholarGoogle Scholar | PubMed |