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

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 A

A 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 http://dx.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.


References

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
doi:10.1111/j.1095-8312.1992.tb00655.x

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 doi:10.1007/BF00347530

Bibiloni M. A. (1990). Fauna de esponjas de las isles Baleares. Variación cualitatova y cuantitativa de la población de esponjas en un gradiente batimétrico. Comparación Baleares-Costa Catalana. Ph.D. Thesis, University of Barcelona, Spain.

Bibiloni M. A. 1993 Some new or poorly known sponges of the Balearic Islands (western Mediterranean). Scientia Marina 57 307 318

Blanquer A. (2007). Molecular markers for phylogenetic and population studies of the genus Scopalina (Porifera: Demospongiae). Ph.D. Thesis, University of Barcelona, Spain.

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
doi:10.1016/j.ympev.2007.03.004

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 doi:10.1080/00222939200770131

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 doi:10.1017/S0025315498000046

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. 2007 a Contrasting effects of heavy metals on sponge cell behaviour. Archives of Environmental Contamination and Toxicology 53 552 558


Cebrian E. Uriz M. J. 2007 b 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
doi:10.1016/j.jembe.2007.02.010

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

Cruz T. (2002). ‘Esponjas marinas de Canarias.’ (Consejería de Política Territorial y Medio Ambiente del Gobierno de Canarias: La Laguna-Sta. Cruz de Tenerife, Spain.)

Duran S. Rützler K. 2006 Ecological speciation in a Caribbean marine sponge. Molecular Phylogenetics and Evolution 40 292 297
doi:10.1016/j.ympev.2006.02.018

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

Hooper J. N. A. , and Van Soest R. W. M. (2002). ‘Systema Porifera, A Guide to the Classification of Sponges?’ (Kluwer Academic/Plenum Publishers: New York, USA.)

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
doi:10.1016/0305-1978(94)90027-2

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 doi:10.2307/2640888

Knowlton N. 1993 Sibling species in the sea. Annual Review of Ecology and Systematics 24 189 216 doi:10.1146/annurev.es.24.110193.001201

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
doi:10.1007/s002270100542

Lee M. S. Y. 2004 The molecularisation of taxonomy. Invertebrate Systematics 18 1 6 doi:10.1071/IS03021

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 doi:10.1007/BF00349250

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 doi:10.1007/s00442-006-0429-9

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 doi:10.1007/s00338-004-0398-6

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 doi:10.1007/s002270100574

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 doi:10.3354/meps138181

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 doi:10.1111/j.1096-3642.1998.tb00572.x

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
doi:10.1016/j.jembe.2005.02.012

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. (1978). Sponges in coral reefs. In ‘Coral Reefs: Research Methods. Monographs on Oceanographic Methodology, Vol. 5’. (Eds D. R. Stoddart and R. E. Johannes.) pp. 299–313. (Unesco: Paris, France.)

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
doi:10.1111/j.1439-0485.1981.tb00089.x

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

Schmidt O. (1862). ‘Die spongien des Adriatischen Meeres.’ (Wihelm Engelmann: Leipig, Germany.)

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
doi:10.1007/BF00508262

Solé-Cava A. M. , and Thorpe J. P. (1987). The use of electrophoresis in sponge taxonomy. In ‘Taxonomy of Porifera. NATO ASI series, Vol. 13’. (Eds J. Vacelet and N. Boury-Esnault.) pp. 243–258. (Springer-Verlag: Berlin-Heidelberg, Germany.)

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 doi:10.1007/BF00702468

Solé-Cava A. M. Klautau M. Boury-Esnault N. Borojevic R. Thorpe J. P. 1991 a Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge Clathrina. Marine Biology 111 381 386 doi:10.1007/BF01319410

Solé-Cava A. M. , Thorpe J. P. , and Manconi R. (1991 b). A new Mediterranean species of Axinella detected by biochemical genetic methods. In ‘Fossil and Recent Sponges’. (Eds J. Reitner and H. Keuoo.) pp. 313–321. (Springer-Verlag: Berlin, Germany.)

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 doi:10.1111/j.1365-294X.2004.02306.x

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
doi:10.3354/meps167137

Uriz M. J. , Turon X. , and Mariani S. (2002). Ultrastructure of sponge larvae with contrasting behaviours. In ‘Book of Abstracts. 5th International Larval Biology Meeting’. (Ed. E. Vazquez.) pp. 39–40. (Universidad de Vigo: Vigo, Spain.)

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 doi:10.3354/meps270117

Vacelet J. Vasseur P. 1971 Éponges des récifs corallines du Tuléar (Madagascar). Tethys (Marseilles) 1 Suppl. 51 126

Van Soest R. W. M. , Erpenbeck D. , and Alvarez B. (2002). Family Dictyonellidae Van Soest, Diaz & Pomponi 1990. In ‘Systema Porifera. A Guide to the Classification of Sponges’. (Ed. J. N. A. Hooper and R. W. M. V. Soest.) pp. 773–786. (KluwerAcademic/Plenum Publishers: New York, USA.)

Voultsiadou E. 2005 Demosponge distribution in the eastern Mediterranean: a NW-SE gradient. Helgoland Marine Research 59 237 251
doi:10.1007/s10152-005-0224-8

Wiedenmayer F. (1977) A monograph of the shallow-water sponges of the western Bahamas. Experientia Supplentum 28. (Birhäuser Verlag: Basel, Germany).

Williams S. T. 2000 Species boundaries in the starfish genus Linckia. Marine Biology 136 137 148 doi:10.1007/s002270050016

Wörheide G. , Degnan B. M. , Hooper J. N. A. , and Reitner J. (2000). Phylogeography and taxonomy of the Indo-Pacific reef cave dwelling coralline demosponge Astrosclerawilleyana’: new data from nuclear internal transcribed spacer sequences. In ‘Proceedings of the 9th International Coral Reef Sysmposium, Vol. 1, Bali, Indonesia’. (Ed. K. Moosa.) pp. 131–138.

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 doi:10.2307/4134581



Export Citation