Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-16T07:27:29.113Z Has data issue: false hasContentIssue false
  • English
  • Français

Redescription and new records of Celtodoryx ciocalyptoides (Demospongiae: Poecilosclerida)—a sponge invader in the north east Atlantic Ocean of Asian origin?

Published online by Cambridge University Press:  07 February 2011

Daniela Henkel  and
Dorte Janussen
Daniela Henkel*
Affiliation:
Forschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany
Dorte Janussen
Affiliation:
Forschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany
*
Correspondence should be addressed to: D. Henkel, Forschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, 60325 Frankfurt am Main, Germany email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In 1996 a sponge was found in a well studied area in the Ria of Etel, Brittany, France, that had never been recorded there before. This sponge was later described as a new species and genus, Celtodoryx girardae by Perez et al. (2006), who concluded that it is probably an invasive species. Over several years C. girardae was found to occur successively in the Gulf of Morbihan, France, and Oosterschelde estuary, Netherlands. This sponge is characterized by an extensive spatial broading and therewith it rates today among the dominant benthic megafauna in the shallow waters of the Gulf of Morbihan and Dutch inshore waters. During our recent survey of the Chinese Yellow Sea sponge fauna, we found an abundant species with close morphological similarities to C. girardae. Further taxonomic studies have revealed that both the Chinese and European sponges are in fact conspecific with Cornulum ciocalyptoides described by Burton (1935) from Posiet Bay, Sea of Japan and later recorded from other localities of the North West Pacific (e.g. Koltun, 1971; Sim & Byeon, 1989). In this paper we transfer the species of Burton from Cornulum to Celtodoryx and consequently it becomes the senior synonym of C. girardae. Furthermore, we conclude that Celtodoryx ciocalyptoides was introduced to the North East Atlantic from the North West Pacific with aquaculture of the Pacific oyster Crassostrea gigas as the probable vector. This is probably the first case recorded so far of a sponge species being transferred from one ocean to another by human activity.

Keywords

PoriferasystematicstaxonomyCeltodoryxC. ciocalyptoidesC. girardaenon-indigenous speciesaquaculturevector
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Special Issue 2: Biodiversity and Taxonomy , March 2011 , pp. 347 - 355
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Barnes, D.K.A. (2002a) Human rubbish assists alien invasions of seas. Directions in Science 1, 107–112.Google Scholar
Barnes, D.K.A. (2002b) Biodiversity: invasions by marine life on plastic debris. Nature 416, 808–809.CrossRefGoogle ScholarPubMed
Barthel, D. (1986) On the ecophysiology of the sponge Halichondria panicea in Kiel Bight. I. Substrate specificity, growth and reproduction. Marine Ecology Progress Series 32, 291–298.CrossRefGoogle Scholar
Barthel, D. (1988) On the ecophysiology of the sponge Halichondria panicea in Kiel Bight II. Biomass, production, energy budget and integration in environmental processes. Marine Ecology Progress Series 43, 87–93.CrossRefGoogle Scholar
Bavestrello, G., Bonito, M. and Sarà, M. (1993a) Influence of depth of the size of sponge spicules. Scientia Marina 57, 415–420.Google Scholar
Bavestrello, G., Bonito, M. and Sarà, M. (1993b) Silica content and spicular size variation during an annual cycle in Chondrilla nucula Schmidt (Porifera, Demospongiae) in the Ligurian Sea. Scientia Marina 57, 421–425.Google Scholar
Burton, M. (1935) Some sponges from the Okhotsk Sea and the Sea of Japan. Exploration des Mers de l'URSS 22, 61–79.Google Scholar
Candelas, G.C. and Candelas, G.A. (1963) Notes on the seasonal distribution of the sponge Hymeniacidon heliophila at Beaufort. North Carolina Ecology 44, 595–597.Google Scholar
Dendy, A. (1922) Report on the Sigmatotetraxonida collected by H.M.S. ‘Sealark’ in the Indian Ocean. Reports of the Percy Sladen Trust Expedition to the Indian Ocean in 1905Volume 7. Transactions of the Linnean Society of London (2) 18, 1–164.Google Scholar
de Wit, M.P., Crookes, D.J. and van Wilgen, B.W. (2001) Conflicts of interest in environmental management: estimating the costs and benefits of a tree invasion. Biological Invasions 3, 167–178.CrossRefGoogle Scholar
di Castri, F. (1989) History of biological invasions with special emphasis on the Old World. In Drake, J.A., Moyle, P.B., Rejmánek, M. and Vermeij, G. (eds) Biological invasions, a global perspective. Chichester: John Wiley & Son, pp. 1–30.Google Scholar
Dijkstra, J., Harris, L.G. and Westerman, E. (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 342, 61–68.CrossRefGoogle Scholar
Duckworth, A.R. and Battershill, C.N. (2001) Population dynamics and chemical ecology of New Zealand Demospongiae Latrunculia sp. nov. and Polymastia croceus (Poecilosclerida: Latrunculiidae; Polymastiidae). New Zealand Journal of Marine and Freshwater Research 35, 935–949.CrossRefGoogle Scholar
Convey, P., Barnes, D.K.A. and Morton, A. (2002) Debris accumulation on oceanic island shores of the Scotia Arc, Antarctica. Polar Biology 25, 612–617.CrossRefGoogle Scholar
Denslow, J.S. (2002) Invasive alien woody species in Pacific island forests. Unasylva 209, 62–63.Google Scholar
Golani, D., Azzurro, E., Corsini-Foka, M., Falautano, M., Andaloro, F. and Bernardi, G. (2007) Genetic bottlenecks and successful biological invasions: the case of a recent Lessepsian migrant. Biology Letters 3, 541–545.CrossRefGoogle ScholarPubMed
Gollasch, S., Minchin, D. and Wolff, W.J. (2009) Introduced aquatic species of the North Sea coasts and adjacent brackish waters. In Rilov, G. and Crooks, J.A. (eds) Biological invasions in marine ecosystems, ecological, management and geographic perspectives. Ecological studies 204. Berlin: Springer-Verlag, pp. 507–525.Google Scholar
Hajdu, E., van Soest, R.W.M. and Hooper, J.N.A. (1994) Proposal for a phylogenetic subordinal classification of poecilosclerid sponges. In van Soest, R.W.M., van Kempen, T.M.G. and Braekman, J.-C. (eds) Sponges in time and space. Rotterdam: Balkema, pp. 123–139.Google Scholar
Hoshino, T. (1987) A preliminary catalogue of marine species of the class Demospongia (Porifera) from Japanese waters. Mukaishima Marine Biological Station Faculty of Science, Hiroshima University, Mukaishima, Hiroshima, Japan, pp. 1–48.Google Scholar
Jones, W.C. (1987) Seasonal variations in the skeleton and spicule dimensions of Haliclona elegans (Bowerbank) sensu Topsent (1887) from two sites in North Wales. In Jones, W.C. (ed.) European contributions to the taxonomy of sponges. Publications of the Sherkin Island Marine Station 1, 109–129.Google Scholar
Jørgensen, C.B. (1944) On the spicule formation of Spongilla lacustris (L.). 1. The dependence of the spicule-formation on the content of dissolved and solid silicic acid in the milieu. Kongelinke Danske Videnskabernes Selskab Biologiske Meddelande 19, 1–45.Google Scholar
Khodakovskaya, A.V. (2003) Zoogeographical aspects of the sponge fauna of the north-western part of the Sea of Japan. Proceedings of the Zoological Institute of the Russian Academy of Science 299, 73–82.Google Scholar
Khodakovskaya, A.V. (2005) Fauna of sponges (Porifera) of Peter the Great Bay, Sea of Japan. Russian Journal of Marine Biology 31, 209–214.CrossRefGoogle Scholar
Koltun, V.M. (1959) Siliceous horny sponges of the northern and fareastern seas of the U.S.S.R.. Opredeliteli po faune SSR, Izdavaemye Zoologicheskim Muzeem Akademii Nauk 67, 1–236. [In Russian.]Google Scholar
Koltun, V.M. (1971) To a knowledge of the sponge fauna of the Possjet Bay of the Sea of Japan. In Explorations of the flora and fauna of the seas VIII (XVI), Fauna and flora of the Possjet Bay of the Sea of Japan. Academy of Sciences of the USSR—Zoological Institute, pp. 22–30.Google Scholar
Lévi, C. (1961) Spongiaires des Iles Philippines, principalement récoltées au voisinage de Zamboanga. Philippine Journal of Science 88, 509–533.Google Scholar
Liu, S., Zhang, J., Chen, H. and Raabe, T. (2004) Benthic nutrient recycling in shallow coastal waters of the Bohai Sea. Chinese Journal of Oceanology and Limnology 22, 365–372.Google Scholar
Lowenstam, H.A. and Weiner, S. (1989) On biomineralization. New York: Oxford University Press.CrossRefGoogle Scholar
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evens, H., Clout, M. and Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.CrossRefGoogle Scholar
Maldonado, M., Carmona, M.C., Uriz, M.J. and Cruzado, A. (1999) Decline in Mesozoic reef-building sponges explained by silicon limitation. Nature 401, 785–788.CrossRefGoogle Scholar
Mercurio, M., Corriero, G., Scalera-Liaci, L. and Gaino, E. (2000) Silica content and spicule size variations in Pellina semitubulosa (Porifera: Demospongiae). Marine Biology 137, 87–92.CrossRefGoogle Scholar
Minchin, D., Gollasch, S., Cohen, A.N., Hewitt, C.L. and Olenin, S. (2009) Characterizing vectors of marine invasion. In Rilov, G. and Crooks, J.A. (eds) Biological invasions in marine ecosystems. Berlin: Springer-Verlag, pp. 109–116.CrossRefGoogle Scholar
Perez, T., Perrin, B., Carteron, S., Vacelet, J. and Boury-Esnault, N. (2006) Celtodoryx girardae gen. nov. sp. nov., a new sponge species (Poecilosclerida: Demospongiae) invading the Gulf of Morbihan (North East Atlantic, France). Cahier de Biologie Marine 47, 205–214.Google Scholar
Pimentel, D., Zuniga, R. and Morrison, D. (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52, 273–288.CrossRefGoogle Scholar
Reise, K., Gollasch, S. and Wolff, W.J. (2002) Introduced marine species of the North Sea coasts. In Leppäkoski, E., Gollasch, S. and Olenin, S. (eds) Invasive aquatic species of Europe—distribution, impacts and management. Dordrecht: Kluwer, pp. 260–266.CrossRefGoogle Scholar
Rhymer, J.M. and Simberloff, D. (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27, 83–109.CrossRefGoogle Scholar
Sarà, M. and Vacelet, J. (1973) Ecologie des Démosponges In Grasse, P.-P. (ed.) Traité de zoologie. III. Spongaires. Paris: Masson, pp. 462–576.Google Scholar
Sauriau, P.G. (1991) Spread of Cyclope neritea (Mollusca: Gastropoda) along the north-eastern Atlantic coasts in relation to oyster culture and to climatic fluctuations. Marine Biology 109, 299–309.CrossRefGoogle Scholar
Scagel, R.F. (1956) Introduction of a Japanese alga, Sargassum muticum into the north-east Pacific. Fisheries Research Paper Washington Department of Fisheries 1, 49–58.Google Scholar
Schmidt, O. (1862) Die Spongien des adriatischen Meeres. Leipzig: Wilhelm Engelmann.Google Scholar
Schmidt, O. (1875) Spongien. I. In Die Expedition zur physikalisch-chemischen und biologischen Untersuchung der Nordsee im Sommer 1872. Jahresbericht der Commission zur Wissenschaftlichen Untersuchung der Deutschen Meere in Kiel, Volumes 2–3.Google Scholar
Sim, C.J. and Byeon, H.S. (1989) A systematic study on the marine sponges in Korea. 9. Ceractinomorpha. Korean Journal of Systematic Zoology 5, 33–57.Google Scholar
Simpson, T.L. (1978) The biology of the marine sponge Microciona prolifera (Ellis & Solander) III. Spicule secretion and effect of temperature on spicule size. Journal of Experimental Biology and Ecology 35, 31–42.CrossRefGoogle Scholar
Smaal, A.C., van Stralen, M.R. and Craeymeersch, J. (2005) Does the introduction of the Pacific oyster Crassostrea gigas lead to species shifts in the Wadden Sea? In Dame, R.F. and Olenin, S. (eds) The comparative roles of suspension-feeders in ecosystems. Berlin: Springer-Verlag, pp. 277–289.CrossRefGoogle Scholar
Sollas, W.J. (1885) A classification of the sponges. Annals and Magazine of Natural History 16, 395.CrossRefGoogle Scholar
Thiele, J. (1903) Kieselschwämme von Ternate. II. Abhandlungen Herausgegeben von der Senckenbergischen Naturforschenden Gesellschaft 25, 933–968.Google Scholar
Topsent, E. (1892) Contribution à l'étude des Spongiaires de l'Atlantique Nord (Golfe de Gascogne, Terre-Neuve, Açores). Résultats des Campagnes Scientifiques Accomplies par le Prince Albert I. Monaco 2, 1–165.Google Scholar
Topsent, E. (1928) Spongiaires de l'Atlantique et de la Méditerranée provenant des croisières du Prince Albert ler de Monaco. Résultats des Campagnes Scientifiques Accomplies par le Prince Albert I. Monaco 74, 1–376.Google Scholar
Usio, N., Konishi, M. and Nakano, S. (2001) Species displacement between an introduced and a ‘vulnerable’ crayfish: the role of aggressive interactions and shelter competition. Biological Invasions 3, 179–185.CrossRefGoogle Scholar
Vacelet, J. (2006) New carnivorous sponges (Porifera, Poecilosclerida) collected from manned submersibles in the deep Pacific. Zoological Journal of the Linnean Society 148, 553–584.CrossRefGoogle Scholar
van Soest, R.W.M. (2002) Family Coelosphaeridae Dendy, 1922. In Hooper, J.N.A. and van Soest, R.W.M. (eds) Systema Porifera: a guide to the classification of sponges. New York, Boston, Dordrecht, London and Moscow: Kluwer Academic/Plenum Publishers, pp. 528–546.CrossRefGoogle Scholar
van Soest, R.W.M., de Kluijver, M.J., van Bragt, P.H., Faasse, M., Nijland, R., Beglinger, E.J., de Weerdt, W.H. and de Voogd, N.J. (2007) Sponge invaders in Dutch coastal waters. Journal of the Marine Biological Association of the United Kingdom 87, 1733–1748.CrossRefGoogle Scholar
van Soest, R.W.M. (2009) Isodictya ciocalyptoides. In van Soest R.W.M, Boury-Esnault N., Hooper J.N.A., Rützler K, de Voogd N.J., Alvarez B., Hajdu E., Pisera A.B., Vacelet J., Manconi R., Schoenberg C., Janussen D., Tabachnick K.R. and Klautau M (eds). World Porifera database. Available online at http://www.marinespecies.org/porifera. Consulted on 2010-01-22.Google Scholar
Wasson, K., Zabin, C.J., Bedinger, L., Diaz, C.M. and Pearse, J.S. (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biological Conservation 102, 143–153.CrossRefGoogle Scholar
Webster, N.S. (2007) Sponge disease: a global threat? Environmental Microbiology 9, 1363–1375.CrossRefGoogle ScholarPubMed
Wells, M.J., Poynton, R.J., Balsinhas, A.A., Musil, C.F., Joffe, H., van Hoepen, E. and Abbott, S.K. (1986) The history of introduction of invasive alien plants to southern Africa. In Macdonald, I.A.W., Kruger, F.J. and Ferrar, A.A. (eds) The ecology and management of biological invasions in Southern Africa. Cape Town, South Africa: Oxford University Press, pp. 21–35.Google Scholar
Wiedenmayer, F. (1994) Contributions to the knowledge of post-Palaeozoic neritic archibenthal sponges (Porifera). Schweizerische Paläontologische Abhandlungen 116, 1–147.Google Scholar
Wolff, W.J. and Reise, K. (2002) Oyster imports as a vector for the introduction of alien species into northern and western European waters. In Leppäkoski, E., Gollasch, S. and Olenin, S. (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Dordrecht: Kluwer, pp. 193–205.CrossRefGoogle Scholar
Wolff, W.J. (2005) Non-indigenous marine and estuarine species in the Netherlands. Zoölogische Mededelingen Leiden 79, 3–116.Google Scholar
Zou, L., Zhang, J., Pan, W.-X. and Zhang, Y.-P. (2001) In situ nutrient enrichment experiment in the Bohai & Yellow Sea. Journal of Plankton Research 23, 1111–1119.CrossRefGoogle Scholar