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Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel

Published online by Cambridge University Press:  22 December 2009

Noa Shenkar*
Affiliation:
Biology Department, University of Washington, Seattle, Washington
Yossi Loya
Affiliation:
Department of Zoology, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel
*
Correspondence should be addressed to: N. Shenkar, Biology Department, University of Washington, Seattle, Washington email: [email protected]
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Abstract

One of the most extensively documented marine bioinvasion phenomena is the invasion of Red Sea species to the Mediterranean Sea through the Suez Canal. The present study reports the occurrence of seven non-indigenous ascidian species along the Mediterranean coast of Israel: Ecteinascidia thurstoni, Ascidia cannelata, Phallusia nigra, Rhodosoma turcicum, Symplegma brakenhielmi, Microcosmus exasperatus and Herdmania momus. Five of these species (excluding P. nigra, and R. turcicum) probably reached the Mediterranean via the Suez Canal, since they have an extra-tropical Indo-Pacific distribution and a restricted distribution in the eastern Mediterranean. This is the first record of E. thurstoni in the Mediterranean. The accumulating evidence for the negative impact of non-indigenous ascidians on local species and habitats raises the necessity for long-term studies and monitoring of this group.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Barash, A. and Danin, Z. (1992) Fauna Palestina, Mollusca I, Annotated list of Mediterranean molluscs of Israel and Sinai. Jerusalem: Keter Press Enterprises.Google Scholar
Berrill, N.J. (1950) The Tunicata with an account of the British species. London: Ray Society.Google Scholar
Bitar, G. and Bitar-Kouli, S. (1995) Aperçu de bionomie benthique et répartition des different faciès de la roche littorale à Hannouch (Liban-Méditerranée orientale). Rapport de la Commission Internationale Exploration de la Mer Méditerranée 34, 19.Google Scholar
Bitar, G. and Kouli-Bitar, S. (2001) Nouvelles données sur la faune et la flore benthiques de la côte Libanaise. Migration Lessepsienne. Thalassia Salentina 25, 7174.Google Scholar
Blum, J., Chang, A.L., Liljesthröm, M., Schenk, M.E., Steinberg, M.K. and Ruiz, G.M. (2007) The non-native solitary ascidian Ciona intestinalis (L.) depresses species richness. Journal of Experimental Marine Biology and Ecology 342, 514.Google Scholar
Bourque, D., Davidson, J., MacNair, N.G., Arsenault, G., LeBlanc, A.R., Landry, T. and Miron, G. (2007) Reproduction and early life history of an invasive ascidian Styela clava (Herdman) in Prince Edward Island, Canada. Journal of Experimental Marine Biology and Ecology 342, 7884.CrossRefGoogle Scholar
Bullard, S.G., Lambert, G., Carman, M.R., Byrnes, J., Whitlatch, R.B., Ruiz, G., Miller, R.J., Harris, L., Valentine, P.C., Collie, J.S., Pederson, J., McNaught, D.C., Cohen, A.N., Asch, R.G., Dijkstra, J. and Heinonen, K. (2007) The colonial ascidian Didemnum sp. A: current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. Journal of Experimental Marine Biology and Ecology 342, 99108.Google Scholar
Castilla, J.C., Lagos, N.A. and Cerda, M. (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a midintertidal rocky shore. Marine Ecology Progress Series 268, 119130.Google Scholar
Çinar, M.E., Bilecengolu, M., Öztürk, B. and Can, A. (2006) New records of alien species on the Levantine coast of Turkey. Aquatic Invasions 1, 8490.Google Scholar
Cohen, A.N., Harris, L.H., Bingham, B.L., Carlton, J.T., Chapman, J.W., Lambert, C.C., Lambert, G., Ljubenkov, J.C., Murray, S.N., Rao, L.C., Reardon, K. and Schwindt, E. (2005) Rapid assessment survey for exotic organisms in southern California bays and harbors, and abundance in port and non-port areas. Biological Invasions 7, 9951002.Google Scholar
Coles, S.L., DeFelice, R.C., Eldredge, L.G. and Carlton, J.T. (1999) Historical and recent introductions of non-indigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands. Marine Biology 135, 147158.Google Scholar
Coutts, A.D.M., Moore, K.M. and Hewitt, C.L. (2003) Ships' sea-chests: an overlooked transfer mechanism for non-indigenous marine species? Marine Pollution Bulletin 46, 15101513.CrossRefGoogle ScholarPubMed
Coutts, A.D.M. and Dodgshun, T.J. (2007) The nature and extent of organisms in vessel sea-chests: a protected mechanism for marine bioinvasions. Marine Pollution Bulletin 54, 875886.Google Scholar
Dijkstra, J., Sherman, H. and Harris, L.G. (2007a) The role of colonial ascidians in altering biodiversity in marine fouling communities. Journal of Experimental Marine Biology and Ecology 342, 169171.CrossRefGoogle Scholar
Dijkstra, J., Harris, L.G. and Westerman, E. (2007b) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 342, 6168.CrossRefGoogle Scholar
Fishelson, L. (2000) Marine animal assemblages along the littoral of the Israeli Mediterranean seashore: the Red-Med communities of species. Italian Journal of Zoology 67, 393415.Google Scholar
Gab-Alla, A.A.F.A. (2008) Distribution of the sea squirt Ecteinascidia thurstoni Herdman, 1890 (Ascidiacea: Perophoridae) along Suez Canal and Egyptian Red Sea Coasts. Oceanologia 50, 239253.Google Scholar
Galil, B.S. (2000) A sea under siege—alien species in the Mediterranean. Biological Invasions 2, 77186.CrossRefGoogle Scholar
Galil, B.S. (2007) Seeing red: alien species along the Mediterranean coast of Israel. Aquatic Invasions 2, 281312.Google Scholar
Ghobashy, A.F.A. and Adbel Messeih, M.K. (1991) Ascidians in Egyptian waters. Journal of Egyptian German Society of Zoology 4, 313326.Google Scholar
Golani, D. (1998) Impact of Red Sea fish migrants through the Suez Canal on the aquatic environment of the Eastern Mediterranean. Yale University School of Forestry and Environmental Studies Bulletin 103, 375385.Google Scholar
Izquierdo-Muñoz, A., Diaz-Valdés, M., Ramos-Esplá, A.A. (2007) Non-indigenous ascidians in the Mediterranean Sea. Proceedings of the II International Invasive Sea Squirt Conference, Brudenell, PEI, Canada. October 2007.Google Scholar
Kott, P. (1985) The Australian Ascidiacea. Part 1: Phelobranchiata and Stolidobranchiata. Memoirs of the Queensland Museum 23, 1440.Google Scholar
Kott, P. (1990) The Australian Ascidiacea. Part 2: Aplousobranchia (1). Memoirs of the Queensland Museum 29, 1226.Google Scholar
Kott, P. (1992) The Australian Ascidiacea. Part 3: Aplousobranchia (2). Memoirs of the Queensland Museum 32, 375620.Google Scholar
Kott, P. (2001) The Australian Ascidiacea. Part 4: Aplousobranchia (3), Didemnidae. Memoirs of the Queensland Museum 47, 1407.Google Scholar
Kott, P. (2002) The genus Herdmania Lahille, 1888 (Tunicata, Ascidiacea) in Australian waters. Zoological Journal of the Linnean Society, London 134, 359374.Google Scholar
Kott, P. (2004) Ascidiacea (Tunicata) in Australian waters of the Timor and Arafura Seas. The Beagle, Records of the Museums and Art Galleries of the Northern Territory 2, 3781.Google Scholar
Koukouras, A., Voultsiadou-Koukoura, E., Kevrekidis, T. and Vafidis, D. (1995) Ascidian fauna of the Aegean Sea with a check list of the Eastern Mediterranean and Black Sea species. Annales de l'Institut Océanographique 71, 1934.Google Scholar
Lambert, G. (2001) A global overview of ascidian introductions and their possible impact on the endemic fauna. In Sawada, H., Yokosawa, H. and Lambert, C.C. (eds.) The biology of ascidians. Tokyo: Springer-Verlag, pp. 249257.Google Scholar
Lambert, G. (2002) Nonindigenous ascidians in tropical waters. Pacific Science 56, 291298.Google Scholar
Lambert, G. (2005) Ecology and natural history of the protochordates. Canadian Journal of Zoology 83, 3450.CrossRefGoogle Scholar
Lambert, G. (2007) Invasive sea squirts: a growing global problem. Journal of Experimental Marine Biology and Ecology 342, 34.Google Scholar
Lambert, C.C. and Lambert, G. (1998) Non-indigenous ascidians in southern California harbours and marinas. Marine Biology 130, 675688.CrossRefGoogle Scholar
Lambert, C.C. and Lambert, G. (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Marine Ecology Progress Series 259, 145161.Google Scholar
Lotan, A., Fine, M. and Ben-Hillel, R. (1994) Synchronization of the life cycle and dispersal pattern of the tropical invader scyphomedusan Rhopilema nomadica is temperature dependent. Marine Ecology Progress Series 109, 5965.Google Scholar
Marshall, D.J., Pechenik, J.A. and Keough, M.J. (2003) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Marine Ecology Progress Series 246, 153162.Google Scholar
Mastrototaro, F., Petrocelli, A., Cecere, E. and Matarrese, A. (2004) Non indigenous species settle down in the Taranto seas. Biogeographia 25, 4753.Google Scholar
Millar, R.H. (1971) The biology of ascidians. Advances in Marine Biology 9, 1100.Google Scholar
Monniot, C., Monniot, F. and Laboute, P. (1991) Coral reef ascidians of New Caledonia. Paris: ORSTOM.Google Scholar
Monniot, C. and Monniot, F. (1997) Records of ascidians from Bahrain, Arabian Gulf with three new species. Journal of Natural History 31, 16231643.Google Scholar
Monniot, C. and Monniot, F. (2001) Ascidians from the tropical western Pacific. Zoosystema 23, 201383.Google Scholar
Monniot, C. (2002) Stolidobranch ascidians from the tropical western Indian Ocean. Zoological Journal of the Linnean Society, London 135, 65120.Google Scholar
Naranjo, S.A., Caraballo, J.L. and Garcìa-Gómez, J.C. (1996) Effects of environmental stress on ascidian populations in Algeciras Bay (southern Spain). Possible marine bioindicators? Marine Ecology Progress Series 144, 119131.CrossRefGoogle Scholar
Nishikawa, T. (2002) Revision of the genus Herdmania (Urochordata: Ascidiacea) inhabiting Japanese waters. Species Diversity 7, 217250.Google Scholar
Nomaguchi, T.A., Nishijima, C., Minowa, S., Hashimoto, M., Haraguchi, C., Amemiya, S. and Fujisawa, H. (1997) Embryonic thermosensitivity of the ascidian Ciona savignyi. Zoological Science (Tokyo) 14, 511516.Google Scholar
Pérès, J.M. (1958a) Ascidies recoltees sur les cotes mediterraneannes d'Israel. Bulletin of the Research Council of Israel 7B, 143150.Google Scholar
Pérès, J.M. (1958b) Ascidies de la baie de Haifa collectees par E. Gottlieb. Bulletin of the Research Council of Israel 7B, 151164.Google Scholar
Por, F.D. (1978) Lessepsian migration. The influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Berlin: Springer-Verlag, 228 pp.Google Scholar
Safriel, U.N. and Ritte, U. (1986) Population biology of Suez Canal migration—which way, what kind of species and why? In Karlin, S. and Nevo, E. (eds) Evolutionary processes and theory. Orlando, FL: Academic Press, pp. 561582.Google Scholar
Savigny, J.C. (1816) Mémoires sur les Animoux sans Vertèbres. Part 2. Paris: G. Dufour.Google Scholar
Shenkar, N. (2008) Ecological aspects of the ascidian fauna along the Israeli coast. PhD dissertation. Tel Aviv University.Google Scholar
Shenkar, N. and Loya, Y. (2008) The solitary ascidian Herdmania momus: native (Red Sea) vs. non-indigenous (Mediterranean) populations. Biological Invasions 10, 14311439.Google Scholar
Sims, L.L. (1984) Osmoregulatory capabilities of three macrosympatric stolidobranch ascidians, Styela clava Herdman, S. plicata (Lesueur) and S. montereyensis (Dall). Journal of Experimental Marine Biology and Ecology 82, 117129.Google Scholar
Spanier, E, and Galil, B.S. (1991) Lessepsian migration—a continuous biogeographical process. Endeavour 15, 102106.Google Scholar
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B. and Osman, R.W. (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proceedings of the National Academy of Sciences of the United States of America 99, 1549715500.Google Scholar
Steinitz, H. (1967) A tentative list of immigrants via the Suez Canal. Israel Journal of Zoology 16, 166169.Google Scholar
Steinitz, H. (1970) A critical list of immigrants via the Suez Canal. In The Hebrew University–Smithsonian Institution Joint Program: Biota of the Red Sea and the Eastern Mediterranean, Progress Report. Department of Zoology, Hebrew University Jerusalem, pp. 6474 [mimeo].Google Scholar
Streftaris, N., Zenetos, A. and Papathanassiou, E. (2005) Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanography and Marine Biology: an Annual Review 43, 419453.Google Scholar
Turon, X., Nishikawa, T. and Rius, M. (2007) Spread of Microcosmus squamiger (Ascidiacea: Pyuridae) in the Mediterranean Sea and adjacent waters. Journal of Experimental Marine Biology and Ecology 342, 185188.Google Scholar
Valentine, P.C., Collie, J.S., Reid, R.N., Asch, R.G., Guida, V.G. and Blackwood, D.S. (2007) The occurrence of the colonial ascidian Didemnum sp. on Georges Bank gravel habitat—ecological observations and potential effects on groundfish and scallop fisheries. Journal of Experimental Marine Biology and Ecology 342, 179181.Google Scholar
Van Name, W.G. (1921) Ascidians of the West Indian region and south eastern United States. Bulletin of the American Museum of Natural History 44, 283494.Google Scholar
Van Name, W.G. (1931) New North and South American ascidians. Bulletin of the American Museum of Natural History 61, 207227.Google Scholar
Van Name, W.G. (1945) The North and South American ascidians. Bulletin of the American Museum of Natural History 84, 1476.Google Scholar
Wasson, K., Zabinc, C.J., Bedinger, L., Diaz, M.C., Pearse, J.S. (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biological Conservation 102, 143153.CrossRefGoogle Scholar