First records of the benthic, bloom-forming, non-toxic dinoflagellate Thecadinium yashimaense (Dinophyceae) in Europe: with special emphasis on the invasion in the North Sea

Helgol Mar Res (2007) 61:157–165 DOI 10.1007/s10152-007-0063-x O RI G I NAL ART I C LE First records of the benthic, bloom-forming, non-toxic dinoXagellate Thecadinium yashimaense (Dinophyceae) in Europe: with special emphasis on the invasion in the North Sea Mona Hoppenrath · Malte Elbrächter · Hannelore Halliger · Reinoud P. T. Koeman · Alexander Krakhmalnyy · Barbara Surek · Katrin Erler · Bernd Luckas Received: 1 June 2006 / Revised: 12 December 2006 / Accepted: 8 January 2007 / Published online: 22 February 2007 © Springer-Verlag and AWI 2007 Abstract Thecadinium yashimaense was recorded for the Wrst time in France, Great Britain, The Netherlands, and Germany. The invasion and establishment of the species in the German Bight was documented reliably and is presented here. The geographic expansion of the species from the North PaciWc to the North Atlantic Ocean is discussed. This bloom-forming, marine, sand-dwelling dinoXagellate was shown to be non-toxic. Also Thecadinium kofoidii, the type species of the genus, was analyzed for potential toxin production and turned out to be non-toxic as well. Keywords Benthos · DinoXagellate · Invasion · Plankton · Thecadinium · Toxins Introduction The number of introduced and established marine species of the North Sea coasts is about 80 and comprises invertebrates, macroalgae, and protists (Reise et al. 1999). It is a very diYcult task to distinguish between real exotics and misinterpreted native species (pseudo-exotics), which were discovered late but may have been around long before without being noticed (Reise et al. 1999). This is especially true for small organisms like phytoplankton and protist taxa. Methodological problems and extrinsic factors (Lee and Patterson 1998) make it diYcult to prove the exoticsstatus of protists (Elbrächter 1999). There are only a few examples of well documented invasions of planktonic Communicated by H.-D. Franke. M. Hoppenrath Biologische Anstalt Helgoland, Alfred Wegener Institute for Polar and Marine Research, Kurpromenade, 27498 Helgoland, Germany M. Hoppenrath (&) Department of Botany, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4 Canada e-mail: M. Elbrächter Deutsches Zentrum für Marine Biodiversität, Wadden Sea Station Sylt, Forschungsinstitut Senckenberg, Hafenstr. 43, 25992 List/Sylt, Germany H. Halliger Wadden Sea Station Sylt, Alfred Wegener Institute for Polar and Marine Research, Hafenstr. 43, 25992 List/Sylt, Germany R. P. T. Koeman Koeman en Bijkerk BV, Kerklaan 30, Haren, The Netherlands A. Krakhmalnyy N.G. Kholodny Institute of Botany, National Academy of Sciences of the Ukraine, 2 Tereschenkovskaya St., 01001 Kiev, Ukraine B. Surek Culture Collection of Algae at the University of Cologne (CCAC), Universität zu Köln, Gyrhofstraße 15, 50931 Köln, Germany K. Erler · B. Luckas Institut für Ernährungswissenschaften, Friedrich-Schiller-Universität, Dornburger Str. 25, 07743 Jena, Germany 123 158 diatoms into the North Sea, e.g., Odontella sinensis (Greville) Grunow (as Biddulphia sinensis Greville, in Ostenfeld 1908), Thalassiosira punctigera (Castracane) Hasle (Dürselen and Rick 1999), and Coscinodiscus wailesii Gran et Angst (Boalch and Harbour 1977; Dürselen and Rick 1999; Rick and Dürselen 1995; Robinson et al. 1980). Flagellates have rarely been documented as invasive species (Elbrächter 1999), and the only known examples are Karenia mikimotoi (Miyake et Kominami ex Oda) Hansen et Moestrup (as Gyrodinium aureolum Hulburt, in Braarud and Heimdal 1970; Hickel et al. 1971) and Alexandrium leei Balech (Koeman 1997). The possible vectors for the dispersal of non-indigenous species are aquaculture, migratory birds, and ocean going vessels. The transport of protists via ballast water is documented (Galil and Hülsmann 1997; HallegraeV and Bolch 1991, 1992; HallegraeV et al. 1990). Surviving the harsh conditions inside ballast water tanks is a prerequisite for a successful invasion, especially for phototrophic species. Most of them will die because of darkness, but a few cells and cysts can stay alive (Dickmann and Zhang 1999; HallegraeV and Bolch 1992; Yoshida et al. 1996). The ability to form resting cysts is only known for a minority of dinoXagellate species (HallegraeV and Bolch 1992). The awareness of a possible survival of resting cells of phototrophic species is relatively new (e.g., Dickmann and Zhang 1999; Zhang and Dickmann 1999). Resting cells can survive for lengthy periods in ballast water tanks (C.J.S. Bolch, personal communication). There is also the possibility that species may naturally expand their range via ocean currents. Galil and Hülsmann (1997) showed that the protists found in ballast water tanks belong mainly to the benthic communities. Deciding whether a newly recorded benthic protist species is introduced to the North Sea habitat or has been overlooked in the past, is nearly impossible in most cases because knowledge about the species assemblage is missing for nearly all taxa (for example, see Houpt and Hoppenrath 2006). There are no monitoring programs for benthic microalgae/protists, as there are for the phytoplankton community. Moreover, intensive taxonomic investigations and published accounts are missing in many cases. Sand-dwelling dinoXagellates, euglenoids, and ciliates of the North Frisian Wadden Sea are an exception (Hoppenrath 2000a; Hartwig 1973), and dinoXagellates and euglenoids are also documented for the Danish Wadden Sea (Larsen 1985, 1987). Thecadinium yashimaense Yoshimatsu, Toriumi et Dodge was described from Japan (Yoshimatsu et al. 2004). There was some taxonomic confusion about this species (Hoppenrath et al. 2005). The taxon has been 123 Helgol Mar Res (2007) 61:157–165 known for nearly 40 years, Wrst recognized at the North American PaciWc coast, but misidentiWed at that time (Baillie 1971; Hoppenrath et al. 2004). Six marine, sand-dwelling Thecadinium species were observed in the German Wadden Sea (Hoppenrath 2000b; Hoppenrath et al. 2004). Here we present the Wrst records of T. yashimaense in the North Sea and the reliably documented invasion. Shortly before submitting the manuscript we learnt about an isolate of T. yashimaense from France, and we have integrated this information too. Methods Samples and cultures Benthic sand samples were collected with a spoon during low tide, and dinoXagellates were separated from the sand by extraction with melting seawater-ice (Uhlig 1964) through a Wne Wlter (Hoppenrath et al. 2004). They were accumulated in a Petri dish beneath the Wlter and were then identiWed with a Leitz Fluovert FS invert-microscope at 40 to 250£ magniWcation. Sampling sites were in bare, eulittoral regions, south of List Harbor (55°00.85⬘N; 08°06.30⬘E; tidal Xat of 100 m) and at the “Oddewatt” northeast of List (55°01.80⬘N; 08°26.00⬘E; tidal Xat of 500 m). For more details on the sampling sites, see Hoppenrath (2000c). Net samples from surface water near List (55°01.30 (...truncated)