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Marine Pollution Bulletin 56 (2008) 620–628 www.elsevier.com/locate/marpolbul


Phytoplankton invasions: Comments on the validity of categorizing the non-indigenous dinoflagellates and diatoms in European Seas
´ mez * Fernando Go
´ anographie et de Bioge ´ ochimie, CNRS UMR 6535, Centre d’Oce ´ anologie de Marseille, Laboratoire d’Oce ´ de la Me ´ diterrane ´ e, 163 Avenue de Luminy, Case 901, F-13288 Marseille, France Universite

Abstract The validity of categorizing the diatoms and dinoflagellates reported in the literature as non-indigenous phytoplankton in the European Seas was investigated. Species that are synonymous are often included as separate species (Gessnerium mochimaensis = Alexandrium monilatum, Gymnodinium nagasakiense = Karenia mikimotoi, Pleurosigma simonsenii = P. planctonicum), while other species names are synonyms of cosmopolitan taxa (Prorocentrum redfieldii = P. triestinum, Pseliodinium vaubanii = Gyrodinium falcatum, Gonyaulax grindleyi=Protoceratium reticulatum, Asterionella japonica = Asterionellopsis glacialis). Epithets of an exotic etymology (i.e. japonica, sinensis, indica) imply that a cosmopolitan species may be non-indigenous, and several taxa are even considered as non-indigenous in their type locality (Alexandrium tamarense and A. pseudogoniaulax). The records of Alexandrium monilatum, A. leei and Corethron criophilum are doubtful. Cold or warm-water species expand their geographical ranges or increase their abundances to detectable levels during cooling (Coscinodiscus wailesii) or warming periods (Chaetoceros coarctatus, Proboscia indica, Pyrodinium bahamense). These are a few examples of marginal dispersal associated with climatic events instead of species introductions from remote areas. The number of non-indigenous phytoplankton species in European Seas has thus been excessively inflated. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Introduced species; Invasive diatoms; Non-native dinoflagellates; Mediterranean-Black Seas; Atlantic; Baltic

1. Introduction Climate change (‘global warming’) and eutrophication are expected to alter the species composition of local planktonic communities as well as increase their susceptibility to invasion by exotic species (Nehring, 1998; OcchipintiAmbrogi, 2007). Human activities are responsible for the massive transfer of species between the different oceans of the world. This happens particularly when ships take on ballast water in one harbour and pump it out in another, frequently in a different part of the world (Carlton, 1985). A non-indigenous species, also known as exotic, introduced, invasive, alien or non-native (OcchipintiAmbrogi and Galil, 2004), is a species that is brought to


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a place well-separated in time and place from its native range where it is able to reproduce and establish a population. This may be caused directly or indirectly by human activity. It is generally assumed that (1) a non-indigenous species colonizes a new area where it did not previously occur, (2) extension of its range is linked, directly or indirectly to human activity and (3) there is a remote dispersal, i.e. geographical discontinuity between its native area and the new area (Boudouresque and Verlaque, 2002). This means that marginal dispersal, i.e. occasional advance of a species at the frontiers of its native range (advances or withdrawals that are linked to climatic episodes) should not be considered an invasion. If it is not known for certain whether a species is native or introduced, it can be labelled cryptogenic, meaning that further study to determine its geographic origin is required (Carlton, 1996). Within the context of the decrease in taxonomic expertise (Cotterill, 1995), the reviews providing lists of

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´ mez / Marine Pollution Bulletin 56 (2008) 620–628 F. Go


non-indigenous phytoplankton in European Seas have proliferated in the last decade (Boalch, 1994; Eno et al., 1997; Nehring, 1998; Reise et al., 1999; Leppa ¨ koski et al., 2002; Paavola et al., 2005; Streftaris et al., 2005; Wolff, 2005; Gollasch, 2006; ICES, 2007). The species listed are similar among the lists and usually there is not a critical study of the validity of these non-indigenous species. The aim of the present study is to discuss the validity of the taxa. Among the numerous inventories in the literature, this study will discuss the list of species reported by Streftaris et al. (2005) because it is recent, complete and available in a high impact and prestigious journal. Streftaris et al. (2005, p. 444) listed 53 species of non-indigenous marine phytoplankton in the European Seas subdivided among the Arctic, Baltic, North, Atlantic, Mediterranean and Black Seas. The list includes 25 dinoflagellates (Table 1), 15 diatoms (Table 2) and 9 flagellates. Their list of phytoplankton includes four seaweeds: Gymnophycus hapsipho-

rus Huisman et Kraft, Platysiphonia caribaea Ballantine et Wynne, Scageliopsis patens Wollaston and Symphyocladia marchantioides (Harvey) Falkenberg. The freshwater dinoflagellates Gymnodinium uberrimum and Pfiesteria piscicida were also listed. Several entries are duplicated due to the inclusion of commonly accepted synonyms such as Gessnerium mochimaensis (=Alexandrium monilatum), Gymnodinium nagasakiense (=Gymnodinium mikimotoi) and Pleurosigma simonsenii (=Pleurosigma planctonicum). The nomenclature and synonymy of the dinoflagellates listed by Streftaris et al. (2005) has been corrected accord´ mez (2005). ing to Go 2. Non-indigenous species in the European Atlantic (Arctic, Baltic, North, Atlantic) The European Atlantic waters, especially the North Sea and the Scandinavian coasts, accounted for the largest his-

Table 1 List of non-indigenous dinoflagellates in European Seas according to Streftaris et al. (2005) Name (as reported by Streftaris et al., 2005) Alexandrium andersoni [M] Alexandrium catenella [M] Alexandrium leei [At, N] Alexandrium minutum [At] Alexandrium monilatum [Bl] Alexandrium pseudogonyaulax [M] Alexandrium tamarense [At, B, M, N] Coolia monotis [M] Gesnerium mochimaensis [Bl] Gonaulax grindley [M] Gymnodinium breve [M] Gymnodinium catenatum [At, B, M, N] Gymnodinium cf. nagasakiense [At] Gymnodinium mikimotoi [B, N] Gymnodinium uberrimum [Bl] Gyrodinium aureolum [At, M, N] Ostreopsis lenticularis [M] Ostreopsis ovata [M] Pfiesteria piscida [N] Prorocentrum mexicanum [M] Prorocentrum minimum [B, N] Prorocentrum redfieldii [N] Pseliodinium vaubanii [M] Pyrodinium bahamense [At] Scrippsiella trochoidea [Bl] Correct and accepted name A. andersonii Balech A. catenella (Whedon et Kofoid) Balech A. A. A. A. leei Balech minutum Halim monilatum (Howell) Balech pseudogoniaulax (Biecheler) Horiguchi ex Kita et Fukuyo Comments Difficult identification, overlooked Difficult identification, overlooked with A. tamarense Doubtful record Marginal dispersal Doubtful record Native species Native species, marginal dispersal Underinvestigated, undersampled Synonym, doubtful record Synonym of a cosmopolitan species Difficult identification, misidentification Cryptogenic species Synonym, difficult identification Difficult identification, probably reported in ancient literature Common European freshwater species Difficult identification, marginal dispersal Underinvestigated, undersampled, difficult identification Underinvestigated, undersampled, difficult identification Freshwater/estuarine, difficult identification Difficult identification, probably reported in ancient literature Marginal dispersal Synonym, marginal dispersal Cosmopolitan Marginal dispersal Native

A. tamarense (Lebour) Balech C. monotis Meunier Alexandrium monilatum (Howell) Balech) (=Gessnerium mochimaensis Halim ex Halim) ` de et Lachmann) Bu Protoceratium reticulatum (Clapare ¨ tschli (=Gonyaulax grindleyi Reinecke) Karenia brevis (Davis) G. Hansen et Moestrup G. catenatum Graham Karenia mikimotoi (Miyake et Kominami ex Oda) G. Hansen et Moestrup (=G. nagasakiense Takayama et Adachi) Karenia mikimotoi (Miyake et Kominami ex Oda) G. Hansen et Moestrup G. uberrimum (Allman) Kofoid et Swezy Gymnodinium aureolum (Hulburt) G. Hansen (non K. mikimotoi) O. lenticularis Fukuyo O. ovata Fukuyo Pfiesteria piscicida Steidinger et Burkholder P. mexicanum Osorio-Tafall (non P. rhathymum) P. minimum (Pavillard) Schiller Prorocentrum redfieldii Bursa (=? P. triestinum Schiller) Gyrodinium falcatum Kofoid et Swezy (=Gymnodinium fusus Schu ¨ tt) P. bahamense Plate var. bahamense S. trochoidea (Stein) Balech ex Loeblich III

Please note the misspelling of some taxa. Regions between brackets: [Ar = Arctic; At = Atlantic; B = Baltic; Bl = Black; M = Mediterranean; N = North].


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Table 2 List of non-indigenous diatoms in European Seas according to Streftaris et al. (2005) Name (as reported by Streftaris et al., 2005) Asterionella japonica [Bl] Chaetoceros coarctatus [M] Corethron criophilum [N] Coscinodiscus wailesii [At, B, N] Odontella sinensis [At, B, N] Pleurosigma planctonicum [At] Pleurosigma simonsenii [B, N] Pleurosira leavis cf. polymorpha [B] Rhizosolenia (=Pseudosolenia) calcar-avis [Bl] Rhizosolenia indica [M, N] Stephanopyxis palmeriana [N] Thalassiosira hendeyi [N] Thalassiosira nordenskioeldii [Bl] Thalassiosira punctigera [B, N] Thalassiosira tealata [N] Correct and accepted name Asterionellopsis glacialis (Castracane) Round Ch. coarctatus Lauder C. criophilum Castracane C. wailesii Gran et Angst O. sinensis (Greville) Grunow P. planctonicum Cleve-Euler or P. planctonicum R. Simonsen? P. simonsenii Hasle (=P. planctonicum R. Simonsen) ` re P. laevis f. polymorpha (Grunow in Van Heurck) Compe Pseudosolenia calcar-avis (Schultze) Sundstro ¨m ´ ndez-Becerril Proboscia indica (H. Peragallo) Herna S. palmeriana (Greville) Grunow T. hendeyi Hasle et Fryxell (=Coscinodiscus hustedtii Mu ¨ llerMelchers) T. nordenskioeldii Cleve T. punctigera (Castracane) Hasle T. tealata Takano Comments Synonym, cosmopolitan Marginal dispersal Misidentification for C. hystrix Marginal dispersal Cosmopolitan Synonym, difficult identification Difficult identification, overlooked Native, complex nomenclature Native, marginal dispersal Marginal dispersal Cosmopolitan, ?S. turris Difficult identification, overlooked Marginal dispersal Cosmopolitan, misidentified Difficult identification, overlooked

Regions between brackets: [Ar = Arctic; At = Atlantic; B = Baltic; Bl = Black; M = Mediterranean; N = North].

torical dataset and traditionally the highest concentration of taxonomic expertise. In open waters, the Continuous Plankton Recorder survey provides a long-term dataset of plankton abundance in the North Atlantic and North Sea. The survey has been running for almost 70 years with a sampling that is restricted to 10 m depth. The organisms are captured on a silk 270 lm mesh and preserved in boraxbuffered formalin (Warner and Hays, 1994). This sampling procedure is inappropriate for most of the phytoplankton species. The usefulness of the Continuous Plankton Recorder is restricted to capturing large diatoms such as Coscinodiscus wailesii or large armoured dinoflagellates such as Ceratium spp. (Edwards et al., 2001). Recent studies based on non-concentrated samples showed the northwards spreading of warm-water diatoms along the European ´ mez and Souissi, 2007). Atlantic waters (Go 2.1. Non-indigenous dinoflagellates in the European Atlantic Ocean The identification at the species level of the unarmoured dinoflagellates is often difficult. Fixation causes cell deformation and the live cells viewed with a microscope also cease to move and begin to disintegrate. The main problem when identifying the species is an almost immediate disappearance of the structures such as the apical groove currently used for the differentiation of the species. More than one hundred species of unarmoured dinoflagellates were described from the European Atlantic coasts in the late 19th and the beginning of 20th century (Pouchet, 1885; Lebour, 1925). These ancient descriptions are often insufficient in properly recognizing the species. The globally distributed Gymnodinium mikimotoi species complex, Karenia mikimotoi (Miyake et Kominami ex Oda) G. Hansen et Moestrup (=Gymnodinium nagasakiense

Takayama et Adachi), is a common bloom-forming species in the European Atlantic. The epithets ‘‘mikimotoi” and ‘‘nagasakiense” are exotic in Europe and Karenia mikimotoi tends to be considered as a non-indigenous species. Before the description of G. mikimotoi in Japan, numerous gymnodinioid cells (such as Gymnodinium punctatum Pouchet, Gymnodinium minus Lebour, Gyrodinium lingulifera Lebour and Gymnodinium pygmaeum Lebour) that may have corresponded to Karenia mikimotoi were described in the European Atlantic coasts. There is no reason to consider K. mikimotoi as non-indigenous simply because the description by Japanese researchers was more detailed. Another species, Gymnodinium aureolum (Hulburt) G. Hansen, was until recently considered a synonym of K. mikimotoi (Hansen et al., 2000). Gymnodinium aureolum was described from the North American Atlantic coasts and there is not a geographical separation that justified the consideration as an introduced species, more than simple transport by the North Atlantic current circulation. The toxic dinoflagellate Gymnodinium catenatum is considered as an introduced species in several world regions. This taxon received much attention in the 1980s and 1990s in alarmist articles with titles such as ‘‘Gymnodinium catenatum in Europe: a growing problem” for its supposed spread along the English Channel and the North Sea (Nehring, 1995). However, the large colonies of G. catenatum never proliferated in the English Channel and the North Sea. More rigorous studies revealed that G. catenatum was misidentified with the non-toxic species Gymnodinium nolleri Ellegaard et Moestrup, which only forms chains of two cells (Ellegaard and Moestrup, 1999). In other cases, the records of G. catenatum corresponded to G. impudicum (Fraga et Bravo) G. Hansen et Moestrup or G. microreticulatum Bolch, Negri et Hallegraeff (Fraga et al., 1995; Bolch et al., 1999). The European G. catenatum was first

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detected in the Iberian Atlantic coasts in 1976, and recurrent blooms were recorded until 1995. Amorim and Dale (2006) reported the presence of G. catenatum cysts back to the turn of the 20th century (c. 1898) off the Iberian Peninsula. The abundance of G. catenatum seems to show important oscillations, and until this phenomenon is completely understood, this taxon should be considered as a cryptogenic species. The identification of armoured dinoflagellates is usually easier than for the unarmoured forms. However, the identification of the species of Alexandrium Halim is also difficult. Since Balech re-described Alexandrium minutum Halim in 1989, more than 30 morphospecies have been reported. Delineations between species are made on the basis of plate shape, attachment and pore locations (Balech, 1995). However, these features may not be stable characters. The type species, A. minutum, described from the Mediterranean Sea, is distributed worldwide (Lilly et al., 2005). In European Atlantic waters A. minutum was described as A. ibericum Balech and A. lusitanicum Balech and was also cited as A. angustitabulatum F.J.R. Taylor. Lilly et al. (2005) concluded that all of the European A. minutum are closely related, and may originate from the same ancestral population. In Europe, Alexandrium leei Balech, described from the Korean coasts, is restricted to one record from the Dutch coasts, and lacks illustrations and rigorous study (Koeman, 1997). It is surprising to find Alexandrium tamarense listed as non-indigenous in the European Atlantic. Its basionym, Gonyaulax tamarensis Lebour, was described from the Tamar Estuary near Plymouth (Lebour, 1925) and it has been recorded as A. excavatum (Braarud) Balech et Tangen on the Norwegian coasts. Pyrodinium bahamense Plate var. bahamense is a toxic species described from the tropical North Atlantic Ocean. I was unable to find any reference reporting plankton cells of P. bahamense in European waters. If reported, the sporadic records result from marginal dispersal by warm Atlantic currents. Prorocentrum redfieldii Bursa, described from the North American Atlantic coasts, is considered to be a synonym of the common species P. triestinum Schiller (Dodge, 1975). Even if P. redfieldii is considered as a separate species, there is no geographical discontinuity between its native area and the European Atlantic waters. Prorocentrum minimum, described from the Gulf of Lions (NW Mediterranean), tends to show high abundance in eutrophic shallow environments. This taxon was later described as P. triangulatum Martin and P. cordiformis Bursa in North American Atlantic coasts and Exuviaella mariae-lebouriae Parke et Ballantine in the European Atlantic coasts. Blooms attributed to P. balticum (Lohmann) Loeblich III along European coasts may correspond to P. minimum (Silva, 1985). The species Exuviaella cordata Ostenfeld, reported from the Caspian and Black Seas, may be a conspecific of P. minimum (Velikova and Larsen, 1999). The increase of eutrophication levels in brackish environments such as

the Baltic Sea may favour the proliferation of this native European species. 2.2. Non-indigenous diatoms in the European Atlantic Ocean Odontella sinensis is a large, easily identifiable species and is widely distributed in European waters. It was described from the warm-waters of the China Sea in one of the earlier phytoplankton studies (Greville, 1866). According to Eno et al. (1997) and Wyatt and Carlton (2002), O. sinensis was first detected in the North Sea in 1889. I am unable to find records in the literature before 1903 (Ostenfeld, 1908). Before 1889 or 1903, the studies and sample coverage of phytoplankton were scarce. Stephanopyxis palmeriana (Greville) Grunow, as well as Odontella sinensis, was described from warm Chinese waters (Greville, 1865) and it is largely known from the European Atlantic (Drebes, 1966). It is not easy to differentiate from Stephanopyxis turris (Greville et Arnott in Gregory) Ralfs in Pritchard, since the earlier studies of both taxa are largely confused with each other. It is risky to consider O. sinensis and S. palmeriana as introduced species in European waters. Coscinodiscus wailesii, first detected off Plymouth in January 1977, is a very large diatom easily collected by net sampling. Despite the high number of specimens available for examination and its large size, it was initially misidentified as Coscinodiscus nobilis (Boalch and Harbour, 1977a; Robinson et al., 1980). Coscinodiscus wailesii was described in a difficult-to-access publication from the Canadian Pacific coast and may have gone unnoticed (Gran and Angst, 1931). Ballast water transport or introduction through the importation of oysters was hypothesized as a potential vector of introduction in Europe ´ and Paulmier, 1986; Reise et al., 1999). Coscinodis(Rince cus wailesii received much attention after the unusual proliferation in January 1977 (Boalch and Harbour, 1977a). This date coincided with the final years of the 1961–79 cooling period, a short period of negative values of the winter North Atlantic Oscillation index, and the arrival of the ‘Great Salinity Anomaly’ to the European Atlantic (Southward et al., 2005; Belkin et al., 1998). Coscinodiscus wailesii showed high abundances between 1977 and 1990 and is currently restricted to residual populations during the winter (Boalch, 1987; Edwards et al., 2001). The unusual climatic conditions in 1977 may have induced the proliferation of C. wailesii, attracting the attention of researchers. It cannot be ruled out that some of the records of Coscinodiscus nobilis Grunow, C. centralis Ehrenberg, C. concinnus W. Smith or C. janischii A. Schmidt prior to the 1980’s may correspond to C. wailesii. Odontella sinensis and Coscinodiscus wailesii are two large diatoms. Their large size and robust nature facilitate collection and their identification. However, Thalassiosira punctigera has a smaller size (50 lm in diameter) and the net sampling may damage the valve processes that are essential for species identification. The type species,


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Ethmodiscus punctiger Castracane, was described from the Tokyo Bay (Castracane, 1886). Coscinodiscus verecundus Mann, described from the Okhotsk Sea (Mann, 1907), is considered a synonym (Hasle, 1983). Another synonym, Thalassiosira japonica Kisselev, was later described from the Sea of Japan. In the boreal North Pacific, also the same type locality for Coscinodiscus wailesii, Gran and Angst (1931) described Coscinodiscus angstii Gran (now Thalassiosira angstii (Gran) Makarova), which is also considered a synonym of T. punctigera. According to Hasle (1983), T. punctigera is an extremely variable species with regard to size and valve structure and it may be confused with other species. Hasle (1983) described ‘‘a widely distributed marine planktonic diatom” that reflected the cosmopolitan character of this taxon. Other diatoms began to receive attention after the proliferation of C. wailesii in 1977, and in 1978, T. punctigera was also considered a non-indigenous species (Kat, 1982). The epithet of Corethron criophilum refers to the cold water preference of this taxon described from the Antarctic Ocean (Castracane, 1886). Curiously, it has been reported in the European Atlantic as a thermophilic species (Nehring, 1998). Crawford et al. (1998) reviewed the genus and reported three species: Corethron pennatum (Grunow) Ostenfeld (=C. criophilum) and C. inerme Karsten occur in Antarctic and South Atlantic Oceans, whereas C. hystrix Hensen is found in the North Atlantic and North Pacific (Crawford et al., 1998). The records of C. criophilum in the European Atlantic waters seem to be misidentifications of the native C. hystrix. According to Eno et al. (1997) and Wyatt and Carlton (2002), Thalassiosira tealata Takano appeared for the first time in the south of England in 1950. Thalassiosira tealata was described from Japanese waters in 1980 (Takano, 1980). It is confusing to have a citation of a species 30 years before it was described. Despite its abundance in Japanese waters, T. tealata was described relatively late due to the difficulty of identification. Consequently, it is highly probable that T. tealata may have been misidentified with other Thalassiosira species in the past. Pleurosira laevis f. polymorpha showed the difficulties associated with variable morphology denoted by ‘‘polymorpha” and its complex historical nomenclature. Pleuros` re ira laevis f. polymorpha (Grunow in Van Heurck) Compe ` re (=Bidis a form of Pleurosira laevis (Ehrenberg) Compe dulphia laevis Ehrenberg, =Cerataulus laevis (Ehrenberg) Ralfs in Pritchard) that also received the name Biddulphia polymorpha (Grunow in Van Heurck) Wolle (=Cerataulus polymorphus Grunow in Van Heurck). This taxon, historically known from European waters, is a native species. Generally, the identification of the pennate diatom species is more difficult than for centric diatoms. The identification of the benthic or tychoplanktonic species of the genus Pleurosigma, usually found in coastal or estuarine environments, is especially difficult. The lack of authority in the species names is a common feature in the lists of non-indigenous species. This makes the differentiation of

the homonyms difficult. Two species were described under the name Pleurosigma planctonicum: P. planctonicum Cleve–Euler from the European Atlantic (Cleve-Euler, 1952) and P. planctonicum R. Simonsen from the Arabian Sea (Simonsen, 1974). In addition, Schrader and Fenner (1976) described the fossil diatom Pleurosigma planktonicum H.J. Schrader from the Norwegian Sea. In order to solve the homonymy, Hasle and Syvertsen (1996) proposed P. simonsenii Hasle for the later homonym P. planctonicum R. Simonsen. Consequently if P. planctonicum refers to P. planctonicum R. Simonsen, it is a repetition of P. simonsenii or it refers to P. planctonicum Cleve-Euler, which is a native species. Boalch and Harbour (1977b) observed P. planctonicum R. Simonsen in 1966 in the English Channel. The difficult identification of this pennate diatom and the scarce information preclude considering this taxon as a non-indigenous species. 3. Mediterranean Sea The Mediterranean Sea has a complex environmental history as a remnant of the extensive Tethys Ocean in the Triassic (c. 200 Ma BP). In the Miocene (c. 10 Ma BP), the Isthmus of Suez was formed, isolating the Mediterranean from the Indo-Pacific Ocean. Toward the end of the Miocene, the connection with the Atlantic Ocean closed and the Messinian salinity crisis led to nearly complete evaporation of the sea (c. 5.96 Ma BP). The Messinian salinity crisis ended 5.33 Ma BP, during the Pliocene, with the re-opening of the Strait of Gibraltar and the inundation of the Mediterranean by Atlantic waters along with plankton. During the Quaternary, the alternating ice ages and warm interglacial periods resulted in a repopulation of the Mediterranean with boreal or subtropical species (Bianchi and Morri, 2000). Since 1869, the Suez Canal, a narrow man-made channel, has connected the Mediterranean and the Indian Ocean with a northbound migration of Erythrean invaders, formerly Lessepsian migrants. The Mediterranean coasts of France and Italy fortunately have a rich historical tradition of phytoplankton taxonomy studies. However, other regions, especially along the Afri´ mez (2006a) can coasts have received less attention. Go reviewed the endemic and Indo-Pacific dinoflagellates in the Mediterranean Sea. 3.1. Non-indigenous dinoflagellates in the Mediterranean Sea The species Alexandrium pseudogoniaulax (=Goniodoma pseudogoniaulax Biecheler) was described from the Gulf of Lions (Biecheler, 1952) and consequently, should not be considered as non-indigenous in the Mediterranean Sea. Alexandrium tamarense, described from the European Atlantic (Lebour, 1925), is the type of A. tamarense species complex, a group that included other taxa of difficult identification such as Alexandrium catenella (Whedon et Kof´ n et al., 2005). Alexandrium oid) Balech (Ruiz Sebastia tamarense is largely cited in the Mediterranean Sea

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´ mez, 2003a) and A. catenella was first noted in 1983 (Go (Margalef and Estrada, 1987; Lilly et al., 2002). Alexandrium andersonii is also included as a non-indigenous dinoflagellate in the Mediterranean. This taxon was recently described from the North American Atlantic coasts (Balech, 1990). Ciminiello et al. (2000) reported A. andersonii in a culture germinated from a cyst collected in the Bay of Naples. The difficulties in the identification of the Alexandrium species are responsible because numerous species went unnoticed. For example Elbra ¨ chter in Wyatt and Zingone (2004) hypothesised that the original description of Blepharocysta splendor-maris (Ehrenberg) Stein in the Tyrrhenian Sea may correspond to the species described as Alexandrium balechii (Steidinger) F.J.R. Taylor. Species of Alexandrium in the Mediterranean Sea may have been labelled as Gonyaulax sp., G. tamarensis or Blepharocysta splendor-maris in the past. Gonyaulax grindleyi is a synonym of Protoceratium retic` de et Lachmann) Bu ulatum (Clapare ¨ tschli. Protoceratium reticulatum was described in the North Sea in one of the ` de and pioneer studies of marine phytoplankton (Clapare Lachmann, 1859) and it was reported since the first studies in the Mediterranean Sea. There is no reason to consider Gonyaulax grindleyi as a non-indigenous species in the Mediterranean Sea. Beyond the planktonic species, other benthic or epiphytic toxic species such as Coolia, Ostreopsis and Prorocentrum have received more attention in the last decade. Prorocentrum mexicanum Osorio-Tafall was described in the Gulf of California. Prorocentrum rhathymum Loeblich III, Sherley et R.J. Schmidt, described from the tropical western Atlantic, has been until recently considered a ´ s-Altamirano and synonym of P. mexicanum (Corte ´ n, 2003). Dodge (1975) considered the MediSierra-Beltra terranean species P. ovale (Gourret) Schiller and P. maximum (Gourret) Schiller a synonym of P. mexicanum. However, the synonymies of Prorocentrum proposed by Dodge (1975) were very often considered to be erroneous. While P. mexicanum and P. rhathymum are well investigated, there is a lack of information on P. maximum, and this makes it difficult to confirm the synonymy. In that case, P. maximum has the priority versus P. mexicanum, and obviously it cannot be considered as non-indigenous in the Mediterranean Sea. The species Prorocentrum venetum Tolomio et Cavolo described from the Adriatic Sea is closely related (if not a conspecific) to P. mexicanum (Tolomio and Cavolo, 1985). Another epiphytic species, Coolia monotis Meunier, is cited as a non-indigenous species. However, this taxon has been known in the Mediterranean since the 1930s as Glenodinium monotis (Meunier) Biecheler (Biecheler, 1952). The first studies on benthic/epiphytic toxic dinoflagellates in tropical waters resulted in the relatively recent description of Ostreopsis lenticularis Fukuyo and O. ovata Fukuyo in the Pacific Ocean (Fukuyo, 1981). There have been few studies of the benthic/epiphytic dinoflagellates in the Mediterranean compared to other regions and these

species have simply been recorded when studies were carried out (i.e. Monti et al., 2007). So these new entries should not be considered as recent species introductions in the Mediterranean Sea. Gymnodinium catenatum, an unarmoured dinoflagellate, ´ n and African coasts is also known mainly from the Albora ´ mez, 2003b). In other cases, of the Mediterranean Sea (Go the citations of G. catenatum in the Mediterranean Sea corresponded to the non-toxic Gymnodinium impudicum, described from the Iberian coasts (Fraga et al., 1995). Karenia brevis (=Gymnodinium breve) is responsible for blooms ´ xico. In the Mediterranean Sea, Gymnodiin the Gulf of Me nium breve was cited as responsible for blooms in the coastal Aegean Sea, although the identification needs to be confirmed (Gotsis-Skretas and Frigilos, 1990; Moncheva et al., 2001). Since the formation of the genus Karenia in 2000, numerous new species have been described (Haywood et al., 2004). Beyond K. brevis, other taxa such as K. selliformis and K. papilionacea begin to be cited in the Mediterranean Sea. Karenia species such as K. selliformis may be related to the Mediterranean species Gymnodinium maguelonnense Biecheler (Biecheler, 1939). According to ´ mez et al. (2005) and Go ´ mez (2006b) Karenia papilionaGo cea is only the coastal morphotype, lacking the body extensions of Brachidinium F.J.R. Taylor or Asterodinium Sournia. Brachidinium is reported in the Mediterranean ´ ger (1971). Go ´ mez and Claustre (2003) reported since Le the occurrence of Asterodinium associated with exceptionally warm temperatures in the Tyrrhenian and Ligurian Seas in September 1999. The form Asterodinium is the response of species of Karenia to the thermal stratification associated with high temperatures. There is no reason to consider the species of Karenia as introduced taxa; most of them have been reported in the past as Gymnodinium sp., due to the difficulties in identification. The highly polymorphic Pseliodinium vaubanii Sournia is a synonym of Gyrodinium falcatum Kofoid et Swezy (=Gymnodinium fusus Schu ¨ tt) (Konovalova, 2003). Gyrodinium falcatum or Gymnodinium fusus should not be considered as nonindigenous species in the Mediterranean Sea. 3.2. Non-indigenous diatoms in the Mediterranean Sea According to Streftaris et al. (2005) the non-indigenous diatoms are restricted to two taxa: Chaetoceros coarctatus Lauder and Rhizosolenia indica H. Peragallo. According to Por (1990) Ch. coarctatus was introduced through the Suez Canal. Chaetoceros coarctatus is a widespread tropical species, also recorded in temperate waters of the European Atlantic (Hendey, 1974) and reported even in the colder ´ ˆ ic sub-basins of the Mediterranean Sea (Travers, 1975; Vilic et al., 2002). ´ ndez-BecerProboscia indica (H. Peragallo) D.U. Herna ril (=Rhizosolenia indica) was found previously in the Indian Ocean more than in the Mediterranean or Atlantic. It was historically considered as a variety of the cosmopolitan Rhizosolenia alata Brightwell. Proboscia indica is asso-


´ mez / Marine Pollution Bulletin 56 (2008) 620–628 F. Go

ciated with intrusion of warm oceanic waters in the English Channel and North Sea (Nehring, 1998). Chaetoceros coarctatus and Proboscia indica are widespread warmwater species. The entrance of warm-water species into the Mediterranean is a continuous process favoured by pat´mez terns of circulation through the Strait of Gibraltar (Go et al., 2000). The scarce phytoplankton studies in the ´ n Sea and along the African coasts of the western Albora Mediterranean make the monitoring of this phenomenon difficult. The spreading of diatoms such as Chaetoceros coarctatus and Proboscia indica may be favoured during warming episodes.

4.2. Non-indigenous diatoms in the Black Sea It is surprising to find Asterionella japonica Cleve et Mo ¨ ller listed as a non-indigenous diatom in the Black Sea. It is also an example induced by exotic etymology of the epithet. Wolff (1996) also reported A. japonica as a non-indigenous species in Dutch waters and later corrected the error (Wolff, 2005). Asterionella japonica is a synonym of the common and cosmopolitan species Asterionellopsis glacialis (Castracane) Round. Thalassiosira nordenskioeldii is a typical cold-water species described from Arctic waters. In the current warming period this taxon is restricted to the colder Mediterranean sub-basins such as Gulf of Lions (Travers, 1975) and the ´ et al., 2002). ˆ ic Adriatic Sea (Revelante et al., 1984; Vilic This taxon may have had wider distributions during the last glacial periods. The occurrence of T. nordenskioeldii in the colder waters of the Black Sea is not unexpected. Pseudosolenia calcar-avis (=Rhizosolenia calcar-avis) is a common species in the Mediterranean Sea, and historic evidence of this species is revealed in sediment core samples (Kemp et al., 1999). This taxon entered with the first Mediterranean waters that inundated the Black Sea basin c. 12,000 years ago. It is obvious that distinguishing between elements of the indigenous plankton and newcomers from elsewhere is increasingly difficult. Competent taxonomists and effective monitoring are essential for responding to the challenge of assessing the flow of arriving alien phytoplankton species in European waters. The phytoplankton identification studies require experienced observers, although there is a paucity of well-educated alpha-taxonomists, and their numbers are quickly decreasing (Cotterill, 1995). Instead of generating repetitive lists of doubtful non-indigenous species, direct studies by long-term monitoring plankton programs are essential to detect and evaluate the changes in the phytoplankton communities in the European Seas. Acknowledgements I am supported by a post-doctoral grant of the Ministe´ n y Ciencia #2007-0213. I thank T. rio Espan ˜ ol de Educacio Overton for improving the manuscript and the comments and suggestions of an anonymous reviewer. References
Amorim, A., Dale, B., 2006. Historical cyst record as evidence for the recent introduction of the dinoflagellate Gymnodinium catenatum in the north-eastern Atlantic. Afr. J. Marine Sci. 28, 193–197. Balech, E., 1990. Four new dinoflagellates. Helgol. Meersunters. 44, 387– 396. Balech, E., 1995. The genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Sherkin Island, Cork, Ireland. Belkin, I.M., Levitus, S., Antonov, J., Malmberg, S.A., 1998. ‘‘Great Salinity Anomalies” in the North Atlantic. Prog. Oceanogr. 41, 1–68. Bianchi, C.N., Morri, C., 2000. Marine Biodiversity of the Mediterranean Sea: Situation, problems and prospects for future research. Marine Pollut. Bull. 40, 367–376.

4. Black Sea The Black Sea is an interglacial lake inundated by Mediterranean waters during the sea rise 12,000 years ago. It is a quasi-enclosed basin with the Bosphorus–Dardanelles Strait as the only contact to the world’s oceans and is a highly eutrophic brackish basin with hypoxia in deeper waters. The European intercontinental aquatic transportation system established at the end of the 18th century connects the Baltic and Black Seas through the central European rivers. The phytoplankton studies in the Black Sea are few, usually less rigorous and are often in less accessible literature sources when compared to literature ´ mez about phytoplankton in other European Seas (Go and Boicenco, 2004). The Black Sea has a short history on a geological time scale and consequently all the marine species are recently established.

4.1. Non-indigenous dinoflagellates in the Black Sea The average salinity in the Black Sea is low (17). Freshwater species may temporarily remain near estuaries and even proliferate. Moncheva and Kamburska (2002, p. 48) listed the freshwater dinoflagellates Gymnodinium uberrimum (Allman) Kofoid et Swezy and Gymnodinium fuscum (Ehrenberg) Stein as non-indigenous species. These taxa are common in European reservoirs and lakes and their appearance in estuarine areas of the Black Sea is not unexpected (Wyatt and Carlton, 2002). According to Moncheva et al. (2001) Alexandrium monilatum (Howell) Balech (=Gessnerium mochimaensis Halim) is responsible for blooms in the Black Sea since 1991. Alexandrium monilatum is known from tropical western Atlantic and the Eastern Pacific Ocean. There is no rigorous study to confirm the record of this warm-water species in the cold waters of the Black Sea (only reported by one author, Moncheva et al., 2001). Scrippsiella trochoidea is a wide-spread cosmopolitan species, although under this name, it may have been cited several different species. Scrippsiella trochoidea entered in the Black Sea 12,000 years ago along with the other Mediterranean phytoplankton species.

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