po

nes

o G

NR

e Lu

Abstract

range where it is able to reproduce and establish a popula-

cryptogenic, meaning that further study to determine itsgeographic origin is required (Carlton, 1996).

Within the context of the decrease in taxonomicexpertise (Cotterill, 1995), the reviews providing lists of

* Tel.: +33 491041662; fax: +33 491041643.E-mail address: fernando.gomez@toplancton.com

Available online at www.sciencedirect.com

Marine Pollution Bulletin 56Climate change (global warming) and eutrophicationare expected to alter the species composition of local plank-tonic communities as well as increase their susceptibility toinvasion by exotic species (Nehring, 1998; Occhipinti-Ambrogi, 2007). Human activities are responsible for themassive transfer of species between the dierent oceans ofthe world. This happens particularly when ships take onballast water in one harbour and pump it out in another,frequently in a dierent part of the world (Carlton,1985). A non-indigenous species, also known as exotic,introduced, invasive, alien or non-native (Occhipinti-Ambrogi and Galil, 2004), is a species that is brought to

tion. This may be caused directly or indirectly by humanactivity. It is generally assumed that (1) a non-indigenousspecies colonizes a new area where it did not previouslyoccur, (2) extension of its range is linked, directly or indi-rectly to human activity and (3) there is a remote dispersal,i.e. geographical discontinuity between its native area andthe new area (Boudouresque and Verlaque, 2002). Thismeans that marginal dispersal, i.e. occasional advance ofa species at the frontiers of its native range (advances orwithdrawals that are linked to climatic episodes) shouldnot be considered an invasion. If it is not known for certainwhether a species is native or introduced, it can be labelledThe validity of categorizing the diatoms and dinoagellates reported in the literature as non-indigenous phytoplankton in the Euro-pean Seas was investigated. Species that are synonymous are often included as separate species (Gessnerium mochimaensis = Alexandriummonilatum, Gymnodinium nagasakiense = Karenia mikimotoi, Pleurosigma simonsenii = P. planctonicum), while other species names aresynonyms of cosmopolitan taxa (Prorocentrum redeldii = P. triestinum, Pseliodinium vaubanii = Gyrodinium falcatum, Gonyaulax grind-leyi=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 typelocality (Alexandrium tamarense and A. pseudogoniaulax). The records of Alexandrium monilatum, A. leei and Corethron criophilum aredoubtful. 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 examplesof marginal dispersal associated with climatic events instead of species introductions from remote areas. The number of non-indigenousphytoplankton species in European Seas has thus been excessively inated. 2008 Elsevier Ltd. All rights reserved.

Keywords: Introduced species; Invasive diatoms; Non-native dinoagellates; Mediterranean-Black Seas; Atlantic; Baltic

1. Introduction a place well-separated in time and place from its nativeView

Phytoplankton invasions: Commethe non-indigenous dinoagellat

Fernand

Laboratoire dOceanographie et de Biogeochimie, C

Universite de la Mediterranee, 163 Avenue d0025-326X/$ - see front matter 2008 Elsevier Ltd. All rights reserved.doi:10.1016/j.marpolbul.2007.12.014int

ts on the validity of categorizingand diatoms in European Seas

omez *

S UMR 6535, Centre dOceanologie de Marseille,

miny, Case 901, F-13288 Marseille, France

www.elsevier.com/locate/marpolbul

(2008) 620628

non-indigenous phytoplankton in European Seas have pro-liferated in the last decade (Boalch, 1994; Eno et al., 1997;Nehring, 1998; Reise et al., 1999; Leppakoski et al., 2002;Paavola et al., 2005; Streftaris et al., 2005; Wol, 2005;Gollasch, 2006; ICES, 2007). The species listed are similaramong the lists and usually there is not a critical study ofthe validity of these non-indigenous species. The aim ofthe present study is to discuss the validity of the taxa.

Among the numerous inventories in the literature, thisstudy will discuss the list of species reported by Streftariset al. (2005) because it is recent, complete and availablein a high impact and prestigious journal. Streftaris et al.(2005, p. 444) listed 53 species of non-indigenous marinephytoplankton in the European Seas subdivided amongthe Arctic, Baltic, North, Atlantic, Mediterranean andBlack Seas. The list includes 25 dinoagellates (Table 1),15 diatoms (Table 2) and 9 agellates. Their list of phyto-plankton includes four seaweeds: Gymnophycus hapsipho-

rus Huisman et Kraft, Platysiphonia caribaea Ballantineet Wynne, Scageliopsis patens Wollaston and Symphyocl-adia marchantioides (Harvey) Falkenberg. The freshwaterdinoagellates Gymnodinium uberrimum and Pesteriapiscicida were also listed. Several entries are duplicateddue to the inclusion of commonly accepted synonyms suchas Gessnerium mochimaensis (=Alexandrium monilatum),Gymnodinium nagasakiense (=Gymnodinium mikimotoi)and Pleurosigma simonsenii (=Pleurosigma planctonicum).The nomenclature and synonymy of the dinoagellateslisted by Streftaris et al. (2005) has been corrected accord-ing to Gomez (2005).

2. Non-indigenous species in the European Atlantic (Arctic,

Baltic, North, Atlantic)

The European Atlantic waters, especially the North Seaand the Scandinavian coasts, accounted for the largest his-

Table 1List of non-indigenous dinoagellates in European Seas according to Streftaris et al. (2005)

Name (as reported byStreftaris et al., 2005)

Correct and accepted name Comments

Alexandrium andersoni [M] A. andersonii Balech Dicult identication, overlookedAlexandrium catenella [M] A. catenella (Whedon et Kofoid) Balech Dicult identication, overlooked with

A. tamarense

Alexandrium leei [At, N] A. leei Balech Doubtful recordAlexandrium minutum [At] A. minutum Halim Marginal dispersalAlexandrium monilatum [Bl] A. monilatum (Howell) Balech Doubtful recordAlexandrium pseudogonyaulax

[M]A. pseudogoniaulax (Biecheler) Horiguchi ex Kita et Fukuyo Native species

Alexandrium tamarense

[At, B, M, N]A. tamarense (Lebour) Balech Native species, marginal dispersal

Coolia monotis [M] C. monotis Meunier Underinvestigated, undersampledGesnerium mochimaensis [Bl] Alexandrium monilatum (Howell) Balech) (=Gessnerium mochimaensis

Halim ex Halim)Synonym, doubtful record

Gonaulax grindley [M] Protoceratium reticulatum (Clapare`de et Lachmann) Butschli (=Gonyaulaxgrindleyi Reinecke)

Synonym of a cosmopolitan species

stru

ex

ex

nsen

er

hym

tinu

Gym

F. Gomez /Marine Pollution Bulletin 56 (2008) 620628 621Gymnodinium breve [M] Karenia brevis (Davis) G. Hansen et MoeGymnodinium catenatum

[At, B, M, N]G. catenatum Graham

Gymnodinium cf. nagasakiense[At]

Karenia mikimotoi (Miyake et Kominami(=G. nagasakiense Takayama et Adachi)

Gymnodinium mikimotoi

[B, N]Karenia mikimotoi (Miyake et Kominami

Gymnodinium uberrimum [Bl] G. uberrimum (Allman) Kofoid et SwezyGyrodinium aureolum

[At, M, N]Gymnodinium aureolum (Hulburt) G. Ha

Ostreopsis lenticularis [M] O. lenticularis Fukuyo

Ostreopsis ovata [M] O. ovata Fukuyo

Pesteria piscida [N] Pesteria piscicida Steidinger et Burkhold

Prorocentrum mexicanum [M] P. mexicanum Osorio-Tafall (non P. rhat

Prorocentrum minimum [B, N] P. minimum (Pavillard) SchillerProrocentrum redeldii [N] Prorocentrum redeldii Bursa (=? P. triesPseliodinium vaubanii [M] Gyrodinium falcatum Kofoid et Swezy (=Pyrodinium bahamense [At] P. bahamense Plate var. bahamense

Scrippsiella trochoidea [Bl] S. trochoidea (Stein) Balech ex Loeblich III

Please note the misspelling of some taxa. Regions between brackets: [Ar = Arctip Dicult identication, misidenticationCryptogenic species

Oda) G. Hansen et Moestrup Synonym, dicult identication

Oda) G. Hansen et Moestrup Dicult identication, probably reportedin ancient literatureCommon European freshwater species

(non K. mikimotoi) Dicult identication, marginal dispersal

Underinvestigated, undersampled,dicult identicationUnderinvestigated, undersampled,dicult identicationFreshwater/estuarine, dicultidentication

um) Dicult identication, probably reportedin ancient literatureMarginal dispersal

m Schiller) Synonym, marginal dispersalnodinium fusus Schutt) Cosmopolitan

Marginal dispersal

Native

c; At = Atlantic; B = Baltic; Bl = Black; M =Mediterranean; N = North].

t al

astr

owr oranc

unochu

llouno(=

Has

lack

n Btorical dataset and traditionally the highest concentrationof taxonomic expertise. In open waters, the ContinuousPlankton Recorder survey provides a long-term datasetof plankton abundance in the North Atlantic and NorthSea. The survey has been running for almost 70 years witha sampling that is restricted to 10 m depth. The organismsare captured on a silk 270 lmmesh and preserved in borax-buered formalin (Warner and Hays, 1994). This samplingprocedure is inappropriate for most of the phytoplanktonspecies. The usefulness of the Continuous Plankton Recor-der is restricted to capturing large diatoms such as Coscin-

Table 2List of non-indigenous diatoms in European Seas according to Streftaris e

Name (as reported by Streftaris et al., 2005) Correct and accepted name

Asterionella japonica [Bl] Asterionellopsis glacialis (CChaetoceros coarctatus [M] Ch. coarctatus LauderCorethron criophilum [N] C. criophilum CastracaneCoscinodiscus wailesii [At, B, N] C. wailesii Gran et AngstOdontella sinensis [At, B, N] O. sinensis (Greville) GrunPleurosigma planctonicum [At] P. planctonicum Cleve-EulePleurosigma simonsenii [B, N] P. simonsenii Hasle (=P. pl

Pleurosira leavis cf. polymorpha [B] P. laevis f. polymorpha (GrRhizosolenia (=Pseudosolenia) calcar-avis

[Bl]Pseudosolenia calcar-avis (S

Rhizosolenia indica [M, N] Proboscia indica (H. PeragaStephanopyxis palmeriana [N] S. palmeriana (Greville) GrThalassiosira hendeyi [N] T. hendeyi Hasle et Fryxell

Melchers)Thalassiosira nordenskioeldii [Bl] T. nordenskioeldii CleveThalassiosira punctigera [B, N] T. punctigera (Castracane)Thalassiosira tealata [N] T. tealata Takano

Regions between brackets: [Ar = Arctic; At = Atlantic; B = Baltic; Bl = B

622 F. Gomez /Marine Pollutioodiscus wailesii or large armoured dinoagellates such asCeratium spp. (Edwards et al., 2001). Recent studies basedon non-concentrated samples showed the northwardsspreading of warm-water diatoms along the EuropeanAtlantic waters (Gomez and Souissi, 2007).

2.1. Non-indigenous dinoagellates in the European Atlantic

Ocean

The identication at the species level of the unarmoureddinoagellates is often dicult. Fixation causes cell defor-mation and the live cells viewed with a microscope alsocease to move and begin to disintegrate. The main problemwhen identifying the species is an almost immediate disap-pearance of the structures such as the apical groove cur-rently used for the dierentiation of the species. Morethan one hundred species of unarmoured dinoagellateswere described from the European Atlantic coasts in thelate 19th and the beginning of 20th century (Pouchet,1885; Lebour, 1925). These ancient descriptions are ofteninsucient in properly recognizing the species.

The globally distributed Gymnodinium mikimotoi speciescomplex, Karenia mikimotoi (Miyake etKominami ex Oda)G. Hansen et Moestrup (=Gymnodinium nagasakienseTakayama et Adachi), is a common bloom-forming speciesin the European Atlantic. The epithets mikimotoi andnagasakiense are exotic in Europe and Karenia mikimo-toi tends to be considered as a non-indigenous species.Before the description of G. mikimotoi in Japan, numerousgymnodinioid cells (such as Gymnodinium punctatum Pou-chet, Gymnodinium minus Lebour, Gyrodinium linguliferaLebour and Gymnodinium pygmaeum Lebour) that mayhave corresponded to Karenia mikimotoi were describedin the European Atlantic coasts. There is no reason to con-sider K. mikimotoi as non-indigenous simply because the

. (2005)

Comments

acane) Round Synonym, cosmopolitanMarginal dispersalMisidentication for C. hystrixMarginal dispersalCosmopolitan

P. planctonicum R. Simonsen? Synonym, dicult identicationtonicum R. Simonsen) Dicult identication,

overlookedw in Van Heurck) Compe`re Native, complex nomenclatureltze) Sundstrom Native, marginal dispersal

) Hernandez-Becerril Marginal dispersalw Cosmopolitan, ?S. turrisCoscinodiscus hustedtii Muller- Dicult identication,

overlookedMarginal dispersal

le Cosmopolitan, misidentiedDicult identication,overlooked

; M =Mediterranean; N = North].

ulletin 56 (2008) 620628description 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 aureolumwas described from the North American Atlantic coastsand there is not a geographical separation that justiedthe consideration as an introduced species, more than sim-ple transport by the North Atlantic current circulation.

The toxic dinoagellate Gymnodinium catenatum is con-sidered as an introduced species in several world regions.This taxon received much attention in the 1980s and1990s in alarmist articles with titles such as Gymnodiniumcatenatum in Europe: a growing problem for its supposedspread along the English Channel and the North Sea (Neh-ring, 1995). However, the large colonies of G. catenatumnever proliferated in the English Channel and the NorthSea. More rigorous studies revealed that G. catenatumwas misidentied with the non-toxic species Gymnodiniumnolleri Ellegaard et Moestrup, which only forms chains oftwo 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. microreti-culatum Bolch, Negri etHallegrae (Fraga et al., 1995; Bol-ch et al., 1999). The European G. catenatum was rst

n Bdetected in the Iberian Atlantic coasts in 1976, and recur-rent blooms were recorded until 1995. Amorim and Dale(2006) reported the presence of G. catenatum cysts backto the turn of the 20th century (c. 1898) o the Iberian Pen-insula. The abundance of G. catenatum seems to showimportant oscillations, and until this phenomenon is com-pletely understood, this taxon should be considered as acryptogenic species.

The identication of armoured dinoagellates is usuallyeasier than for the unarmoured forms. However, the iden-tication of the species of Alexandrium Halim is also di-cult. Since Balech re-described Alexandrium minutumHalim in 1989, more than 30 morphospecies have beenreported. Delineations between species are made on thebasis of plate shape, attachment and pore locations(Balech, 1995). However, these features may not be stablecharacters. The type species, A. minutum, described fromthe Mediterranean Sea, is distributed worldwide (Lillyet al., 2005). In European Atlantic waters A. minutumwas described as A. ibericum Balech and A. lusitanicumBalech and was also cited as A. angustitabulatum F.J.R.Taylor. Lilly et al. (2005) concluded that all of the Euro-pean A. minutum are closely related, and may originatefrom the same ancestral population. In Europe, Alexandri-um leei Balech, described from the Korean coasts, isrestricted to one record from the Dutch coasts, and lacksillustrations and rigorous study (Koeman, 1997). It is sur-prising to nd Alexandrium tamarense listed as non-indige-nous in the European Atlantic. Its basionym, Gonyaulaxtamarensis Lebour, was described from the Tamar Estuarynear Plymouth (Lebour, 1925) and it has been recorded asA. excavatum (Braarud) Balech et Tangen on the Norwe-gian coasts.

Pyrodinium bahamense Plate var. bahamense is a toxicspecies described from the tropical North Atlantic Ocean.I was unable to nd any reference reporting plankton cellsof P. bahamense in European waters. If reported, the spo-radic records result from marginal dispersal by warmAtlantic currents.

Prorocentrum redeldii Bursa, described from the NorthAmerican Atlantic coasts, is considered to be a synonym ofthe common species P. triestinum Schiller (Dodge, 1975).Even if P. redeldii is considered as a separate species, thereis no geographical discontinuity between its native area andthe European Atlantic waters. Prorocentrum minimum,described from the Gulf of Lions (NW Mediterranean),tends to show high abundance in eutrophic shallow envi-ronments. This taxon was later described as P. triangula-tum Martin and P. cordiformis Bursa in North AmericanAtlantic coasts and Exuviaella mariae-lebouriae Parke etBallantine in the European Atlantic coasts. Blooms attrib-uted to P. balticum (Lohmann) Loeblich III along Euro-pean coasts may correspond to P. minimum (Silva, 1985).The species Exuviaella cordata Ostenfeld, reported fromthe Caspian and Black Seas, may be a conspecic of P.

F. Gomez /Marine Pollutiominimum (Velikova and Larsen, 1999). The increase ofeutrophication levels in brackish environments such asthe Baltic Sea may favour the proliferation of this nativeEuropean species.

2.2. Non-indigenous diatoms in the European Atlantic Ocean

Odontella sinensis is a large, easily identiable speciesand is widely distributed in European waters. It wasdescribed from the warm-waters of the China Sea in oneof the earlier phytoplankton studies (Greville, 1866).According to Eno et al. (1997) and Wyatt and Carlton(2002), O. sinensis was rst detected in the North Sea in1889. I am unable to nd records in the literature before1903 (Ostenfeld, 1908). Before 1889 or 1903, the studiesand sample coverage of phytoplankton were scarce. Steph-anopyxis palmeriana (Greville) Grunow, as well as Odontel-la sinensis, was described from warm Chinese waters(Greville, 1865) and it is largely known from the EuropeanAtlantic (Drebes, 1966). It is not easy to dierentiate fromStephanopyxis turris (Greville et Arnott in Gregory) Ralfsin Pritchard, since the earlier studies of both taxa are lar-gely confused with each other. It is risky to consider O. sin-ensis and S. palmeriana as introduced species in Europeanwaters.

Coscinodiscus wailesii, rst detected o Plymouth in Jan-uary 1977, is a very large diatom easily collected by netsampling. Despite the high number of specimens availablefor examination and its large size, it was initially misiden-tied as Coscinodiscus nobilis (Boalch and Harbour,1977a; Robinson et al., 1980). Coscinodiscus wailesii wasdescribed in a dicult-to-access publication from theCanadian Pacic coast and may have gone unnoticed(Gran and Angst, 1931). Ballast water transport or intro-duction through the importation of oysters was hypothe-sized as a potential vector of introduction in Europe(Rince and Paulmier, 1986; Reise et al., 1999). Coscinodis-cus wailesii received much attention after the unusual pro-liferation in January 1977 (Boalch and Harbour, 1977a).This date coincided with the nal years of the 196179cooling period, a short period of negative values of the win-ter North Atlantic Oscillation index, and the arrival of theGreat Salinity Anomaly to the European Atlantic (South-ward et al., 2005; Belkin et al., 1998). Coscinodiscus wailesiishowed high abundances between 1977 and 1990 and iscurrently restricted to residual populations during the win-ter (Boalch, 1987; Edwards et al., 2001). The unusual cli-matic conditions in 1977 may have induced theproliferation of C. wailesii, attracting the attention ofresearchers. It cannot be ruled out that some of the recordsof Coscinodiscus nobilis Grunow, C. centralis Ehrenberg, C.concinnus W. Smith or C. janischii A. Schmidt prior to the1980s may correspond to C. wailesii.

Odontella sinensis and Coscinodiscus wailesii are twolarge diatoms. Their large size and robust nature facilitatecollection and their identication. However, Thalassiosirapunctigera has a smaller size (50 lm in diameter) and

ulletin 56 (2008) 620628 623the net sampling may damage the valve processes thatare essential for species identication. The type species,

n BEthmodiscus punctiger Castracane, was described from theTokyo Bay (Castracane, 1886). Coscinodiscus verecundusMann, described from the Okhotsk Sea (Mann, 1907), isconsidered a synonym (Hasle, 1983). Another synonym,Thalassiosira japonica Kisselev, was later described fromthe Sea of Japan. In the boreal North Pacic, also the sametype locality for Coscinodiscus wailesii, Gran and Angst(1931) described Coscinodiscus angstii Gran (now Thalass-iosira angstii (Gran) Makarova), which is also considered asynonym of T. punctigera. According to Hasle (1983), T.punctigera is an extremely variable species with regard tosize and valve structure and it may be confused with otherspecies. Hasle (1983) described a widely distributed mar-ine planktonic diatom that reected the cosmopolitancharacter of this taxon. Other diatoms began to receiveattention after the proliferation of C. wailesii in 1977,and in 1978, T. punctigera was also considered a non-indig-enous species (Kat, 1982).

The epithet of Corethron criophilum refers to the coldwater preference of this taxon described from the AntarcticOcean (Castracane, 1886). Curiously, it has been reportedin the European Atlantic as a thermophilic species (Neh-ring, 1998). Crawford et al. (1998) reviewed the genusand reported three species: Corethron pennatum (Grunow)Ostenfeld (=C. criophilum) and C. inerme Karsten occurin Antarctic and South Atlantic Oceans, whereas C. hystrixHensen is found in the North Atlantic and North Pacic(Crawford et al., 1998). The records of C. criophilum inthe European Atlantic waters seem to be misidenticationsof the native C. hystrix.

According to Eno et al. (1997) and Wyatt and Carlton(2002), Thalassiosira tealata Takano appeared for the rsttime in the south of England in 1950. Thalassiosira tealatawas described from Japanese waters in 1980 (Takano,1980). It is confusing to have a citation of a species 30 yearsbefore it was described. Despite its abundance in Japanesewaters, T. tealata was described relatively late due to thediculty of identication. Consequently, it is highly prob-able that T. tealata may have been misidentied with otherThalassiosira species in the past.

Pleurosira laevis f. polymorpha showed the dicultiesassociated with variable morphology denoted by poly-morpha and its complex historical nomenclature. Pleuros-ira laevis f. polymorpha (Grunow in Van Heurck) Compe`reis a form of Pleurosira laevis (Ehrenberg) Compe`re (=Bid-dulphia laevis Ehrenberg, =Cerataulus laevis (Ehrenberg)Ralfs in Pritchard) that also received the name Biddulphiapolymorpha (Grunow in Van Heurck) Wolle (=Ceratauluspolymorphus Grunow in Van Heurck). This taxon, histori-cally known from European waters, is a native species.

Generally, the identication of the pennate diatom spe-cies is more dicult than for centric diatoms. The identi-cation of the benthic or tychoplanktonic species of thegenus Pleurosigma, usually found in coastal or estuarineenvironments, is especially dicult. The lack of authority

624 F. Gomez /Marine Pollutioin the species names is a common feature in the lists ofnon-indigenous species. This makes the dierentiation ofthe homonyms dicult. Two species were described underthe name Pleurosigma planctonicum: P. planctonicumCleveEuler from the European Atlantic (Cleve-Euler,1952) and P. planctonicum R. Simonsen from the ArabianSea (Simonsen, 1974). In addition, Schrader and Fenner(1976) described the fossil diatom Pleurosigma planktoni-cum H.J. Schrader from the Norwegian Sea. In order tosolve the homonymy, Hasle and Syvertsen (1996) proposedP. simonsenii Hasle for the later homonym P. planctonicumR. Simonsen. Consequently if P. planctonicum refers to P.planctonicum R. Simonsen, it is a repetition of P. simonseniior it refers to P. planctonicum Cleve-Euler, which is a nativespecies. Boalch and Harbour (1977b) observed P. plancton-icum R. Simonsen in 1966 in the English Channel. The dif-cult identication of this pennate diatom and the scarceinformation preclude considering this taxon as a non-indig-enous species.

3. Mediterranean Sea

The Mediterranean Sea has a complex environmentalhistory as a remnant of the extensive Tethys Ocean in theTriassic (c. 200 Ma BP). In the Miocene (c. 10 Ma BP),the Isthmus of Suez was formed, isolating the Mediterra-nean from the Indo-Pacic Ocean. Toward the end of theMiocene, the connection with the Atlantic Ocean closedand the Messinian salinity crisis led to nearly completeevaporation of the sea (c. 5.96 Ma BP). The Messiniansalinity crisis ended 5.33 Ma BP, during the Pliocene, withthe re-opening of the Strait of Gibraltar and the inundationof the Mediterranean by Atlantic waters along with plank-ton. During the Quaternary, the alternating ice ages andwarm interglacial periods resulted in a repopulation ofthe Mediterranean with boreal or subtropical species(Bianchi and Morri, 2000). Since 1869, the Suez Canal, anarrow man-made channel, has connected the Mediterra-nean and the Indian Ocean with a northbound migrationof Erythrean invaders, formerly Lessepsian migrants. TheMediterranean coasts of France and Italy fortunately havea rich historical tradition of phytoplankton taxonomystudies. However, other regions, especially along the Afri-can coasts have received less attention. Gomez (2006a)reviewed the endemic and Indo-Pacic dinoagellates inthe Mediterranean Sea.

3.1. Non-indigenous dinoagellates in the Mediterranean Sea

The species Alexandrium pseudogoniaulax (=Goniodomapseudogoniaulax Biecheler) was described from the Gulf ofLions (Biecheler, 1952) and consequently, should not beconsidered as non-indigenous in the Mediterranean Sea.Alexandrium tamarense, described from the EuropeanAtlantic (Lebour, 1925), is the type of A. tamarense speciescomplex, a group that included other taxa of dicult iden-tication such as Alexandrium catenella (Whedon et Kof-

ulletin 56 (2008) 620628oid) Balech (Ruiz Sebastian et al., 2005). Alexandriumtamarense is largely cited in the Mediterranean Sea

n B(Gomez, 2003a) and A. catenella was rst noted in 1983(Margalef and Estrada, 1987; Lilly et al., 2002). Alexandri-um andersonii is also included as a non-indigenous dinoa-gellate in the Mediterranean. This taxon was recentlydescribed from the North American Atlantic coasts(Balech, 1990). Ciminiello et al. (2000) reported A. anderso-nii in a culture germinated from a cyst collected in the Bayof Naples. The diculties in the identication of the Alex-andrium species are responsible because numerous specieswent unnoticed. For example Elbrachter in Wyatt and Zin-gone (2004) hypothesised that the original description ofBlepharocysta splendor-maris (Ehrenberg) Stein in the Tyr-rhenian Sea may correspond to the species described asAlexandrium balechii (Steidinger) F.J.R. Taylor. Speciesof Alexandrium in the Mediterranean Sea may have beenlabelled as Gonyaulax sp., G. tamarensis or Blepharocystasplendor-maris in the past.

Gonyaulax grindleyi is a synonym of Protoceratium retic-ulatum (Clapare`de et Lachmann) Butschli. Protoceratiumreticulatum was described in the North Sea in one of thepioneer studies of marine phytoplankton (Clapare`de andLachmann, 1859) and it was reported since the rst studiesin the Mediterranean Sea. There is no reason to considerGonyaulax grindleyi as a non-indigenous species in theMediterranean Sea.

Beyond the planktonic species, other benthic or epi-phytic toxic species such as Coolia, Ostreopsis and Proro-centrum have received more attention in the last decade.Prorocentrum mexicanum Osorio-Tafall was described inthe Gulf of California. Prorocentrum rhathymum LoeblichIII, Sherley et R.J. Schmidt, described from the tropicalwestern Atlantic, has been until recently considered asynonym of P. mexicanum (Cortes-Altamirano andSierra-Beltran, 2003). Dodge (1975) considered the Medi-terranean species P. ovale (Gourret) Schiller and P. maxi-mum (Gourret) Schiller a synonym of P. mexicanum.However, the synonymies of Prorocentrum proposed byDodge (1975) were very often considered to be erroneous.While P. mexicanum and P. rhathymum are well investi-gated, there is a lack of information on P. maximum, andthis makes it dicult to conrm the synonymy. In thatcase, P. maximum has the priority versus P. mexicanum,and obviously it cannot be considered as non-indigenousin the Mediterranean Sea. The species Prorocentrum vene-tum Tolomio et Cavolo described from the Adriatic Seais closely related (if not a conspecic) to P. mexicanum(Tolomio and Cavolo, 1985).

Another epiphytic species, Coolia monotis Meunier, iscited as a non-indigenous species. However, this taxonhas been known in the Mediterranean since the 1930s asGlenodinium monotis (Meunier) Biecheler (Biecheler,1952). The rst studies on benthic/epiphytic toxic dinoa-gellates in tropical waters resulted in the relatively recentdescription of Ostreopsis lenticularis Fukuyo and O. ovataFukuyo in the Pacic Ocean (Fukuyo, 1981). There have

F. Gomez /Marine Pollutiobeen few studies of the benthic/epiphytic dinoagellatesin the Mediterranean compared to other regions and thesespecies have simply been recorded when studies were car-ried out (i.e. Monti et al., 2007). So these new entriesshould not be considered as recent species introductionsin the Mediterranean Sea.

Gymnodinium catenatum, an unarmoured dinoagellate,is also known mainly from the Alboran and African coastsof the Mediterranean Sea (Gomez, 2003b). In other cases,the citations of G. catenatum in the Mediterranean Sea cor-responded to the non-toxic Gymnodinium impudicum,described from the Iberian coasts (Fraga et al., 1995). Kare-nia brevis (=Gymnodinium breve) is responsible for bloomsin the Gulf of Mexico. In the Mediterranean Sea, Gymnodi-nium breve was cited as responsible for blooms in thecoastal Aegean Sea, although the identication needs tobe conrmed (Gotsis-Skretas and Frigilos, 1990; Monche-va et al., 2001). Since the formation of the genus Kareniain 2000, numerous new species have been described (Hay-wood et al., 2004). Beyond K. brevis, other taxa such asK. selliformis and K. papilionacea begin to be cited in theMediterranean Sea. Karenia species such as K. selliformismay be related to the Mediterranean species Gymnodiniummaguelonnense Biecheler (Biecheler, 1939). According toGomez et al. (2005) and Gomez (2006b) Karenia papiliona-cea is only the coastal morphotype, lacking the body exten-sions of Brachidinium F.J.R. Taylor or AsterodiniumSournia. Brachidinium is reported in the Mediterraneansince Leger (1971). Gomez and Claustre (2003) reportedthe occurrence of Asterodinium associated with exception-ally warm temperatures in the Tyrrhenian and LigurianSeas in September 1999. The form Asterodinium is theresponse of species of Karenia to the thermal straticationassociated with high temperatures. There is no reason toconsider the species of Karenia as introduced taxa; mostof them have been reported in the past as Gymnodiniumsp., due to the diculties in identication. The highly poly-morphic Pseliodinium vaubanii Sournia is a synonym ofGyrodinium falcatum Kofoid et Swezy (=Gymnodiniumfusus Schutt) (Konovalova, 2003). Gyrodinium falcatumor Gymnodinium fusus should not be considered as non-indigenous species in the Mediterranean Sea.

3.2. Non-indigenous diatoms in the Mediterranean Sea

According to Streftaris et al. (2005) the non-indigenousdiatoms are restricted to two taxa: Chaetoceros coarctatusLauder and Rhizosolenia indica H. Peragallo. Accordingto Por (1990) Ch. coarctatus was introduced through theSuez Canal. Chaetoceros coarctatus is a widespread tropicalspecies, also recorded in temperate waters of the EuropeanAtlantic (Hendey, 1974) and reported even in the coldersub-basins of the Mediterranean Sea (Travers, 1975; Vilicicet al., 2002).

Proboscia indica (H. Peragallo) D.U. Hernandez-Becer-ril (=Rhizosolenia indica) was found previously in theIndian Ocean more than in the Mediterranean or Atlantic.

ulletin 56 (2008) 620628 625It was historically considered as a variety of the cosmopol-itan Rhizosolenia alata Brightwell. Proboscia indica is asso-

tion system established at the end of the 18th century con-nects the Baltic and Black Seas through the central

taxa are common in European reservoirs and lakes and

n Btheir appearance in estuarine areas of the Black Sea isnot unexpected (Wyatt and Carlton, 2002).

According to Moncheva et al. (2001) Alexandrium mon-ilatum (Howell) Balech (=Gessnerium mochimaensis Halim)is responsible for blooms in the Black Sea since 1991. Alex-andrium monilatum is known from tropical western Atlan-tic and the Eastern Pacic Ocean. There is no rigorousstudy to conrm the record of this warm-water species inthe cold waters of the Black Sea (only reported by oneauthor, Moncheva et al., 2001). Scrippsiella trochoidea isa wide-spread cosmopolitan species, although under thisname, it may have been cited several dierent species.Scrippsiella trochoidea entered in the Black Sea 12,000European rivers. The phytoplankton studies in the BlackSea are few, usually less rigorous and are often in lessaccessible literature sources when compared to literatureabout phytoplankton in other European Seas (Gomezand Boicenco, 2004). The Black Sea has a short historyon a geological time scale and consequently all the marinespecies are recently established.

4.1. Non-indigenous dinoagellates in the Black Sea

The average salinity in the Black Sea is low (17).Freshwater species may temporarily remain near estuariesand even proliferate. Moncheva and Kamburska (2002,p. 48) listed the freshwater dinoagellates Gymnodiniumuberrimum (Allman) Kofoid et Swezy and Gymnodiniumfuscum (Ehrenberg) Stein as non-indigenous species. Theseciated with intrusion of warm oceanic waters in the EnglishChannel and North Sea (Nehring, 1998). Chaetoceroscoarctatus and Proboscia indica are widespread warm-water species. The entrance of warm-water species intothe Mediterranean is a continuous process favoured by pat-terns of circulation through the Strait of Gibraltar (Gomezet al., 2000). The scarce phytoplankton studies in theAlboran Sea and along the African coasts of the westernMediterranean make the monitoring of this phenomenondicult. The spreading of diatoms such as Chaetoceroscoarctatus and Proboscia indica may be favoured duringwarming episodes.

4. Black Sea

The Black Sea is an interglacial lake inundated by Med-iterranean waters during the sea rise 12,000 years ago. It isa quasi-enclosed basin with the BosphorusDardanellesStrait as the only contact to the worlds oceans and is ahighly eutrophic brackish basin with hypoxia in deeperwaters. The European intercontinental aquatic transporta-

626 F. Gomez /Marine Pollutioyears ago along with the other Mediterranean phytoplank-ton species.4.2. Non-indigenous diatoms in the Black Sea

It is surprising to nd Asterionella japonica Cleve etMoller listed as a non-indigenous diatom in the BlackSea. It is also an example induced by exotic etymology ofthe epithet. Wol (1996) also reported A. japonica as anon-indigenous species in Dutch waters and later correctedthe error (Wol, 2005). Asterionella japonica is a synonymof the common and cosmopolitan species Asterionellopsisglacialis (Castracane) Round.

Thalassiosira nordenskioeldii is a typical cold-water spe-cies described from Arctic waters. In the current warmingperiod this taxon is restricted to the colder Mediterraneansub-basins such as Gulf of Lions (Travers, 1975) and theAdriatic Sea (Revelante et al., 1984; Vilicic et al., 2002).This taxon may have had wider distributions during thelast glacial periods. The occurrence of T. nordenskioeldiiin the colder waters of the Black Sea is not unexpected.

Pseudosolenia calcar-avis (=Rhizosolenia calcar-avis) is acommon species in the Mediterranean Sea, and historic evi-dence of this species is revealed in sediment core samples(Kemp et al., 1999). This taxon entered with the rst Med-iterranean waters that inundated the Black Sea basin c.12,000 years ago.

It is obvious that distinguishing between elements of theindigenous plankton and newcomers from elsewhere isincreasingly dicult. Competent taxonomists and eectivemonitoring are essential for responding to the challenge ofassessing the ow of arriving alien phytoplankton speciesin European waters. The phytoplankton identicationstudies require experienced observers, although there is apaucity of well-educated alpha-taxonomists, and theirnumbers are quickly decreasing (Cotterill, 1995). Insteadof generating repetitive lists of doubtful non-indigenousspecies, direct studies by long-term monitoring planktonprograms are essential to detect and evaluate the changesin the phytoplankton communities in the European Seas.

Acknowledgements

I am supported by a post-doctoral grant of the Ministe-rio Espanol de Educacion y Ciencia #2007-0213. I thank T.Overton for improving the manuscript and the commentsand suggestions of an anonymous reviewer.

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Phytoplankton invasions: Comments on the validity of categorizing the non-indigenous dinoflagellates and diatoms in European SeasIntroductionNon-indigenous species in the European Atlantic (Arctic, Baltic, North, Atlantic)Non-indigenous dinoflagellates in the European Atlantic OceanNon-indigenous diatoms in the European Atlantic Ocean

Mediterranean SeaNon-indigenous dinoflagellates in the Mediterranean SeaNon-indigenous diatoms in the Mediterranean Sea

Black SeaNon-indigenous dinoflagellates in the Black SeaNon-indigenous diatoms in the Black Sea

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