Distribution patterns of isomorphic cold-water dinoflagellates

(Scrippsiella/Woloszynskia complex) causing ‘red tides’ in the Baltic Sea

Andres Jaanus1,*, Susanna Hajdu2, Seppo Kaitala3, Agneta Andersson4, Kaire Kaljurand1,Iveta Ledaine5, Inga Lips1 & Irina Olenina61Estonian Marine Institute, Tartu University, Maealuse 10a, 12618, Tallinn, Estonia2Department of Systems Ecology, Marine and Brackish Water Ecology, Stockholm University, Svante Arrheniusvag 21 A,

SE-106 91, Stockholm, Sweden3Finnish Institute of Marine Research, P.O. Box 33, FIN-00931, Helsinki, Finland4Dept of Ecology and Environmental Science, Umea Marine Sciences Centre, SE-910 20, Hornefors, Sweden5Inst. of Aquatic Ecology, Marine Monitoring Center, University of Latvia, Daugavgrivas str., 8 Riga, LV-1048, Latvia6Centre of Marine Research, Taikos str., 26, LT-5802, Klaipeda, Lithuania(*Author for correspondence: Tel.: +372-671-8974; Fax: +372-671-8973; E-mail: andres@sea.ee)

Key words: Baltic Sea, dinoflagellates, Scrippsiella/Woloszynskia complex

Abstract

During the latest years medium-sized (15–30 lm), single-celled dinoflagellates have been reported to formblooms in the northern Baltic Proper and the Gulf of Finland in winter and spring. Recent studies(Kremp et al., 2003. Proceedings of the 7th International conference of Modern and Fossil Dinoflagel-lates, September 21–25, Nagasaki, Japan, 66 pp.) indicate that those blooms are caused by twoisomorphic species – Scrippsiella hangoei (Schiller) Larsen, and a new species, tentatively belonging to thegenus Woloszynskia. Until now there has been no report on how widely distributed these phytoplanktonspecies are in the Baltic Sea. In this study, the occurrence of Scrippsiella/Woloszynskia complex in theentire Baltic Sea was investigated, by using monitoring data from 1997 to 2003. The species occurred in asalinity range from 2 to 8 PSU. Highest concentrations were observed at salinity 4.5–6.5 PSU. Maximumcell densities of Scrippsiella/Woloszynskia complex in the water column were mainly obtained in April orin the beginning of May by the water temperature <3 �C prior to stratification was formed. In thecentral Gulf of Finland, the second maximum was found in 1999 and 2002 by the temperature >6 �C.Bloom formations in the Baltic Proper and in the Gulf of Finland may not only be explained byoptimum temperature and salinity, but also with other factors e.g. high nutrient concentrations and goodseeding conditions from the sediments.

Introduction

During the last decades ‘red tides’ of dinoflagel-lates have become a regular phenomenon duringspring period in the northern Baltic Proper and theGulf of Finland (e.g. Lignell et al., 1993). Theblooms have been attributed to a single-celled,medium-sized (15–30 lm) species with delicatethecal plates called Scrippsiella hangoei (Schiller)

Larsen. Before its re-description by Larsen et al.(1995) S. hangoei was probably recognised underdifferent taxonomical names – Peridinium sp., P.hangoei, Gymnodinium sp., Glenodinium sp. (e.g.Niemi, 1975; Hobro, 1979; HELCOM, 1990, 1996;Heiskanen, 1993; Lignell et al., 1993). However,recent molecular and SEM analyses (Kremp et al.,2003) revealed considerable differences to thespecies description of Larsen et al. (1995), imply-

Hydrobiologia (2006) 554:137–146 � Springer 2006J. Kuparinen, E. Sandberg-Kilpi & J. Mattila (eds), Baltic Sea: A Lost System or a Future TreasuryDOI 10.1007/s10750-005-1014-7

ing that another, hitherto unrecognized speciesco-occurs with S. hangoei during spring bloom.SEM images of this dinoflagellate suggest assign-ment of this species to the genus Woloszynskia.

S. hangoei as well as Woloszynskia sp. are moreor less isomorphic (Kremp et al., 2003) and cannotbe unequivocally identified in Lugol fixed samples.Re-analyzing the historical and even recent sam-ples to specify the taxonomical composition isimpossible or requires different techniques, whichare not used in routine monitoring. Of these rea-sons we use the concept of Scrippsiella/Wol-oszynskia complex further in the text.

The temporal sequence and also the peculiar-ities of bloom onset and development of Scrip-psiella/Woloszynskia on the coastal–open seagradient have been studied thoroughly during thelast decade (Kremp, 2000a, b; Kremp & Heiska-nen, 1999). At the same time we had relativelypoor knowledge about the distribution of thiscomplex on a larger basin-wide scale. S. hangoeisensu Larsen et al. (1995) has been consideredendemic, which is adapted to the specific lowsaline environment of the Baltic Sea. Earlierstudies and laboratory experiments had mostlybeen conducted in a restricted area in the north-ern coastal Baltic. In the present paper, we try tomark out the general features of the spatio-temporal dynamics, supported mainly by themonitoring data from different sub-areas of theBaltic Sea.

We give an account that the taxonomic con-fusions considerably hamper the assessment ofthe distribution and quantitative characteristicsof medium-sized single-celled dinoflagellates. Inorder to avoid a blend of several genus names,which have been probably used for the samecomplex in earlier records (before 1995), weevaluated only recent data (1997–2003) in ourstudy.

Material and methods

The samples were collected within the frameof selected national, HELCOM and Alg@linemonitoring programmes in 1997–2003. The num-ber of monitoring stations by different sub-basinswas the following: Gulf of Finland 18 (incl. 10

Alg@line stations), Gulf of Riga 10, Baltic Proper28, Gulf of Bothnia 6 stations and one station inthe Aland Sea (Fig. 1, Table 1). The salinity rangewas between 1.3 in the Stockholm Archipelagoand 7.2 PSU in the southern Baltic Proper. Theselected stations also represent very diversebathymetric structure from shallow bays to deep-est basins in the Baltic Sea and from erosion toactive accumulation areas (Table 1).

In the coastal and open sea monitoring stationsintegrated samples from surface to 10 or 20 mdepth were taken mainly according to the recom-mendations of the BMP (HELCOM, 1988). Somedifferences in sampling methods were caused bydifferent equipment used. Swedish stations weresampled from the photic zone (0–20 m) using ahose (a plastic tube with inside diameter of25 mm), as the samples from Estonian, Latvianand Lithuanian stations were pooled from discretedepths (1, 5 and 10 m). To make counting resultsof 0–10 m comparable with those of 0–20 m, datafrom 0–20 m were multiplied by a factor of 1.36.This factor was derived from intensive verticalstudies during the spring of 1996 at the Swedishoffshore station H3 (Hoglander et al., 2004).Alg@line stations were sampled weekly fromApril to early June from �5 m depth onboardmoving ship by the flow-through system pumps(Rantajarvi & Leppanen, 1994).

Sampling frequency was mostly 1–2 times amonth from March to early June in 1997–2003with some interruptions or reductions dependingon the specific monitoring programmes or on themeteorological conditions (ice-cover). Station H3and H12 were collected weekly during the ongoingspring bloom (mainly April) and biweekly there-after. 1058 samples were analysed in total, 71% ofthose represent April-May, the normal period forphytoplankton spring bloom in the northern andcentral parts of the Baltic Sea (e.g. Hallfors &Niemi, 1981).

Samples were preserved with acetic Lugol’ssolution and counted by the inverted microscopetechnique following the recommendations ofHELCOM (1988). Biomass calculations weredone by multiplying the cell number with the cellvolume, derived from measurements of cell size.We used five categories to characterise thepeak abundances of Scrippsiella/Woloszynskiacomplex:

138

Results

Spatial distribution

Distribution of Scrippsiella/Woloszynskia withindication of relative maximum abundances in

different areas of the Baltic Sea is presented inFigure 1. The map is based on the maximum cellnumber found in all collected samples at eachstation (Table 1). Despite of different samplingstrategies we were able to demonstrate the loca-tions of the strongest bloom potential of the spe-cies. The maximum abundances were highest in theGulf of Finland – up to 10 · 106 cells l)1. At somestations in the northern Baltic Proper and near theLithuanian coast the peak abundance indicatedmoderate blooms (0.5–1 · 106 cells l)1). Cell den-sity decreased gradually both towards the southernBaltic Proper and northward in the Gulf ofBothnia. Scrippsiella/Woloszynskia was also lessabundant in the coastal areas under the influence

.

Maximum cells/l Rank

Seeding banks >5 000 000 5

Strong blooms 1 000 000–5 000 000 4

Moderate blooms 500 000–1 000 000 3

Common 100 000–500 000 2

Present <100 000 1

Figure 1. Sampling locations and distribution of the dinoflagellate Scrippsiella/Woloszinskia complex in the Baltic Sea. Scale bar for

maximum cell densities: 5 – Seeding banks, 4 – Strong blooms, 3 – Moderate blooms, 2 – Common, 1 – Present, 0 – Absent or no

information.

139

Table

1.Descriptionofsamplingstationsandtheconditionsatmaxim

um

celldensity

Station

Area

Coord

NCoord

EDepth

Maxcellsl)1

Rank

Date

of

maxcell

density

Average

salinity

(Apr–May)

Water

temperature

(�C)

Total

No.of

samples

Bottom

sedim

ents

WQ3

CentralGulfofFinland

600200

245930

20

10738944

507.05.02

4.95

7.2

43

Mud

WQ5

CentralGulfofFinland

600200

245750

25

6006200

527.04.98

5.16

0.2

45

Mud

WQ1

CentralGulfofFinland

600924

250006

15

1861040

412.05.03

4.54

6.0

44

N12

CentralGulfofFinland

593800

272700

40

1177344

406.05.92

4.6

3.6

18

Muddysilt

F1

CentralGulfofFinland

600403

262050

66

1316336

406.05.92

5.00

2.9

18

Sandyorsiltymud

WQ6

CentralGulfofFinland

595600

245600

50

3016944

425.04.02

5.18

3.4

29

WQ7

CentralGulfofFinland

595000

244800

65

1238664

419.04.01

5.37

1.7

49

Muddysilt

F3

CentralGulfofFinland

595030

245030

80

1566702

416.05.99

5.40

4.4

34

Muddysilt

WQ9

CentralGulfofFinland

593695

244050

85

1470976

422.04.03

5.79

0.4

49

SS6

Western

GulfofFinland

594140

231590

1073488

423.04.01

5.82

23

H3

NorthernBaltic

Proper

583500

181400

459

1004333

410.04.01

6.46

2.7

81

Mud,clay

38

EasternGulfofFinland

592440

274700

8868700

306.05.92

4.52

4.2

22

Coarse-grained

sand

WQ8

CentralGulfofFinland

594295

243850

86

862568

319.04.01

5.52

1.7

32

WQ10

CentralGulfofFinland

593350

244295

55

817600

311.04.01

5.94

3.7

49

Sandysiltwithmud

WQ11

CentralGulfofFinland

592900

244650

30

716560

311.04.01

6.00

3.1

48

Muddysand

H1

NorthernBaltic

Proper

592900

225400

80

560056

325.05.95

6.11

6.3

22

Muddysilt

64

Lithuaniancoast

554600

205400

34

867224

309.05.03

6.64

5.7

11

Aleurite,mud

20

Lithuaniancoast

554200

205100

40

856293

310.05.03

6.95

6.1

28

Finesand,silt,clay

G6

GulfofRiga

580400

235720

10

103417

203.05.01

4.66

5.9

26

Sandygravel

G1

GulfofRiga

573700

233700

54

111417

220.05.97

5.34

7.7

36

Mud

140

M3

CentralGulfofFinland

593280

245700

43

186004

220.04.94

5.71

1.3

10

Fine-grained

sand

SS2

ArchipelagoSea

600000

194500

151424

205.05.02

6.00

17

E2

CentralGulfofFinland

593220

244130

44

312732

208.05.03

6.03

5.0

33

Coarse-grained

sand

57a

CentralGulfofFinland

592700

244730

7225784

222.04.02

6.08

3.2

32

Muddysand

H12

Swedisheast

coast

584818

173752

42

220476

226.04.02

6.29

4.3

80

Mud,clay

1B

Lithuaniancoast

560200

205000

27

366202

208.05.03

6.50

4.9

11

Boulders,coarsesand

J57

Lithuaniancoast

555600

205800

18

317011

208.05.03

6.51

6.3

11

Boulders,coarsesand

1Lithuaniancoast

560200

210100

16

307901

208.05.03

6.54

5.9

8Finesand,silt,clay

H2

NorthernBaltic

Proper

590200

210500

180

185469

224.05.95

6.63

5.9

14

Mud

SS4

NorthernBaltic

Proper

592640

212148

203944

203.05.99

6.65

3.7

6

5Lithuaniancoast

554300

210400

15

118424

209.05.03

6.77

6.2

11

Finesand,silt

7Lithuaniancoast

551900

205700

15

428147

209.05.03

6.85

7.5

11

Aleurite

J2Lithuaniancoast

555300

202000

47

329764

209.05.03

7.02

5.0

13

Aleurite,mud

K2

Bornholm

Sea

551500

155900

90

295717

228.03.01

7.10

2.7

15

4Lithuaniancoast

554400

210300

16

109313

209.05.03

7.10

6.2

11

Finesand,silt

J1EasternGotlandBasin

572000

200600

240

274992

227.04.00

7.14

5.8

30

Mud,clay

K4

Bornholm

Sea

550000

140500

47

354960

227.03.99

7.20

2.9

13

C1

BothnianSea

623500

195900

212

113424

204.06.99

5.22

13

Rankingformaxim

um

celldensity:5–Seedingbanks(>

5*106l)1),4–Strongblooms(1–5*106l)1),3–Moderate

blooms(0.5–1*106l)1),2–Common(1–5*105l)1).

141

of fresh-water inflow (salinity <4 PSU). In morethan 70% of all stations the maximum cell num-bers did not exceed 0.5 · 106 per litre, which weconsidered insufficient to define as bloom-likedensity.

In areas where Scrippsiella/Woloszynskia formedmoderate to strong blooms, the surface layer(0–10 m) salinity varied from 4.52 to 6.46 PSU. Thetwo Lithuanian coastal stations (20 and 64) had,however, higher salinity (6.64–6.95 PSU). Somewhatunexpectedly, in the Gulf of Riga, the area withsalinity from 4 to 6 PSU, Scrippsiella/Woloszynskiacomplex did not belong to the dominant species.

Temporal sequence of the bloom

Peak abundances were usually reached earlier inthe southern part of the Baltic Sea (in the end ofMarch) than in the Western Gotland Basin and inthe southern coastal area of the Gulf of Finland(during the first decade in April). The bloomstarted at latest in the northern Baltic Proper andin the Gulf of Bothnia with maximum cell densitiesin the end of May or in the beginning of June.Exceptionally, all maximum abundances of Scrip-psiella/Woloszynskia in the Lithuanian coastal andoffshore stations were measured during the firstdecade of May 2003. That was probably due to thespecific sampling design, as those stations werevisited only once per season (in February andMay). Peak abundances were followed only in theareas, where the maximum cell density was higherthan 105 per litre.

Figure 2. Seasonal biomass (lg l)1) dynamics of Scrippsiella/

Woloszinskia complex along the transect between Tallinn and

Helsinki. Averaged weekly values from 1998–2003.

Figure 3. Examples of the seasonal abundance dynamics (cells l)1) of Scrippsiella/Woloszynskia during April–May 2002 at selected

stations. Note the difference in scales.

142

Due to the scarcity of intensive monitoring data,the variation in cell maxima and the duration ofmedium-sized dinoflagellate blooms on interannualbasis was only possible to evaluate in the samplesfrom the central Gulf of Finland and for Swedishstations (B1 and H3). The bloom peaked almostsimultaneously in both locations, but in generalbetween 10th and 30th April. The peak values werefound during a relatively short period (1–2 weeks).Only after the severe winter in 2003, the bloompersisted from the mid of April to the mid of May,i.e. almost a month. A second maximum of Scrip-psiella/Woloszynskia was, however, found at sta-tionsWQ5 andWQ3near the Finnish south coast inMay 1999 and 2002, respectively (Figs. 2 and 3).The water temperature measured during the inten-sive growth of Scrippsiella/Woloszynskia wasmainly below 3 �C, indicating unstable conditionswhen the stratification was not yet developed.During the second maximum and also at theLithuanian stations, the temperature was >6 �C.

At the stations in the Gulf of Finland we fol-lowed the succession of Scrippsiella/Woloszynskiacomplex more in detail during 1998–2003. In mostcases, this complex made 25–70% of the totalphytoplankton biomass from the beginning ofApril to the first decade of May (Fig. 4). Only inthe second half of May Scrippsiella/Woloszynskiawere gradually replaced by Peridiniella catenataand other species. The number of cysts found inthe water samples in the end May reached up to68% of all motile cells a week before. The absolutenumber of cysts recorded was considerably highernear the Finnish coast and the open Gulf of Fin-land as compared to the southern part of the gulf(up to 0.9 · 106 and 0.1 · 106 l)1, respectively).Dinoflagellate cysts were present in low numbers

already in mid April, constituting still only a fewper cent of vegetative cells in maximum.

Discussion

The dominance of dinoflagellates is rather excep-tional in temperate coastal waters, where diatomsform the major part of the vernal bloom biomass.During 1979–1999 dinoflagellates generallyincreased in the Baltic Proper and the observedtrend might indicate shifts in the ecosystem(Wasmund & Uhlig, 2003). In our material Scrip-psiella/Woloszynskia complex reached bloomconditions, both in the Gulf of Finland and in thenorthern Baltic Proper, contributing up to 90–96% of total phytoplankton biomass at theintensive monitoring stations WQ3 and WQ5 nearthe Finnish south coast in 1998 and 2002. In thewestern Gulf of Finland, the spring maximumbiomass, observed at the end of April 1998, wasproduced solely (97%) by the same complex (Ka-uppila & Lepisto, 2001). Heiskanen (1993) andLarsen et al. (1995) reported contribution of 60–90% to the total spring phytoplankton biomass inthe same area, as well. The reason of such highdominance of dinoflagellates is not clear, but adramatic decrease in the ratio of SiO4 to DIN(DIN = NO3+NH4) was recorded in the north-ern Baltic during the period 1973–1999 (Kupari-nen & Tuominen, 2001). The change in the Si:Nratio is enhanced by the eutrophication (e.g. Paerl,1997). If dissolved silica limits the spring bloom,diatoms become replaced by flagellates (Smayda,1990). However, Wasmund et al. (1998) suggestthat mild, ice-free winters seem to promote aspring bloom dominated by dinoflagellates ratherthan diatoms, probably due to the lack of deepmixing, which gives an advantage to motile cellsover non-motile ones.

Spatial distribution

Analysing the recent monitoring data from dif-ferent sub-basins of the Baltic Sea, Wasmund et al.(2000) consider salinity to be the main factorinfluencing the species distribution. In our study,Scrippsiella/Woloszynskia formed the strongestblooms in the areas with salinity from 4.5 to

Figure 4. Percentage of Scrippsiella/Woloszinskia in the total

phytoplankton biomass during spring bloom period in the Gulf

of Finland. Mean ± standard deviation in bold.

143

6.5 PSU. However, it concerns only the Gulf ofFinland and the northern Baltic Proper and eventhere the variation was extremely large in a rela-tively short distance (Fig. 2). High abundance(1–3 · 106 l)1) was also obtained in some deeperareas in the Gulf of Finland and the northernBaltic Proper. Kremp (2000a) suggested that theannual blooms of medium-sized dinoflagellates inthe northern Baltic Sea are seeded by large coastalresting cyst populations and the offshore bloomslikely originate from those coastal inocula trans-ported to the central parts of the Baltic Sea byoutflowing surface water. On the other hand, inthe deeper basins of the Baltic Proper and the Gulfof Finland anoxia, particularly if coupled to thepresence of H2S, may prevent germination ofdinoflagellate cysts from sediments (Kremp &Anderson, 2000).

As the station grid for regular monitoring inthe Baltic Sea is rather uneven, the real distribu-tion pattern may differ from that derived from ourstudy. We probably miss information on severalpotential seeding/bloom areas, especially in theBaltic Proper and the Gulf of Bothnia, but also onsome coastal sites in the northern Gulf of Finland.Scrippsiella and/or Woloszynskia cysts have beenfound in the low-saline coastal areas (Kremp,2000a), however, the maximum number of livingcells at the stations with average salinity<4.5 PSU remained below 105 l)1 in our data set.Due to the lack of recent phytoplankton data fromthe SE Finnish coastal area and the Bothnian Bay,we have rather poor knowledge on the lowestsalinity tolerance of Scrippsiella/Woloszynskia.The species was sporadically found in the Stock-holm archipelago (station SS1, average salinity1.34 PSU), but not observed or recognized inNeva Estuary, the easternmost part of the Gulf ofFinland (salinity 0.3–1.7 PSU) (Nikulina, 2003).One or another species of the complex has beenpresent in the plankton of Mecklenburg Bight withsalinity 8–9 PSU (Alg@line, 2001). Scrippsiella/Woloszynskia have probably not spread outsidethe Baltic Sea, however, dinoflagellate cysts maysurvive transport with ballast water and can bemoved to areas where they have not recordedpreviously. ‘S. hangoei’ cysts have been found inthe sediment samples from English and Welshports (McCollin et al., 1999), but without anyrecord of living cells.

Although the maximum cell number decreasedboth towards the higher and lower salinity areas,salinity is probably not the main factor governingthe distribution of these species as they were notdominating in the Gulf of Riga with the samesalinity range. It may also be possible that thedinoflagellates found in the southern and northernparts of the Baltic Sea are not con-specific.Moreover, Kremp et al. (2003) found thatWoloszynskia sp. thrives in salinities that are muchhigher than what the species experience in thenorthern Baltic Proper, whereas salinities lowerthan 6 PSU seemed to inhibit growth.

Analysing the distribution of dinoflagellatecysts along an estuarine salinity gradient(2–7 PSU), Kremp (2000a) also took into consid-eration the character of bottom sediments.Although no correlation was found between cystconcentration and water depth of the samplingsites, almost all sampling locations with high cystabundances were muddy with a high percentage oforganic content. The Finnish coastline mainlyconsists of bedrock, but the sediments in the outerarchipelago and open sea zone are mostly mud-covered. This is also characteristic for the stationsWQ3 and WQ5 near the Finnish south coast wherethe observed number of living cells of Scrippsiella/Woloszynskia was the highest – up to 107 l)1 (seealso Fig. 2).

The Gulf of Riga has no permanent haloclineand it is mixed down to the bottom in winter. Thecharacter of bottom sediments is variable althoughorganic-rich soft bottom are prevailing only in themiddle deepest (40–55 m) part of the gulf (Stiebrins& Valing, 1996). Theoretically, a seed populationcan be permanently available. Monitoring obser-vations made in the Gulf of Riga and in theadjacent areas to the central Baltic Proper inMarch–April still indicate the clear dominance ofdiatoms, mainly Thalassiosira baltica and Pauliellataeniata. The percentage of dinoflagellates hasincreased in the spring blooms at the end of 1980sand the beginning of the 1990s, but it is mainly dueto the increase in Peridiniella catenata biomass(Yurkovskis et al., 1999).

Temporal distribution

A maximum cell density of Scrippsiella/Wol-oszynskia in the water column was mainly obtained

144

in March–April or in the beginning of May by thewater temperature <3 �C, under unstable condi-tions prior to stratification was formed. Krempet al. (2003) found Woloszynskia sp. to be a trulystenothermic organism, with a temperature windowbetween 0 and 6 �C. As S. hangoei has optimumtemperatures a few centigrade higher, they sug-gested that temperature may be a potential factorseparating niches of the two species. Here is acontradiction with our data, as the salinity opti-mum for Woloszynskia sp. is in general higher(>6 PSU) than in the areas of strongest ‘red tide’dinoflagellate blooms in the Baltic Sea. The bloomsprobably appear to be a mixture of several specieswith unknown proportions, involving both, Scrip-psiella and Woloszynskia.

According to Kremp et al. (2003) also theresting cysts, which had previously assigned toS. hangoei were formed in clonal cultures of theWoloszynskia isolates and the species also differ intheir mode of sexual reproduction. In the experi-ment, dinoflagellate (probably Woloszynskia)cysts, formed during the spring bloom terminationin the northern Baltic Sea, remained dormant for6 months (Kremp, 2000a). Thus a new populationcan be seeded even under unfavourable conditionsin early winter when the light conditions are poor.On the other hand, such an early inoculum allowsthe species to immediately exploit favourablegrowth conditions provided. In our material,Scrippsiella/Woloszynskia made up to 75% of thetotal phytoplankton biomass already in March(Fig. 4), and these medium-sized dinoflagellateswere often the first dominants in spring bloomdevelopment. In the Gulf of Finland, these speciespersisted dominant until mid of May. We do notstill understand, in which proportion each speciescontribute to the total dinoflagellate biomass.There are also some opinions that environmentalchanges can influence the further bloom initiationand alter the respective proportions of the specieslater during the spring bloom (Kremp & Heiska-nen, 1999; Kremp, 2000b). Woloszynskia sp. mayhave a benefit in the earlier stage of the bloomaccording to its temperature optimum, whereasScrippsiella hangoei can be the major componentbefore the bloom terminates. The second maximarecorded in May 1999 and 2002, developed by thesurface water temperature >6 �C, thus can beattributed to S. hangoei.

Mild winters without ice cover seem promotethe dominance of dinoflagellates in the springbloom of the Baltic Sea (Heiskanen, 1998; Was-mund et al., 1998; Hajdu, 2002). Extremelystrong blooms of Scrippsiella/Woloszynskia in thecentral Gulf of Finland were observed in 1998and 1999, but especially after mild winters in2000 and 2002. We cannot still agree that med-ium-sized single-celled dinoflagellates are theminor component of the vernal phytoplanktoncommunity after harsh winters (Kremp &Heiskanen, 1999). In 2003, these species made upto 92–94% of the dinoflagellate and 70–88% ofthe total phytoplankton biomass in the same areaduring the spring bloom peak. It allows us toconclude that Scrippsiella/Woloszynskia bloom israther a yearly phenomenon at least in the Gulfof Finland. The observed dominance of thiscomplex in the gulf might be a sign for ecosystemchange due to decreasing inorganic Si:N ratio or/and climatic changes (e.g. Paerl, 1997).

The available monitoring data did not clarifythe ecology of both species mainly due to theidentification problems. These data may still servea basis for the further investigations, including theeffect of eutrophication. On the other hand, any ofsuch basin-wide research needs also a betterintercalibration of methods and carefully plannedsampling strategy of phytoplankton.

Acknowledgements

This work was partly financed by the EstonianMinistry of Environment, the Finnish Ministry ofEnvironment and the EU project FerryBox(EVK2-CT-2002–00144).

References

Alg@line, 2001. Baltic Sea Phytoplankton Sheet. http://jolly.

fimr.fi/Checklist3.nsf/Main?OpenFrameSet.

Hajdu, S., 2002. Phytoplankton of Baltic Environmental Gra-

dients: Observations on potentially Toxic Species. PhD

thesis, Stockholm University, Sweden, 42 pp.

Heiskanen, A.-S., 1993. Mass encystment and sinking of dino-

flagellates during a spring bloom.Marine Biology 116: 161–168.

Heiskanen, A.-S., 1998. Factors Governing Sedimentation and

Pelagic Nutrient Cycles in the Northern Baltic Sea. Mono-

graphs of the Boreal Environment Research 8, 80 pp.

145

HELCOM, 1988. Guidelines for the Baltic Monitoring Pro-

gramme for the third stage; Part D. Biological Determin-

ands. Baltic Sea Environment Proceedings 27D.

HELCOM, 1990. Second periodic assessment of the state of the

marine environment of the Baltic Sea, 1984–1988; Back-

ground document. Baltic Sea Environment Proceedings 35

B: 1–432.

HELCOM, 1996. Third periodic assessment of the state of the

marine environment of the Baltic Sea, 1989–1993; Background

document. Baltic Sea Environment Proceedings 64 B: 1–252.

Hobro, R., 1979. Annual phytoplankton successions in a

coastal area in the northern Baltic. In Naylor, E. & R. G.

Hartnoll (eds.) Cyclic Phenomena in Marine Plants and

Animals. Pergamon, Oxford: 3–10.

Hallfors, G. & A. Niemi, 1981. Vegetation and primary pro-

duction. In Voipio, A. (ed.) The Baltic Sea. Elsevier,

Amsterdam: 220–237.

Hoglander, H., U. Larsson & S. Hajdu, 2004. Vertical distribu-

tion and settling of spring phytoplankton in the offshore NW

Baltic Sea proper.Marine Ecology Progress Series 283: 15–27.

Kauppila, P. & L. Lepisto, 2001. Changes in phytoplankton. In

Kauppila, P. & S. Back (eds.) The State of Finnish Coastal

Waters in the 1990s. Finnish Environment Institute, Hel-

sinki: 61–70.

Kremp, A., 2000a. Distribution, dynamics and in situ seeding

potential of Scrippsiella hangoei (Dinophyceae) cyst popu-

lations from the Baltic Sea. Journal of Plankton Research

22: 2155–2169.

Kremp, A., 2000b. The role of life cycle in the population

dynamics of the bloom forming dinoflagellates Scrippsiella

hangoei and Peridiniella catenata in the Baltic Sea. Walter

and Andree de Nottbeck Foundation Scientific Reports 22.

Kremp, A. & D. M. Anderson, 2000. Factors regulating ger-

mination of resting cysts of the spring bloom dinoflagellate

Scrippsiella hangoei from the northern Baltic Sea. Journal of

Plankton Research 22: 1311–1327.

Kremp, A. & A.-S. Heiskanen, 1999. Sexuality and cyst for-

mation of the spring-bloom dinoflagellate Scrippsiella han-

goei in the coastal northern Baltic Sea. Marine Biology 134:

771–777.

Kremp, A., M. Elbrachter, J. Wolny & A. Shurtleff, 2003. A

new cyst forming spring bloom dinoflagellate co-occuring

with Scrippsiella hangoei in the northern Baltic Sea. Pro-

ceedings of the 7th International Conference of Modern and

Fossil Dinoflagellates. September 21–25, Nagasaki, Japan,

p. 66 (poster abstract).

Kuparinen, J. & L. Tuominen, 2001. Eutrophication and Self-

purification: counteractions forced by large -scale cycles and

hydrodynamic processes. Ambio 30: 190–194.

Larsen, J., H. Kuosa, J. Ikavalko, K. Kivi & S. Hallfors, 1995.

A redescription of Scrippsiella hangoei (Schiller) comb.

nov. – a ‘red tide’ dinoflagellate from the northern Baltic.

Phycologia 34(2): 135–144.

Lignell, R., A.-S. Heiskanen, H. Kuosa, K. Gundersen, P.

Kuuppo-Leinikki, R. Pajuniemi & A. Uitto, 1993. Fate of a

phytoplankton spring bloom: sedimentation and carbon flow

in the planktonic food web in the northern Baltic. Marine

Ecology Progress Series 94: 239–252.

McCollin, T. A., J. P. Hamer & I. A. N. Lucas, 1999. Transport

of Marine Organisms via Ships’ Ballast into Ports around

England and Wales. National Conference on Marine Bio-

invasions. Boston, Massachusetts, 1999.

Niemi, A., 1975. Ecology of phytoplankton in the Tvarminne

area SW coast of Finland. II. Primary production and

environmental conditions in the archipelago and the sea

zone. Acta Botanica Fennica 105: 1–73.

Nikulina, V., 2003. Seasonal dynamics of phytoplankton in the

inner Neva Estuary in the 1980s and 1990s. Oceanologia

45(1): 25–39.

Paerl, H. W., 1997. Coastal eutrophication and harmful algal

blooms: importance of atmospheric deposition and

groundwater as ‘‘new’’ nitrogen and other nutrient sources.

Limnology and Oceanography 42: 1154–1165.

Rantajarvi, E. & J.-M. Leppanen, 1994. Unattended Algal

Monitoring in Merchant Ships in the Baltic Sea. Tema Nord

546, 60 pp.

Smayda, T. J., 1990. Novel and nuisance phytoplankton

blooms in the sea: evidence for a global epidemic. In Graneli,

E., B. Sundstrom, L. Edler & D. M. Anderson (eds), Toxic

Marine Phytoplankton. Proc. Fourth. Int. Conf. on Toxic

Marine Phytoplankton. Elsevier, New York: 29–40.

Stiebrins, O. & P. Valing, 1996. Bottom sediments of the Gulf

of Riga. Geological Survey of Latvia. Geological Survey of

Estonia. Riga, 53 pp. and map.

Wasmund, N. & S. Uhlig, 2003. Phytoplankton trends in

the Baltic Sea. ICES Journal of Marine Science 60: 177–

186.

Wasmund, N., G. Nausch & W. Matthaus, 1998. Phytoplank-

ton spring bloom in the southern Baltic Sea – spatio-tem-

poral development and long-term trends. Journal of

Plankton Research 20: 1099–1117.

Wasmund, N., G. Nausch, L. Postel, Z. Witek, M. Zalewski,

S. Gromisz, E. ysiak-Pastuszak, I. Olenina, R. Kavolyte,

A. Jasinskaite, B. Muller-Karulis, A. Ikauniece, A. Andru-

shaitis, H. Ojaveer, K. Kallaste & A. Jaanus, 2000. Trophic

status of coastal and open areas of the south-eastern Baltic

Sea based on nutrient and phytoplankton data from 1993–

1997. Marine Science Reports 38, 83 pp.

Yurkovskis, A., E. Kostrichkina & A. Ikauniece, 1999. Sea-

sonal succession and growth in the plankton communities of

the Gulf of Riga in relation to long-term nutrient dynamics.

Hydrobiologia 393: 83–94.

146