Changes in Phytoplankton Communities Along a North–South Gradient in the Baltic Sea Between 1990 and 2008

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Changes in phytoplankton communities along a north–south gradient in the Baltic Sea between 1990 and 2008

Andres Jaanus1)*, Agneta Andersson2), Irina Olenina3)4), Kaire Toming1) and Kaire Kaljurand1)

1) Estonian Marine Institute, University of Tartu, Mäealuse 14, EE-12618 Tallinn, Estonia (*corresponding author’s e-mail: [email protected]) 2) Department of Ecology and Environmental Science, Umeå Marine Sciences Centre, Umeå University, SE-901 87 Umeå, Sweden 3) Coastal Research and Planning Institute, Klaipeda University, Manto str. 84, LT-92294 Klaipeda, Lithuania 4) Marine Research Department of the Environmental Protection Agency, Taikos av. 26, LT-91149 Klaipeda, Lithuania

Received 19 Nov. 2009, accepted 3 Nov. 2010 (Editor in charge of this article: Johanna Mattila)

Jaanus, A., Andersson, A., Olenina, I., Toming, K. & Kaljurand, K. 2011: Changes in phytoplankton communities along a north–south gradient in the Baltic Sea between 1990 and 2008. Boreal Env. Res. 16 (suppl. A): 191–208.

Evaluation of changes in Baltic Sea phytoplankton communities has been hampered by a lack of quantitative long-term data. We investigated changes in biomass of summer (June– September) phytoplankton over the last two decades (1990–2008) along a north–south gradient in the Baltic Sea. The areas were characterized by different temperature, salinity and nutrient conditions. Thirty taxonomic groups were selected for the statistical analysis. Increases in total phytoplankton, particularly cyanobacterial, biomass were observed in the Gulfs of Bothnia and Finland. In these two areas over the study period cyanobacteria also became abundant earlier in the season, and in the Curonian Lagoon Planktothrix agardhii replaced Aphanizomenon flos-aquae as the most abundant cyanobacterium. In general, water temperature was the most influential factor affecting the summer phytoplankton communities. Our data suggest that temperature increases resulting from climate change are likely to cause basin-specific changes in the phytoplankton communities, which in turn may affect overall ecosystem functioning in the Baltic Sea.

Introduction Moline and Prézelin 1996). However, long-term measurements with high temporal resolution are Changes in phytoplankton composition may required to separate natural sources of variability reflect structural and functional ecosystem shifts, from the effects of anthropogenic disturbance. and changes in the seasonal succession patterns Two of the most consistent effects of eutrophi- of phytoplankton species are thought to be better cation on phytoplankton are shifts in species predictors of long-term environmental change composition and increases in the frequency and than the more commonly used parameters of intensity of nuisance blooms, which are typically biomass (chlorophyll a) and productivity (e.g. dominated by harmful cyanobacteria (Huisman 192 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) et al. 2005, Carstensen et al. 2007). Unfortu- face temperatures in the late 1980s resulted in nately, most plankton data that are currently an extended growing season and increases in available are unsuitable for trend analysis due to phytoplankton biomass (chlorophyll a) in both sparse sampling and natural inter-seasonal vari- the North and Baltic Seas (Alheit et al. 2005). ability (McQuatters-Gollop et al. 2009). Long-term observations indicate that from the Measurements of phytoplankton species 1960s until the 1990s nearly a four-fold increase abundance, composition and biomass are essen- occurred in the winter inorganic nitrogen concen- tial elements of most monitoring programmes. tration in the northern Baltic Proper and the Gulf However, measuring seasonal changes and inter- of Finland, and almost a two-fold in the Both- annual variability requires extensive sampling nian Sea (HELCOM 2009). The concentration of efforts, and inadequate sampling may provide inorganic phosphorus followed a similar pattern, misleading indications of the timing, performance rising three-fold from the 1970s to the beginning and abundance of the dominant taxa. Ferreira et of the 1990s in the northern Baltic Proper and the al. (2007) suggested that monthly phytoplankton Gulf of Finland, and increasing by 30% in the monitoring is appropriate for restricted coastal Gulf of Bothnia. A slight decrease in phosphorus and transitional waters, but this level of sampling concentrations has been reported since the 1990s may not be sufficient to identify changes in more across the entire Baltic Sea, except in the Gulf complex systems, where variations in hydrologi- of Finland (Fleming-Lehtinen et al. 2008). An cal conditions strongly affect natural succession increase in winter nutrient concentrations should (e.g. Pilkaytitė and Razinkovas 2007). theoretically cause changes in spring phytoplank- Furthermore, evaluation of phytoplankton ton biomass. However, intensive measurements data from different laboratories requires the meth- of chlorophyll a in the open Baltic Sea have not ods used and taxonomic expertise of the people yet confirmed such an increase in spring phy- analyzing the data to be comparable. Unfortu- toplankton biomass, although a slight tendency nately, there is considerable heterogeneity among for the bloom to start earlier has been observed datasets from different countries, especially with (Fleming and Kaitala 2006). This earlier devel- respect to sampling methods and taxonomic pre- opment of the spring bloom suggests that the cision, which limits the comparability of the summer phytoplankton communities will also data and increases the level of uncertainty in the develop earlier. results of any comparative study. This uncertainty Wasmund and Uhlig (2003) suggest that a increases further when biomass data are calcu- consistent time series of > 20 years is required lated from cell size measurements. The need to for reliable indications of long-term changes in standardise collection methods, counting tech- phytoplankton biomass and community struc- niques and the identification of phytoplankton ture. However, there have been few long-term species was recognized in early phytoplankton phytoplankton studies, especially of changes in studies, particularly through the framework of the species composition and abundance, even in Baltic Monitoring Programme in the late 1970s. such well-studied ecosystems as the Baltic Sea. This need was addressed by the establishment Studies from before the 1960s and 1970s are of the HELCOM Phytoplankton Expert Group even rarer, more fragmented and differed sub- (PEG) and publication of standardized size- stantially with respect to the sampling and quan- classes and biovolumes of phytoplankton species tification methods used. Comparisons of histori- found in the Baltic Sea (Olenina et al. 2006). cal data with recent data are always problematic Year-to-year fluctuations in phytoplankton and have to be treated cautiously (e.g. Finni et al. species compositions are governed by hydro- 2001b, Wasmund et al. 2008). Nevertheless, past graphical and hydrochemical drivers. For exam- studies of phytoplankton from the open Baltic ple, increases in salinity and nutrient concentra- Sea (Suikkanen et al. 2007) and the Kiel Bight tions in the Baltic Proper during the 1970s caused (Wasmund et al. 2008) revealed an increase in a general increase in phytoplankton biomass, total biomass (chlorophyll a), but the changes at especially during spring (Kononen and Niemi the community level were more complex, show- 1984). In addition, increasing air and sea sur- ing both upward and downward trends. Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 193

Fig. 1. Locations of the sampling stations in the Baltic Sea.

Quantitative phytoplankton time-series data (62°35´22´´, 19°58´41´´) and C3 (62°39´22´´, have not been collected, or are of poor quality, 18°57´06´´); Öre Estuary, western Gulf of Both- for most of the Baltic sub-basins. The aim of nia — stations B3 (63°29´´98´´, 19°49´18´´) and this study was to assess long-term changes in B7 (63°31´48´´, 19°48´47´´); Tallinn Bay, south- the dominant phytoplankton along a north–south ern Gulf of Finland — stations 2 (59°32´20´´, gradient in the Baltic Sea, including the Gulf of 24°41´30´´) and 57a (59°27´00´´, 24°47´30´´); Bothnia, southern Gulf of Finland (Tallinn Bay) and Curonian Lagoon, southeast Baltic Sea — and Curonian Lagoon. Summer data from high station K2 (55°55´50´´, 20°58´50´´) (Fig. 1). frequency monitoring programmes that began in The Bothnian Bay is the northernmost sub- the 1990s and continued until 2008 were used in basin of the Baltic Sea, and accounts for ca. 10% the analysis. A statistical method (BIOENV) was (36 260 km2) of the total Baltic Sea surface area. used to identify the most influential environmen- This bay has a mean water depth of 43 m, low tal factors affecting the phytoplankton communi- salinity (2–3 practical salinity units, psu) and ties in each of the major Baltic Sea basins. The surface water that is typically covered with ice results are discussed in relation to present and during the winter months (January–April). Light future environmental threats to the Baltic Sea. availability is lower than in other regions of the Sea due to high contents of humic substances in the water. Through a shallow (20 m) sill area Material and methods called the Quark, the bay is connected to the deeper (mean depth 68 m, maximum 147 m) Study area parts of the Bothnian Sea (HELCOM 1996). The Öre estuary is situated just south of the northern We analyzed monitoring data from five basins: Quark. Bothnian Bay — station A13 (64°42´49´´N, Tallinn Bay is located in the southern part 22°03´93´´); Bothnian Sea — stations C1 of the Gulf of Finland and consists of four 194 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) smaller bays and a more open part. A deep trench from 1 to 14 observations per season and basin. (70–90 m) in its northern part allows water from The average frequencies of sampling events per the western Gulf of Finland to enter Tallinn Bay. season were four in the Curonian Lagoon, five in The large urban area affects the nutrient status of the open Gulf of Bothnia and six in the Öre Estu- the surrounding waters, as Tallinn Bay receives ary. It should be noted that samples were always most of the local municipal wastewaters. At a taken simultaneously at the two monitoring sta- broad scale, the Gulfs of Finland and Bothnia tions in Tallinn Bay that contributed data, at a could be considered large estuaries because they similar sampling frequency (6–7 per season) to are strongly influenced by river waters (Kauppila the frequency in other areas. Observations were 2007). generally made at regular intervals throughout The Curonian Lagoon is a shallow (mean the entire investigation period, except that the depth 3.7 m), mostly freshwater, semi-enclosed sampling intensity was lower between 2004 and estuary. The lagoon is connected to the Baltic 2008 in the open Gulf of Bothnia and Curonian Sea at its northern end, while the main inflow Lagoon (Table 1). In Tallinn Bay, only one is from freshwater discharge from the Nemunas sample was collected in both 1995 and 1996. River, which is the third-largest contributor (after Sampling was generally conducted between the Vistula and Oder) of total nitrogen and phos- 0 to 10 m depth using either a plastic hose (in the phorus to the southeast Baltic Sea (Stålnacke et Gulf of Bothnia) or water samplers at discrete al. 1999). horizons (1, 5 and 10 m; the Gulf of Finland). In the Curonian Lagoon, samples were taken from the surface layer (0–0.5 m) using a 5-litre plas- Time-series data tic water sampler. In Tallinn Bay, samples for phytoplankton and chlorophyll a were obtained The data used in this study date back to the early by pooling equal volumes (0.5–1 l) of water 1990s when national monitoring programmes from different horizons, whereas nutrients were were established in all of our study areas. Three determined from discrete samples. In the Gulf of laboratories in three countries contributed to our Bothnia, samples for determining total phospho- study and all analysts were members of PEG, rus (Ptot) and total nitrogen (Ntot) were obtained providing us with confidence that the data are from discrete depths (e.g. 0, 1, 2, 4, 6, 8 and reliable and comparable. 10 m) using a water sampler. Samples were taken between 1990 and 2007 Samples collected from the Curonian Lagoon from the Curonian Lagoon, 1993 and 2008 from were divided into sub-samples for determining Tallinn Bay, and 1995–2008 from the Gulf of phytoplankton biomass and community compo- Bothnia. We focused on the summer period (from sition, and chlorophyll a and nutrient concentra- June to September) for which the phytoplankton tions. Temperature and salinity were measured datasets were most representative. Depending on using CTD probes. Data for chlorophyll a were the location and year, sampling frequency varied not provided from the Gulf of Bothnia.

Table 1. Numbers of sampling events by sub-area, period and month.

Bothnian Bay Bothnian Sea Öre Estuary tallinn Bay curonian Lagoon total

June 23 21 26 50 19 139 July 14 17 16 57 19 123 August 19 17 24 50 23 133 September 17 16 20 30 16 99 Before 1999 31 26 31 58 38 184 1999–2003 25 25 28 62 23 163 2004–2008 17 20 27 67 16 147 Total 73 71 86 187 77 494 Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 195

Biological and chemical analyses Plus autoanalyzers using standard seawater methods (Grasshoff et al. 1983; EVS-EN ISO Phytoplankton samples were preserved with acid 15681:2005 and EVS-EN ISO 11905-1:2003). Lugol solution (0.5–1 ml per 200 ml sample) Average concentrations in the upper 10-m layer and analyzed using inverted microscopes (Gulf were calculated for each sampling occasion of Bothnia samples — Zeiss and Nikon Eclipse using depth integrations. TE 300; Gulf of Finland — Olympus IM, IMT-2 and Leitz Fluovert FU; Curonian Lagoon — Leitz Fluovert FU and Olympus IX-51) and the Statistical analyses sedimentation technique (Utermöhl 1958). The sediment volume and sedimentation time varied Thirty taxonomic groups were used in the phy- between 5 and 50 ml and 4 and 48 h, respec- toplankton analysis, ranging from class to spe- tively. For the samples from the Gulf of Bothnia, cies level depending on the resolution of the 50% of the sedimentation chamber was scanned method. The taxa were selected on the basis at the 100¥ magnification when counting large of their common appearance in all sub-basins, cells (> 10 µm), while small cells (< 10 µm) with some exceptions for species that were were counted at the 400¥ magnification along dominant in only one area (Table 2). To avoid one diagonal. For phytoplankton from Tallinn probable misidentifications by different ana- Bay, the 200¥ magnification was used for larger lysts and due to recent changes in nomencla- cells and cells along one or two diagonals were ture, especially for small-sized flagellates and counted, depending on the density of the sample. colonial cyanobacteria, these organisms were The abundance of smaller cells was estimated aggregated into higher taxonomic groups. For by examining 20 or 30 objective fields using example, the colonial cyanobacterium Micro- the 400¥ magnification. Phytoplankton sam- cystis reinboldii (Pankow 1976, Tikkanen and ples from Curonian Lagoon were counted using Willén 1992) includes several species from the the 100¥ magnification and scanning 50% of genera Aphanocapsa (Hällfors 2004). Due to the sedimentation chamber for large, rare spe- taxonomic changes and identification difficulties cies and 400¥ magnification along one diagonal we merged several species and genera into class or in 10 objective fields for common species. (crypto-, prymnesio-, chryso-, eugleno and prasi- Cell sizes were measured using an ocular scale nophyceae), order (Chroococcales) or subfamily and volumes were calculated from cell geom- (Gomphosphaerioideae) levels before further etry (HELCOM 1988, Hillebrand et al. 1999) analysis. Total autotrophic biomass, chlorophyll- or using standard size-classes (Olenina et al. a content, water temperature and salinity, and the

2006). Recent lists of biovolumes and fixed concentrations of total nitrogen (Ntot) and total size-classes are recommended for use in the phosphorus (Ptot) were used in our analyses as calculation of phytoplankton biomass in routine explanatory variables. monitoring. Wet weight biomasses (mg per litre For statistical analyses, we divided the data- of seawater) were calculated for individual taxa sets into three periods: (1) before 1999, (2) and for the total biomass (http://www.helcom. 1999–2003 and (3) 2004–2008, for which the fi/groups/monas/CombineManual/AnnexesC/ total numbers of samples were 184, 163 and en_GB/annex6). 147, respectively. The data from the offshore The chlorophyll-a concentration was measured and coastal stations in the Gulf of Bothnia were spectrophotometrically (Gulf of Finland — Yanaco treated separately. To obtain symmetric random UO 2000 and Jenway 6400; Curonian Lagoon — deviations, the biomass data of the individual Specol 21 and Jenway 6300) after extraction in taxa were square-root transformed before the sta- ethanol according to the HELCOM COMBINE tistical analysis. Temperature, salinity and nutri- manual (http://www.helcom.fi/groups/monas/ ent concentrations were averaged over 0–10 m CombineManual/AnnexesC/en_GB/annex4). depth. R version 2.8.1 (R project for statistical

Ntot and Ptot were analyzed with Braan & computing) was used to conduct the Welch two Luebbe GmbH TRAACS 800 and Skalar San sample t-test to detect significant differences 196 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A)

(p < 0.05) in the phytoplankton and environmen- to compare the similarity matrices generated for tal data between the periods within a sub-area. the community and environmental data to exam- In these tests, the data were compared across ine the ecological significance of each meas- all seasons and for single months. Relationships ured environmental variable on the dynamics between environmental variables and the whole of selected groups. This analysis was conducted phytoplankton community or dominant phyto- using PRIMER version 5 (Clarke and Warwick plankton groups were identified by BIOENV. 2001). We computed all possible combinations for each environmental variable separately and for all possible combinations simultaneously. Spear- Results r man correlation coefficients ( s) were calculated Variability and environmental trends Table 2. Phytoplankton taxa included in the statistical analysis. Nomenclature according to Hällfors (2004). Seasonal temperature variations were similar in all study areas, with the minimum temperature Taxon name Comments at the beginning of June and the maximum at the end of July or beginning of August (1.4–18.9 °C Nostocophyceae Chroococcales* excl. Gomphosphaerioides in the Bothnian Bay, 1.9–20.7 °C in the Both- Gomphosphaerioides** nian Sea, 3.3–20.8 °C in the Öre Estuary, 4.0– Pseudanabaena spp. 22.6 °C in Tallinn Bay and 6.6–25.8 °C in the Planktothrix agardhii Curonian Lagoon Curonian Lagoon). However, some anomalies Anabaena spp. were correlated with upwelling events in coastal Aphanizomenon sp. A. flos-aquae in Curonian Lagoon areas, the most pronounced occurring in August Nodularia spumigena 1995 (Öre Estuary; mean surface layer tempera- Cryptophyceae ture 6.0–7.5 °C, long-term mean ± SD 14.0 ± Dinophyceae 3.3), July 1997 (Tallinn Bay; 7.8 °C, 16.3 ± 2.6 Dinophysis acuminata and Curonian Lagoon; 6.6 °C, 20.1 ± 4.2) and Gymnodiniales Heterocapsa rotundata August 2006 (Tallinn Bay; 7.5 °C, 16.4 ± 3.0). Heterocapsa triquetra The variation in salinity was higher, as expected, Prymnesiophyceae in the Curonian Lagoon where conditions alter- Chrysophyceae nated between nearly freshwater (minimum 0.05 Diatomophyceae psu) and brackish water (maximum 8.61 psu). Chaetoceros wighamii Actinocyclus normanii Curonian Lagoon The only statistically significant decreasing trend Cyclotella in mean salinity in the summer was observed in choctawhatcheeana Tallinn Bay between 1993 and 1998, and 1999 Skeletonema costatum and 2003 (from 5.89 to 5.67 psu; p < 0.01). Skeletonema subsalsum Curonian Lagoon There were only small differences in the con- Cylindrotheca closterium Eutreptiella gymnastica centrations of Ntot between the Gulf of Bothnia Prasinophyceae (average 16.6, range 7.1–23.1 µM) and Tallinn Chlorophyceae Bay (20.5 and 6.4–39.3 µM, respectively). How- Monoraphidium contortum ever, the concentrations of Ptot in the Gulf of Oocystis spp. Bothnia (0.24 and 0.09–0.61 µM), and especially Planctonema lauterbornii Curonian Lagoon Mesodinium rubrum no data from Curonian the Bothnian Bay (0.17 and 0.09–0.47 µM), Lagoon were markedly lower than those in Tallinn Bay (0.78 and 0.28–1.73 µM). The Curonian Lagoon * Chroococcales comprise the genera Aphanocapsa, was characterized by large variations in both Aphanothece, Chroococcus, Coelosphaerium, Cyano- variables and extremely high maximum values dictyon, Lemmermanniella, Merismopedia and Micro- cystis. (average 85.5 µM, range 10.7–204.9 µM for ** Gomphosphaerioides comprise the genera Coelo- Ntot; average 2.85 µM and range 0.42–9.98 µM moron, Snowella and Woronichinia. for Ptot). In brackish-water conditions, when the Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 197 salinity was > 5 psu, the concentration of both 35 1.4 TN nutrients was markedly lower (average 53.5 µM, 30 TP 1.2 Chl a ) range 21.4–84.2 µM for Ntot; average 1.75 µM –3 25 1.0 and range 0.42–4.20 µM for Ptot), but these P values were still higher than corresponding aver- 20 0.8 to t (µM) age values from the other study sites by factors 15 0.6 of 2.5 for Ntot and 2–10 for Ptot. (µM), Chl a (mg m 10 0.4

In Tallinn Bay, the mean concentrations of to t N Ntot and Ptot increased between periods 1 and 5 0.2 3 (16.7 to 23.4 µM, p < 0.001, and 0.67 to 0 0 0.85 µM, p < 0.001, respectively). In the same 1993–1998 1999–2003 2004–2008 area, the mean summer chlorophyll-a concen- Periods tration increased by 50% over the entire study Fig. 2. Variations in the concentrations of total nitrogen –3 period (3.2 to 4.8 mg m , p < 0.001) (Fig. 2). (Ntot, µM), total phosphorus (Ptot, µM) and chlorophyll a (Chl a, mg m–3) in Tallinn Bay between 1993 and 2008. Standard errors are shown as vertical boxes and stand- Seasonal phytoplankton patterns ard deviations as vertical lines.

Phytoplankton succession showed different timing patterns from north to south. In the Gulf community. The most frequent taxa in summer of Bothnia, the spring bloom often lasted until were Aphanizomenon sp., the dinophyte Dino- the end of June and mainly consisted of diatoms physis acuminata, chrysophytes and prymne- and dinoflagellates (up to 3.67 mgl–1). Nano- siophytes. The autotrophic biomass peaked in planktonic (< 20 µm) flagellates were usually July (median 0.88, maximum 3.54 mg l–1) when represented by crypto-, prasino- and prymne- cyanobacteria constituted over 50% of total bio- siophytes, the last being dominant in the open mass. However, large cyanobacterial blooms in Bothnian Sea. In July, phytoplankton biomass Tallinn Bay were only recorded in 1997 and dropped to the summer values and remained low 2002. In some years (1996, 2003, 2004 and until September (median 0.11–0.25, maximum 2008) dinophytes, mainly Heterocapsa triquetra, 0.30–1.86 mg l–1). Cyanobacteria (mainly Apha- briefly reached 70%–90% of the total phyto- nizomenon sp.) were briefly dominant, but only plankton biomass. The estimated proportion in July and August in the open Bothnian Sea, of nanoplanktonic flagellates (eugleno-, prym- while small-sized flagellates and the autotrophic nesio- and prasinophytes in July–August, and ciliate Mesodinium rubrum formed 40%–60% of cryptophytes in August–September) of the total the total phytoplankton biomass in all sub-areas biomass was on average ~20%. In September, of the Gulf of Bothnia. However, Aphanizome- diatoms reappeared and became the dominant non sp. had relatively low maximum biomass component of the phytoplankton, but in most values (0.3 mg l–1) in the open Bothnian Sea and years the phytoplankton biomass decreased 2–3 was rare in samples from the Bothnian Bay. In fold as compared with the maximum summer the Öre Estuary, diatoms (mainly Thalassiosira values. baltica) were the second largest contributors to Phytoplankton dynamics in the Curonian the total biomass in July and August after M. Lagoon differed substantially from the other rubrum. The percentage of unidentified taxa in study areas. Cyanobacteria, diatoms and chloro- the total phytoplankton biomass remained rela- phytes already dominated in June and the total tively high throughout the season (5%–16% on median biomass was 4.93 mg l–1 (maximum 18.4 average). mg l–1). In eutrophic water bodies, phytoplankton In Tallinn Bay, the total biomass in June biomass typically increases towards late summer varied from 0.05 to 2.63 mg l–1. Samples with and remains high until the end of the season. higher biomass contained mainly spring species The calculated median biomass for July–Sep- with dinoflagellates and diatoms dominating the tember ranged from 11.39 to 18.11 mg l–1 and the 198 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A)

100 Planktothrix agardhii summer phytoplankton. The most abundant green Aphanizomenon flos−aquae algal species, Planctonema lauterbornii, whose

80 abundance was constant during the summer, did not make a major contribution to the total bio-

) mass (2% on average, maximum 13%). −1 60

40 Changes in the biomass of the dominant

Biomass (mg l phytoplankton taxa

20 We observed a significant increase in the - aver age total summer autotrophic biomass in the 0 Bothnian Bay (0.11 to 0.34 mg l–1; p < 0.01) 1990 1995 2000 2005 and Tallinn Bay (0.58 to 0.87 mg l–1, p < 0.05) Year between the periods 1994–1998 and 1999–2003. –1 Fig. 3. Wet weight biomass (mg l ) of the filamentous The rise in total biomass in Tallinn Bay was cyanobacteria Aphanizomenon flos-aquae and Plank- most prominent in June (0.25 to 0.98 mg l–1, tothrix agardhii in the Curonian Lagoon between 1991 and 2007. p < 0.001). Different phytoplankton groups com- prised the autotrophic component of the phytoplankton biomass. Most of the statistically maximum values from 98.74 to 152.63 mg l–1 (in significant changes over the study period were July–September 1999 and August 2001). Only related to increases in the mean seasonal or one extremely high value (90.5 mg l–1) was monthly biomass values at different taxonomic recorded between 2004 and 2007. Both the nutri- levels. In this section, we mainly focus on the ent concentrations and the total phytoplankton dynamics of the cyanobacteria. biomass were markedly lower when brackish- Cyanobacteria were the dominant group in water conditions prevailed (salinity > 5 psu), the Curonian Lagoon (all seasons, up to 87% ranging from 0.54 to 13.5 mg l–1, with a median of the total phytoplankton biomass) and Tallinn of 3.0 mg l–1. However, salinity variation did not Bay (July to September, up to 74%). In the change the relationships between the dominant Bothnian Sea, cyanobacteria also contributed algal groups. 36%–57% at their peak, which occurred from Among the cyanobacteria, Aphanizomenon July to September, but they usually only con- flos-aquae, Planktothrix agardhii, Anabaena stituted ~20% of the total biomass. Increases in spp., gomphosphaerioids and chroococcalean cyanobacterial biomass were observed in the species constituted most of the biomass. Aphani- Gulfs of Bothnia and Finland between periods 1 zomenon flos-aquae was replaced by P. agardhii and 2. In addition, in the coastal Bothnian Sea, as the dominant cyanobacterium in the 2000s statistically significant increases were observed (Fig. 3). Actinocyclus normanii was the domi- between periods 2 and 3. An increase in the nant diatom species, constituting > 20% (maxi- cyanobacterial biomass in June was common in mum 65%) of the total phytoplankton biomass in both the open and coastal sites in the Bothnian freshwater conditions. In addition, Skeletonema Sea and Tallinn Bay (Fig. 4). The main cyano- costatum made a major contribution (mean 6.6%, bacterial species responsible for these biomass maximum 44%) to the total biomass in June. changes was Aphanizomenon sp. (maximum bio- Under brackish-water conditions, the dinoflag- mass in the Bothnian Sea and Tallinn Bay, 0.3 ellate Heterocapsa triquetra constituted up to and 1.5–2.0 mg l–1, respectively). The changes 65% (11% in average) of the total phytoplankton between July and September were insignificant biomass in July and August. In some cases the in all sub-areas. Small biomass increases of chlorophytes Pediastrum boryanum var. borya- the oscillatorean cyanobacteria Pseudanabaena num, P. duplex var. duplex and Oocystis lacus- sp. and the diazotrophic genus Anabaena were tris (10%–52%) contributed significantly to the observed in the Gulf of Finland. Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 199

The autotrophic ciliate Mesodinium rubrum 0.50 Summer showed a steady increase in June in Tallinn Bay, 0.40 and August in the Gulf of Bothnia between peri- 0.30 ods 1 and 2. Similarly to the changes observed in Tallinn Bay, the biomass of M. rubrum continued 0.20 to increase in the Bothnian Sea throughout the 0.10 season between periods 2 and 3. A decrease in 0 cryptophycean biomass was first observed in Tallinn Bay (from period 1 to 2) and the Gulf of 0.40 June Bothnia thereafter (from period 2 to 3). All other 0.30 biomass changes of the selected taxa were basin- 0.20 specific (see Tables 3 and 4). 0.10

0 Relationships between phytoplankton 0.75 and environmental factors ) July –1 0.60 The BIOENV analysis showed that water tem- 0.45 perature had the strongest impact on the summer 0.30 phytoplankton community structure, in combi- Biomass (mg l 0.15 nation with either salinity (Tallinn Bay and the 0 Curonian Lagoon) or nutrients (the Gulf of Both- nia) (Table 5). A similar pattern, but with weaker 0.40 August significance, was detected for cyanobacteria in 0.30 the Bothnian Bay and Öre Estuary. The biomass of diatoms had stronger relationships with tem- 0.20 perature and Ntot in Tallinn Bay and the Gulf of 0.10 Bothnia, but salinity largely explained the variation in the Curonian Lagoon. Small flagellates 0 were abundant in the summer phytoplankton 0.20 September in both the Gulf of Bothnia and Tallinn Bay, showing the best match with temperature in both 0.15 areas, but with Ptot in the Gulf of Bothnia and Ntot 0.10 in Tallinn Bay. The biomass of dinoflagellates 0.05 had no clear correlation with any of the measured environmental variables. 0 BB open BS open BS coastal GoF Until 1998 1999–2003 2004–2008 Discussion Fig. 4. Seasonal and monthly mean cyanobacterial biomass values (mg l–1) in different sub-areas (BB = Bothnian Bay, BS = Bothnian Sea, GoF = Gulf of Fin- Previous case studies have resulted in the rough land) during the study period. Note the different scales. geographic subdivision of the Baltic Sea into the southern and eastern coastal waters, and the northern and western waters. Southern and eastern green algae/cyanobacteria–diatoms and summer Baltic coastal waters are characterized by more dominance of dinoflagellates or N-fixing cyano extensive eutrophication, higher chlorophyll-a bacteria (Schiewer 2008). Our study sites covered concentrations and (in extreme cases) all-season the range of these environmental conditions, from dominance of cyanobacteria and green algae. heavy eutrophication in the Curonian Lagoon to In contrast, northern and western Baltic waters (largely) oligotrophy in the Gulf of Bothnia. As have distinct seasonal successions: diatoms– compared with the Gulf of Bothnia, Tallinn Bay 200 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) , + I X C uronian L agoon C hroococcales Gomphosphaerioides agardhii P. C ryptophyceae, VII < 0.05). Division of periods: t -test ( p , + I X , + VI & VIII , VII , VI oman numerals indicate that changes are valid are changes that indicate numerals R oman , VIII a , VII a , + VIII otal biomass, VI otal nitrogen, + VIII & I X otal phosphorus, + VI otal nitrogen, VI Gulf of Finland N ostocophyceae, VI Pseudanabaena Anabaena Aphanizomenon C. closterium , VIII I X M. contortum , + VI & VIII lauterbornii P. T T T Pseudanabaena C. choctawhatcheeana C. closterium , VII M. contortum , VII M. rubrum , VII & VIII T C hlorophyll M. rubrum , VI C hlorophyll , + VI , + VIII Bothnian S ea (coast) C hroococcales, VIII Dinophyceae D. acuminata C hrysophyceae C. closterium N ostocophyceae, + VI C hroococcales, + VI Gomphosphaerioides Aphanizomenon Diatomophyceae, I X Oocystis , VI M. rubrum , + VI , + VI oman numerals indicate the months with significant changes, “+” and “+” changes, significant with months the indicate numerals R oman Bothnian S ea (open) N ostocophyceae Dinophyceae, I X M. rubrum , VIII N ostocophyceae, VI Gomphosphaerioides Aphanizomenon M. rubrum S ignificant increasing trends for selected phytoplankton and environmentalWelch variables, two-sample analyzed using the otal biomass Bothnian Bay Gomphosphaerioides, I X Prymnesiophyceae Prasinophyceae M. rubrum , VIII c hroococcales, VII both for all seasons and the marked month. Table 3 . Table Increase between periods 1 and 2 n ostocophyceae t Increase between periods 2 and 3 Steady increase from period 1 to 3 1 = before 1999, 2 = 1999–2003, 3 = 2004–2008. = 3 1999–2003, = 2 1999, before = 1 Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 201

in the southern Gulf of Finland may be regarded as a transitional water body between these two < 0.05). extremes, showing either dominance of N-fixing cyanobacteria or dinoflagellates, mainly Hetero-

t -test ( p capsa triquetra, but considerably higher phytoplankton biomass during the summer period. C uronian L agoon Prymnesiophyceae C hrysophyceae

oman numerals identify that identify numerals R oman Changes in phytoplankton — Bothnian Bay

We observed increases in total phytoplankton biomass between 1994–1998 and 1999–2003 in , VI –1 , + VI the Bothnian Bay (0.11 to 0.29 mg l ). High phytoplankton biomass is a common indicator of eutrophication and increased phytoplankton biomass may correspond to an increase in avail- Gulf of Finland C hroococcales, + VI C ryptophyceae Gymnodiniales Prasinophyceae lauterbornii, VIII P. Gomphosphaerioides, I X C. wighamii S alinity Gomphosphaerioides D. acuminata Diatomophyceae, VI C hlorophyceae, VII – I X able nutrients. However, we did not detect any

significant changes in Ntot and Ptot contents in the Bothnian Bay over the study period. Slight

increases in Ntot and Ptot were observed at this site in the 1970s, but they subsequently stabilized and have decreased since that time (HELCOM 2009). In addition, the chlorophyll-a concentrations have remained at a roughly constant level (1.7–1.8 µg l−1) during the past 30 years (Flem- ing-Lehtinen et al. 2008). Hence, the increases otal nitrogen, VI

Bothnian S ea (coast) T in total phytoplankton biomass are difficult to explain. There was no shift in monitoring activi- oman numerals indicate the month with significant changes, “+” and “+” changes, significant with month the indicate numerals R oman ties between these two periods, thus the potential error of unbalanced weighting for a certain month within the season can be excluded. We conclude that the phytoplankton biomass was very low level during the whole summer period.

Open Bothnian Sea Bothnian S ea (open) C ryptophyceae Gymnodiniales The statistical analysis revealed an increase in cyanobacterial biomass between 1994–1998 and 1999–2003. The cyanobacteria responsible included the filamentous speciesAphanizomenon sp. in June. Similarly to the observed changes in the Bothnian Bay, the biomass of M. rubrum first increased in August and the species became abundant over the whole season in later years.

S ignificant fluctuations and decreasing trends for selected phytoplankton and environmental variables, analyzed using the Welch two-sample Our data demonstrated that the spring bloom often lasted until the end of June. Andersson otal biomass, I X

Bothnian Bay Diatomophyceae et al. (1996) observed a M. rubrum peak in the Higher values during period 2 t Decrease between periods 1 and 2 C ryptophyceae, + VIII Decrease between periods 2 and 3 Table 4 . Table Division of periods: 1 = before 1999, 2 = 1999–2003, 3 = 2004–2008. = 3 1999–2003, = 2 1999, before = 1 periods: of Division changes are valid for all seasons and the marked month. Bothnian Sea after the spring bloom, thus the 202 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) increasing biomass of this species together with ca. two times lower in the Bothnian Bay than Aphanizomenon sp. in June may have resulted in the Bothnian Sea during the summer period from an earlier decline of spring communities and (June–September) (Andersson et al. 1996). replacement by summer species during the last Our data generally confirm these observations, decade. In contrast, in a study of the Gulf of Fin- despite the increasing trend in the Bothnian Bay land, the ciliate M. rubrum showed a strong posi- at the beginning of the 2000s, which has inter tive correlation with salinity and a negative cor- alia reduced the difference in biomass bewteen relation with temperature (Rantajärvi et al. 1998). the two areas in July. As in the Bothnian Bay, we did not detect any trends in Ntot and Ptot contents, but observed significant changes in the total phytoplankton Coastal Bothnian Sea — Öre Estuary biomass over the study period in the open Both- nian Sea. For comparison, the summer con- The concentrations of Ntot have followed the centrations of chlorophyll a had increased until same trends in the coastal zone of the Bothnian the end of the 1990s and declined thereafter Sea as in the open sea, with an increase during (Fleming-Lehtinen et al. 2008, HELCOM 2009). the 1970s and a decline thereafter. Both the

Observations from the beginning of the 1990s increase and decline in Ptot were larger in the indicate that the total biomass (wet weight) was coastal zone, magnifying the overall pattern in

Table 5. The results of BIOENV analyses. The best combination of environmental variables and the strength of their relationships with the biomass of the total phytoplankton community and selected groups in different sub-areas r of the Baltic Sea using Spearman’s rank correlation ( s). n = number of observations.

Best combination of variables ρs n

All phytoplankton

Bothnian Bay T °c ntot 0.278 73

Bothnian Sea T °C Ptot 0.32 66

Öre Estuary T °C Ptot 0.232 81 tallinn Bay T °c sal 0.247 138 curonian Lagoon Sal t °c 0.565 72 Cyanobacteria Bothnian Bay Sal t °c 0.072 73

Bothnian Sea T °C Ptot 0.286 66 Öre Estuary T °c 0.075 81 tallinn Bay T °c sal 0.246 138

curonian Lagoon T °C Ptot ntot sal 0.462 72 Dinoflagellates Bothnian Bay T °c 0.055 73 Bothnian Sea T °c 0.158 66

Öre Estuary Ntot t °c 0.039 81 tallinn Bay Sal t °c 0.116 138 curonian Lagoon Sal t °c 0.051 72 Diatoms

Bothnian Bay Ntot 0.173 73

Bothnian Sea T °c ntot 0.079 66

Öre Estuary T °c ntot 0.202 81

tallinn Bay Ntot t °c 0.115 138 curonian Lagoon Sal 0.466 72 Small flagellates (crypto-, prymnesio-, chryso-, eugleno- and prasinophytes

Bothnian Bay T °C Ptot 0.198 73

Bothnian Sea Ptot t °c 0.186 66

Öre Estuary Ptot t °c 0.193 81

tallinn Bay T °c ntot 0.171 138

curonian Lagoon Sal Ptot 0.361 72 Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 203

this region (HELCOM 2009). The Ntot values we ditions in recent decades. Analyses of a large set obtained were similar across the entire Gulf of of data obtained from different parts of the Baltic

Bothnia. However, the Ptot concentrations were Sea indicated that phytoplankton composition markedly higher in both the coastal and open changes with variations in nutrient levels, but parts of the Bothnian Sea as compared with those the composition does not shift abruptly, and only in the Bothnian Bay, marking a switch from P small changes in the phytoplankton community limitation to N limitation. In contrast, the concen- occur in response to moderate increases in nutri- tration of dissolved inorganic phosphorus (DIP) ent levels (Carstensen and Heiskanen 2007). was markedly lower in the coastal zone of the Bothnian Sea than in open waters, and bioassays have shown that this area is still P-limited. Such The Gulf of Finland — Tallinn Bay conditions do not favour the dominance of N-fixing cyanobacteria (Andersson et al. 1996). The Gulf of Finland is regarded as one of the The changes in the phytoplankton commu- areas most affected by eutrophication in the nity varied significantly in the coastal waters, as Baltic Sea, with a nutrient load per unit of water compared with those in the open waters. We also area 2–3 times higher than the average (Pitkänen observed an earlier appearance of cyanobacteria, et al. 2001). Consequently, the higher cell abun- especially Aphanizomenon sp., in both areas dancies of phytoplankton as compared with after the spring bloom. However, the overall those in the Gulf of Bothnia are likely to be due increase in cyanobacterial biomass occurred later to eutrophication. However, the growing season in the coastal waters (between 1999–2003 and is also longer in the Gulf of Finland, which may 2004–2008) than in the open Bothnian Sea. A also contribute to this pattern. As compared common feature in this region was the increased with the other study sites, the changes in both biomass of M. rubrum and gomphosphaerioids environmental variables and phytoplankton have during the last period. Increases in the biomass been more dynamic at this site and have included of the dinophyte Dinophysis acuminata, chryso- both upward and downward trends. phytes and the diatom Cylindrotheca closterium Previous studies have shown that trends in were observed from 1994 to 1998 and from concentrations of Ntot and Ptot differed in recent 1999 to 2003, and for Chroococcales between decades, but overall they have been increasing 2004 and 2008; these features were typical of since the 1990s (HELCOM 2009). We found the coastal waters. Chrysophytes also increased same trends for both nutrients in the southern in summer phytoplankton communities in the Gulf of Finland, but while significant increases northern Baltic Proper and the Gulf of Finland of both nutrients occurred at the start of the

(Suikkanen et al. 2007). According to mesocosm 2000s, they only continued for Ntot in June. In experiments described by Kangro et al. (2007), addition, the summer chlorophyll-a concen- some species of chroococcales (Cyanodictyon trations have been continuously increasing in sp.) and chrysophytes (mainly Pseudopedinella Tallinn Bay (by ~50% since 1993), which is spp.) are favoured by N addition, while D. acu- consistent with the results of Fleming-Lehtinen minata and C. closterium respond positively to et al. (2008), who found an increase of more P enrichment. The positive biomass response of than 150% in the surface chlorophyll-a concen- C. closterium to an increase in P has also been trations in the open parts of the Gulf of Finland demonstrated in natural communities in the Gulf from the 1970s to the present. Nevertheless, of Finland (Jaanus et al. 2009). The latter species the total phytoplankton biomass in Tallinn Bay does not yet dominate in the coastal phytoplank- increased significantly only in June between ton of the Bothnian Sea, but its presence is a 1994–1998 and 1999–2003, accompanied by an sign of a changing environment. Cylindrotheca increase in cyanobacterial biomass, especially closterium has been proposed as an indicator Aphanizomenon sp. of eutrophication in the northern Baltic Sea Finni et al. (2001a) showed that cyanobac- (Jaanus et al. 2009). The coastal waters of the terial blooms have been common in the Gulf Bothnian Sea had relatively stable nutrient con- of Finland for many years, but Gasiūnaitė et 204 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) al. (2005) suggested that cyanobacterial blooms also observed a decrease in summer salinity are highly variable, due to their inhomogeneous accompanied by an increase in cyanobacterial distributions in time and space, which hinders biomass in the Gulf of Finland, and an analy- the identification of steady trends. Accordingly, sis of extensive phytoplankton datasets from the only trends we found in this respect were the same area confirmed that oscillatorean bio- that the dominance of cyanobacteria changed, mass is negatively correlated with salinity, but and they became more abundant earlier in the positively correlated with temperature and Ptot year, although we sampled as frequently as every (Jaanus et al. 2009). In recent decades, the second to third week and hence expected to biomass of Oscillatoriales also increased in the detect almost all bloom events. The lack of clear eastern part of the Gulf of Finland (Nikulina trends may be due to the effects of temperature, 2003). Ptot concentrations had been low in the which has been shown to be one of the most 1970s, increased to much higher levels in the important contributors to variations in cyano- 1980s, then declined but have subsequently fur- prokaryote assemblages in various parts of the ther increased since 1990 (HELCOM 2009). Baltic Sea (Laamanen 1997, Pliński et al. 2007). Notably, high water temperature has often been suggested as a prerequisite for intensive bloom The Curonian Lagoon development, for example, the optimal temperature for A. flos-aquae ranges from 16 to 22 °C Finni et al. (2001b) identified the intensive (e.g. Pliński et al. 2007). However, in 2002, a growth of phytoplankton communities during cyanobacterial bloom in the southern Gulf of the entire vegetation period and very high late Finland had already peaked by the end of June at summer total wet weight biomass (> 10 mg l–1) a surface water temperature of 14–16 °C (Jaanus as indicators of hypereutrophic conditions. The and Pellikka 2003). The earlier appearance of total phytoplankton biomass estimated in the cyanobacteria and the decline of the cold-water Curonian Lagoon exceeded 100 mg l–1 in July diatom Chaetoceros wighamii in summer phy- and August in 1999 and 2001. As only one toplankton may represent an earlier succession extremely high value (90.5 mg l–1) was recorded towards summer communities as a result of during 2004–2007, we did not observe any clear the rise in surface water temperature. Increased trends in total biomass in this area. However, temperature can even have a greater stimulatory Planktothrix agardhii appeared to competitively effect on phytoplankton than excess nutrients. exclude Aphanizomenon flos-aquae from domi- For instance, long-term phytoplankton studies nating filamentous cyanobacterium in this region. in the discharge area of power plant effluents Johansson and Wallström (2001) considered have shown a decrease in the biomass of C. P. agardhii to be indicative of nutrient-rich con- wighamii caused by the rise in water temperature ditions and Carstensen and Heiskanen (2007) (Ilus and Keskitalo 2008). The preference of C. proposed it to be the only species that character- wighamii for more saline and cold-water condi- izes eutrophic conditions in the northern part tions has also been found in a previous study in of the Baltic Sea, since it responds positively the Gulf of Finland (Rantajärvi 1998). Although to increased Ntot levels. This species was sur- our results do not show any significant increase veyed during summer throughout the 20th cen- in surface water temperature, it is possible that tury, when temperature conditions were stable only a very small change may have occurred and until the 1990s in the coastal waters surrounding further changes may cause major shifts in the the cities of Stockholm and Helsinki (Johansson dominant phytoplankton species. and Wallström 2001, Finni et al. 2001b). These Our statistical analysis revealed that some authors attributed the decrease in total biomass other filamentous cyanobacteria (Anabaena spp. and change in phytoplankton dominance from P. and Pseudanabaena sp.) have become more agardhii to a more species-rich community to an abundant in Tallinn Bay since the late 1990s. effective reduction in nutrient load. Despite the These changes correlated with the decrease in water quality improvement in some Lithuanian surface water salinity. Suikkanen et al. (2007) rivers, the Nemunas (the main river discharging Boreal Env. Res. vol. 16 (suppl. A) • Changes in phytoplankton in the Baltic Sea during 1990–2008 205 into the Curonian Lagoon) is still affected by the basis of phytoplankton composition is ambig- municipal and industrial wastewater from Russia uous. The likely long-term effects of increas- and accounts for half of the total nutrient loading ing nutrient concentrations (eutrophication) on (Cetkauskaite et al. 2001). phytoplankton stocks could not be definitively In the Curonian Lagoon, the concentrations determined, because of the overriding effect of of inorganic nutrients are too high to limit total hydrographic changes. Finni et al. (2001b) char- plankton biomass, which is mostly controlled acterized moderately eutrophic coastal water by the ambient physical factors (Pilkaytitė and bodies by the presence of only modest amounts Razinkovas 2007). For example, high rates of of cyanobacteria and gomphosphaerioids rather freshwater discharge reduce both salinity and than oscillatorialean species. These authors also residence time. These conditions generally favour found that small flagellates (crypto-, prymnesio-, fast-growing phytoplankton, such as chlorophytes chryso-, prasinophytes and the euglenoid Eutrep- (green algae) and various flagellates, members of tiella spp.) dominated coastal water bodies and which have been shown to grow optimally under that summer algal blooms are unusual where low salinity conditions (Pinckney et al. 1999). In there is moderate eutrophication. Such a commu- locations with highly turbulent mixing, freshwa- nity structure is more characteristic of the Gulf of ter diatoms may start to dominate summer phyto- Bothnia, which is considered to be non-eutrophic plankton communities rather than cyanobacteria unlike the other surveyed regions. The increased (Rehbehn et al. 1993, Pilkaitytė 2007). However, abundance of planktonic diatoms in the coastal cyanobacteria and diatoms formed a large over- waters of the Gulf of Finland, especially some all component of the total phytoplankton bio- fragile diatom (e.g. small centrales, Skeletonema mass in the Curonian Lagoon and chlorophytes spp., and Chaetoceros minimus) have also been were only the third largest contributors. Although attributed to increased eutrophication and turbid- small flagellates were abundant, their relative ity (Finni et al. 2001b, Weckström et al. 2007). importance in terms of total biomass remained Some small diatoms (e.g. Cylindrotheca closte- low throughout the season. rium and Cyclotella choctawhatcheeana) have Salinity best explained the variation in phy- become more common in the Gulf of Finland toplankton biomass, especially that of diatoms. and already appear in the phytoplankton of the A gradual increase in salinity, due to mixing of Bothnian Sea. Thus, the hypothesis that nutrient- river plumes with sea water, has been associated rich conditions promote the growth of relatively with reductions in nutrient concentration and large planktonic species (e.g. Thingstad and Sak- phytoplankton biomass. Dilution of the high bio- shaug 1990) might not be valid for much of the mass of riverine phytoplankton, however, does Baltic Sea. A mesocosm experiment, in which not result in a steady decrease in all components, seawater from the northern Baltic Sea was used, but in the successive disappearance of different has revealed that relatively small phytoplankton freshwater species (Wasmund et al. 1999). In species appear to be favoured by nutrient loading the Curonian Lagoon, cyanobacteria, diatoms and the average cell-size does not increase with and chlorophytes were still the dominant groups nutrient enrichment (Andersson et al. 2006). when brackish-water conditions prevailed, but However, Niemi (1975) reported that small flag- the median total biomass was ca. 5-fold lower in ellates had considerably contributed to the pri- comparison to the entire dataset of the same area. mary production in the Gulf of Finland since the As the phytoplankton biomass, the mean concen- 1960s, when eutrophication processes were not trations of Ntot and Ptot also decreased by a factor yet occurring, at least in offshore waters. of 1.6 when surface water salinity was > 5 psu.

Overall changes in the phytoplankton Phytoplankton species composition as communities an indicator of eutrophication Significant differences were found in phytoplank- Classification of eutrophic water conditions on ton biomass from class to species level in all 206 Jaanus et al. • Boreal Env. Res. vol. 16 (suppl. A) basins during the study period. Tallinn Bay was perature may influence the northernmost area, the most dynamic according to observed changes particularly the Gulf of Bothnia, most strongly. in both environmental factors and phytoplankton. We found that cyanobacterial biomass increased Observations at Tallinn Bay have been made over time in this region, but the biomass values with similar intensity throughout almost all of of Aphanizomenon were still far from strong the study period, while the frequency of sam- blooms (maximum 0.3 mg ww l–1 compared pling has decreased in the open Gulf of Bothnia with 1.5–2.0 mg ww l–1 in the Gulf of Finland). and Curonian Lagoon. The differences in mean Biomass of the potentially toxic cyanobacterium biomass of the dominant taxa between periods Nodularia spumigena, which favours water tem- should be interpreted with caution, as the data peratures > 20 °C (Lehtimäki et al. 1997), did sets were less homogeneous for the Gulf of Both- not show any clear trends in our study. Although nia and the total number of sampling intervals phytoplankton biomass and species composi- was relatively low in the Gulf of Bothnia and tion are influenced by different mechanisms, the Curonian Lagoon. This probably explains the impact of climate change may be overwhelm- high interannual variation and fewer significant ing in the future and induce changes at higher changes (trends) observed over the study period trophic levels. in these regions than in the Gulf of Finland. Our results highlight the importance of regu- Acknowledgements: Samples examined in this study were lar, frequent phytoplankton monitoring in order collected during several phytoplankton monitoring programs funded by the Swedish Environmental Protection Agency to reliably detect ecosystem shifts, especially and the Estonian Ministry of Environment. The work was over short-term spatio-temporal scales, which is partly supported by the MEECE (Marine Ecosystem Evolu- essential for detecting natural variations. tion in a Changing Environment) project of the European Changes in phytoplankton biomass and spe- Union 7th Framework Programme. We thank the Centre of cies composition reflect not only the effects of Marine Research (Klaipeda, Lithuania), the Estonian Marine Institute and the Umeå Marine Sciences centre for sampling, eutrophication but also climatic change. Sea- analyses and providing data for this study. We also thank the sonal temperature variation may markedly influ- two anonymous reviewers for constructive comments and ence the performance and succession of phyto- suggestions. plankton over the year (Andersson et al. 1994). Temperature was the key physical factor shaping the phytoplankton communities, especially the References total wet weight biomass and the biomass of cyanobacteria in all of the sub-areas we studied. Alheit J., Möllmann C., Dutz J., Kornilovs G., Loewe P., Mohrholz V. & Wasmund N. 2005. Synchronous regime Both experimental results and models indicate shifts in the central Baltic and the North Sea in the late that cyanobacteria respond more strongly to cli- 1980s. ICES J. Mar. Sci. 62: 1205–1215. mate change than diatoms or green algae (De Andersson A., Haecky P. & Hagström Å. 1994. Effect of Senerpont Domis et al. 2007, Moore et al. 2008). light and temperature on the growth of micro-, nano- and We did not detect any significant differences in picoplankton. 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