Journal of Sea Research 61 (2009) 114–123

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Journal of Sea Research

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Long-term changes in phytoplankton in the Kattegat, the Belt Sea, the Sound and thewestern Baltic Sea

Peter HenriksenNational Environmental Research Institute, Aarhus University, Frederiksborgvej 399, DK-4000 Roskilde, Denmark

E-mail address: pet@dmu.dk.

1385-1101/$ – see front matter © 2008 Elsevier B.V. Aldoi:10.1016/j.seares.2008.10.003

a b s t r a c t

a r t i c l e i n f o

Article history:

The development in bioma Received 5 October 2008Accepted 6 October 2008Available online 17 October 2008

Keywords:PhytoplanktonEutrophicationClimate ChangeSpecies CompositionWater Framework Directive

ss and dominant groups and species of phytoplankton was examined at sixmonitoring stations in the Kattegat, the Belt Sea, the Sound and the western Baltic Sea. Since the initiation ofthe monitoring in 1979 the biomass of phytoplankton has decreased significantly. The decrease correlatedwith Danish nitrogen loads to the Danish Straits but also with increases in surface water temperature. Thedecline in biomass was mainly due to less pronounced spring blooms in the Kattegat and the Belt Sea andreduced biomass during late summer–autumn on all stations. Diatoms have been the overall dominantphytoplankton group on all stations but the western Baltic Sea. However, their contribution to the totalbiomass has varied considerably throughout the monitoring period as during the years 1987–1989phytoplankton was dominated by an unusually high dinoflagellate biomass. A qualitative comparisonshowed that the dominant species (diatoms and dinoflagellates) found in plankton net tows taken duringspring and autumn around year 1900 were still among the dominant species during the monitoring period1979–2006. However, several of the dominant species found during the latter period were not present in thesamples taken around year 1900 despite that they should have been captured by the methods used.

© 2008 Elsevier B.V. All rights reserved.

1. Introduction

Phytoplankton is the base of the pelagic marine food web. Primaryproduction and phytoplankton biomass will depend on availability ofnutrients for growth. The close coupling between the supply ofnutrients and the potential phytoplankton biomass and, in addition,potential ecological and economical effects of blooms of toxic phyto-plankton led to the inclusion of routine quantification of phytoplank-ton in the Danish marine monitoring program in 1979. Subsequentlyphytoplankton biomass (either C biomass or the concentration ofchlorophyll a as a proxy of phytoplankton biomass) has been used asone of the measures of effects from three consecutive Danish actionplans for the aquatic environment initiated in 1987, 1998 and 2005,respectively.

Phytoplankton is one of the biological quality elements to be usedfor assessment of the ecological status of coastal waters according tothe European Water Framework Directive (WFD; 2000/60/EC). Pivotalto the assessment is the definition of reference conditions (i.e. con-ditions representing no anthropogenic disturbance) and acceptabledeviations from the reference conditions for the given qualityelement. During the initial European intercalibration of assessmentsonly the concentration of chlorophyll a and a few area-specific indi-

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cator species (e.g. Phaeocystis sp. in the north–east Atlantic region)were included. However, the WFD requires that future assessmentsinclude phytoplankton composition as may also be expected from therecently adopted European Marine Strategy Framework Directivecovering open waters. Quantitative data on phytoplankton composi-tion in Danishwaters date back to only 1979 and thus do not representreference conditions. In contrast, semi-quantitative or qualitativeplankton net samples were collected ca. biweekly during 1897–1901in the Kattegat, the Belt Sea and in the Sound by Ostenfeld (1913) andin the Sound in 1931 by Cleve-Euler (1937). One aim of the presentstudywas to examine if these historical qualitative data collected priorto the intensified use of agricultural fertilizers and concurrenteutrophication of marine areas revealed long-term changes in thedominant species of phytoplankton.

During the last decade climate change and global warming havereceived much attention. A number of studies from the North Sea andthe Baltic Sea have shown changes in abundance, composition andannual succession of phytoplankton related to the North AtlanticOscillation (NAO), the weather pattern affecting northern Europe(Reid et al., 1998; Wasmund and Uhlig, 2003; Edwards andRichardson, 2004; Wiltshire and Manly, 2004; Alheit et al., 2005).Some observed changes in phytoplankton have been the longerduration of elevated biomass from the late 1980s in the North Sea(Reid et al., 1998) and higher spring bloom biomass in the Baltic Sea(Alheit et al., 2005) coupledwith increased dinoflagellate contributionto the spring bloom biomass (Wasmund and Uhlig, 2003). A second

Fig. 1. Geographical location of stations. Black circles represent monitoring stations with station number. Grey circles represent stations sampled by Ostenfeld (1913) during 1897–1901 (A–E) and by Cleve-Euler (1937) in 1931 (F). Note overlap between station 925 and C.

115P. Henriksen / Journal of Sea Research 61 (2009) 114–123

aim of the present study was to examine if these patterns are alsoreflected in the long-term Danish monitoring data.

2. Methods

Data on phytoplankton, Secchi depth, temperature and surfacewater salinity has been collected as part of the Danish national marinemonitoring program. The six stations included in this study coveredthe Kattegat (stations 409, 413 and 925), the Belt Sea (station 939), theSound (station 431) and the western Baltic Sea (station 444) asillustrated in Fig. 1. Quantitative phytoplankton samples werecollected during the following time periods at the different stations;Station 409: 1981–2006, station 413: 1981–1997, station 925: 1982–

Fig. 2. Mean annual biomass of phytoplankton. Each marker represents the mean of allstations. Bars show standard errors.

2006, station 431: 1979–2006, station 939: 1979–1997 and station444: 1979–1997. In addition, historical data from plankton net towswere available from 1897–1901 from five stations (A–E) in theKattegat, the Belt Sea and the Sound (Ostenfeld, 1913) and from onestation (F) in 1931 in the Sound (Cleve-Euler, 1937) (Fig. 1). In thehistorical data sets species were assigned a rank on a five-level scaleranging from ‘very rare’ to ‘very common’. Species assigned ‘common’or ‘very common’ in the historical data sets were used for comparisonwith quantitative data collected during the monitoring period 1979–2006 to evaluate long-term changes in dominant phytoplankton.

Phytoplankton samples from the monitoring program wereintegrated samples (surface to 10 m depth) preserved in Lugols' solu-tion and enumerated in the invertedmicroscope according to HELCOM

Fig. 3. Relationship between N inputs to the Danish Straits and phytoplankton meanannual biomass for the period 1979–2006. N inputs represent yearly values from July ofthe previous year to June of the given year.

Fig. 4. Relationship between mean annual surface water temperature and mean annualbiomass of phytoplankton for the period 1979–2006.

116 P. Henriksen / Journal of Sea Research 61 (2009) 114–123

procedures (HELCOM, 1988). Organisms were identified to species,genus or class/group (in case of specimens to small to identify in themicroscope) and phytoplankton carbon biomass was calculated fromcell counts and dimension measurements assuming simple geometric

Fig. 5. Development of N inputs to the Danish Straits, Secchi depth and phytoplankton biomaKattegat and C: phytoplankton biomass at station 409 in the northern Kattegat. Boxes showvalues outside this interval. Bold horizontal lines represent the mean.

shapes and using conversion factors of 0.13 and 0.11 pg C μm−3 forthecate dinoflagellates and other phytoplankton groups, respectively.Carbon contents of diatoms were corrected for lower C content of cellvacuoles [pg C (μm3 vacuole)−1=0.1⁎pg C (μm3 plasma volume)−1]according to Edler (1979).

Measurements of Secchi depth originated from the Danish nationalmarine data base (http://mads.dmu.dk) supplemented with data fromthe 1960s to 1970s from lightships in the Kattegat. Historical Secchidepthdata fromthenorthernKattegat during1908–1911were obtainedfrom the ICES data base (http://www.ices.dk/Ocean/project/secchi/).

Estimates of nitrogen inputs to the Danish Straits were calculatedon a yearly basis from July to the following June as surpluses from theDanish agricultural sector as described in Conley et al. (2007).

Similarity and dissimilarity between phytoplankton samples(individual samples or annual mean biomass divided into the differentgroups of phytoplankton) was examined by SIMPER-analysis (Primersoftware) using 4th root transformed as well as untransformed data.

Development of total phytoplankton biomass over time as well asrelationships between phytoplankton biomass and N-inputs andtemperature, respectively, were analysed by linear regression (Micro-soft Excel software).

ss over the last century. A: N inputs to the Danish Straits, B: Secchi depth in the northern25th–75th percentiles, bars the interval from the 10th to the 90th percentile and circles

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3. Results

3.1. Annual biomass of phytoplankton

Since the beginning of the monitoring program in 1979 the meanannual biomass has decreased on all stations. When combining allstations, the mean annual biomass showed annual variations around200 μg C l−1 until the mid 1980s and declined to around or below100 μg C l−1 from the early 1990s (Fig. 2). The decrease in biomass forthe whole monitoring period was significant (Pb0.001) while nosignificant trend was found for the mean biomass after 1990.

The mean annual biomass correlated significantly (Pb0.001) withinputs of N to the Danish Straits (Fig. 3). In addition, the mean annualbiomass showed a significant (Pb0.001) negative relation with meanannual temperature of the surface water (Fig. 4).

While quantitative phytoplankton data are available only for theperiod after 1979 measurements of Secchi depth were taken in thenorthern Kattegat near station 409 as early as 1908–1911 and furthermeasurements were taken during the 1960s and 1970s at lightships in

Fig. 6. Contributions from different groups of phytoplankton to the mean annual biomass. Unmicroscopy.

Læsø Rende, Ålborg Bay and at Anholt Knob (stations A, 409 and B inFig. 1). In several areas it has been shown that Secchi depth is coupledto chlorophyll a, a proxy for the biomass of phytoplankton (e.g.Sandén and Håkansson, 1996; Hoyer et al., 2002). Presumably this isalso the case in the Kattegat during summer with low frequency ofhigh wind events and low re-suspension of particulate matter in thispermanently stratified area. The development in Secchi depth in thenorthern Kattegat hasmirrored N-inputs to the Danish Straits over thelast 100 years as well as the biomass of phytoplankton over the last30 years (Fig. 5).

During themonitoring period 1979–2006 the overall composition ofphytoplankton has changed (Fig. 6). In addition, differences in dominantphytoplankton groups were found between the six stations (Fig. 6).Cyanobacteria have been major contributors to the total biomass atstation 444 in the western Baltic Sea and minor contributors at stations431 and 939 in the Sound and the Belt Sea, respectively, while this grouphas had no quantitative importance at the remaining three stations inthe Kattegat (Fig. 6). Diatoms and dinoflagellates have been the majorphytoplankton groups at all stations but 444 in the western Baltic Sea.

identified organisms were mainly nano- and picoplankton too small to identify by light

Fig. 6 (continued).

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Diatoms was the dominant phytoplankton group in the Kattegat(stations 409, 413 and 925) and the Belt Sea (station 939) during theearly to mid 1980s while the years 1987–1989 were characterised byunusual high biomass of dinoflagellates and low biomass of diatoms inthe Kattegat (stations 409, 413 and 925) and the Sound (station 431).

No significant difference in annual surfacewater salinity was foundfor the three decades 1979–1989, 1990–1999 and 2000–2006.

3.2. Monthly biomass and dominant species

When pooling data by decade (1979–1989, 1990–1999 and 2000–2006) the monthly biomass generally declined over time (Fig. 7). Dueto a slightly different sampling scheme at the different stations in the1980s and 1990s it is not possible to evaluate the decadal change inbiomass for January, February, April and June. The most conspicuousreductions in monthly biomass were found during spring in Kattegatand the Belt Sea and during summer–autumn (July–October in thewestern Baltic Sea, the Belt Sea and the Sound, and August–October in

the Kattegat). The reduction in spring biomass was significant(ANOVA, Pb0.001) from the 1980s to the 1990s while the 1990s didnot differ significantly from the period after 2000. Biomass duringAugust–October estimated from the pooling of all stations decreasedsignificantly (ANOVA, Pb0.001) from the 1980s to the 1990s andfurther (P=0.002) from the 1990s to the period after 2000.

A SIMPER-analysis of dissimilarity between phytoplankton sam-ples from the three decades was conducted for spring (March) andautumn (August–October). The main contributors to dissimilaritybetween the three decades were the diatoms Detonula confervaceae,Skeletonema costatum, Thalassiosira spp., Chaetoceros spp., Rhizosole-nia fragilissima and Guinardia flaccida and the dinoflagellates Ceratiumspp. (especially C. tripos and C. furca) and Prorocentrum minimum. Theannual occurrences of these species and two additional importantdiatom species/genera (Pseudo-nitzschia spp. and Cerataulina pelagica)throughout the monitoring period are shown in Fig. 8. Species/generatypically occurring during spring were D. confervaceae, S. costatumand Thalassiosira spp. The genus Chaetoceros occurred during spring

Fig. 7.Meanmonthly biomass of phytoplankton for the three decades covered by the monitoring program. Data from 1979 is included in the 1980s decade. Biomass is shown only if aminimum of two samples was available for the given month.

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and autumn while the remaining species/genera were found in highbiomass mainly in autumn (Fig. 8).

The occurrence and biomass of the individual species/genera havevaried during the monitoring period. D. confervaceae, C. pelagica, S.costatum, Chaetoceros spp. and Thalassiosira spp. were found in highbiomass during the 1980s. Subsequently, the biomass of C. pelagica and,in particular, D. confervaceae has been lower and the occurrence moreinfrequent (D. confervacea). High biomass of Pseudo-nitzschia spp. wasrepeatedly found after 1990. The first record of the dinoflagellate P.minimum in Danish waters is from 1981 (Bjergskov et al., 1990). Duringthe 1980s and until the mid-1990s it formed characteristic late summerblooms. Subsequently, since the mid-1990s, the biomass of P. minimumduring July–August has been lower than during the 1980s and early1990s. The genus Ceratium was found throughout the monitoringperiod, initially mainly from September to November but graduallyincreasing the seasonal occurrence to cover most months of the year.Especially the years 1987–1989 were characterised by high biomass.After 1998 the highest biomass has been found from June (May in 2000)to November.

Comparison of the monitoring data with historical studies ofphytoplankton from 1897–1900 and 1931 should be done with cautiondue to the different sampling techniques employed. Species designated‘common’ or ‘very common’ in the historical net samples were taken asthe dominant species for comparisonwith recent data. A similar numberof species (10–11) were chosen from each of the decades 1979–1989,1990–1999 and 2000–2006 prioritised by mean biomass during the

given decade. A comparison of dominant species chosen this way isjustifiedby the fact thatmost dominant species in the recentmonitoringdata were also registered in the historical data though sometimes as‘rare’ or only in other geographical areas than those covered by themonitoring data from 1979–2006. Thus, it can be concluded that the netsamples would have included most of the dominant species from therecentmonitoring period given they were present. Dominant species inthe recentmonitoring data not registered in the historical datawere of asize that would have ensured their retention in the plankton nets usedfor collection of the historical samples with the possible exception ofChattonella sp. (recently renamed Verrucophora farcimen by Edvardsenet al. (2007)).

Historical net samples and recent quantitative samples showedthat most of the dominant species a century ago were still among thedominant species during 1979–2006 (Table 1). In particular severalspecies of Chaetoceros and S. costatum were characteristic of thephytoplankton community in March in the historical data as well as indata collected during the monitoring period 1979–2006. During the1980s D. confervaceae and S. costatum were the most typical speciesfound in March. Since the 1990s several others, especially species ofThalassiosira and Coscinodiscus, have been among the dominantspecies in March. After 1998 Chattonella sp. (=V. farcimen) has beena characteristic dominant spring species.

A change in dominant species from historical data to themonitoringdata (1979–2006) wasmore evident for late summer–autumn (August–October) than for spring (Table 2). The dominant species in both

Fig. 8. Seasonal occurrences of 10 species that were main contributors to the differences between the three decades. Bubbles indicate the average biomass (μg C l−1) at all six stationsduring the given month and year. Note the different scaling of biomass between species.

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historical and monitoring data was the dinoflagellate Ceratium tripos. Inthe historical data other dominant species included additional species ofCeratium, several species of Chaetoceros and the large diatoms Proboscia(=Rhizosolenia) alata, Eucambia zoodiacus and Rhizosolenia calvar avis.During the monitoring period 1979–2006 the August–October phyto-

planktonwas dominated by several species not found in 1897–1900; thedinoflagellates Prorocentrum micans, P. minimum, Karenia mikimotoi(=Gyrodinium aureolum) and Gymnodinium chlorophorum and thediatoms Rhizosolenia fragilissima and Pseudo-nitzschia spp. In addition,the dinoflagellates Ceratium furca and C. lineatum and the diatoms G.

Table 1Dominant species in March

1899–1901 1931 1980s 1990s After 2000

DiatomsChaetoceros decipiens XChaetoceros diadema XChaetoceros spp. X XRhizosolenia hebetata f. semispina X X XSkeletonema costatum X X X X XChaetoceros debilis X XChaetoceros holsaticus X XChaetoceros socialis X X X XThalassiosira nordenskiöldii X X XRhizosolenia setigera X XThalassionema nitzschioides XAchnanthes taeniata XChaetoceros wighamii XPorosira glacialis XDetonula confervacea X XThalassiosira levanderi X XThalassiosira sp. X X XChaetoceros, phaeoceros-group X XCoscinodiscus sp. X XRhizosolenia sp. XCoscinodiscus concinnus X

EuglenophytesEutreptiella sp. X

CiliatesMyrionecta rubra(=Mesodinium rubrum)

X X

DictyochophytesChatonella sp.(=Verrucophora farcimen)

X

1899–1901 data from Ostenfeld (1913), March 1931 from Cleve-Euler (1937) and theremaining data from the Danish National Monitoring Program.

Table 2Dominant species in August–October

1897–1901 1980s 1990s After 2000

DiatomsChaetoceros contortum XChaetoceros curvisetus XChaetoceros didymus XChaetoceros schüttii XEucambia zoodiacus XRhizosolenia calcar avis XProboscia alata (=Rhizosolenia alata) X XChaetoceros radians XRhizosolenia fragilissima X X XCerataulina pelagica X XGuinardia flaccida XNitzschia sp. XPseudo-nitzschia seriata-group X XPseudo-nitzschia delicatissima-group XRhizosolenia delicatula X

DinoflagellatesCeratium intermedium XCeratium macroceros XCeratium fusus X X X XCeratium tripos X X X XKarenia mikimotoi (=Gyrodinium aureolum) X XProrocentrum minimum X XCeratium furca X X XProrocentrum micans X X XCeratium lineatum X XGymnodinium chlorophorum X

CyanobacteriaGomphosphaeria sp.a X

1897–1901 data from Ostenfeld (1913) and the remaining data from the Danish nationalmonitoring program.

a Gomphosphaeria sp. was dominant at especially stations 444, 431 and 939.

Fig. 9. Temperature in surface water measured in conjunction with phytoplanktonsampling. Lightship data from Ostenfeld (1913).

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flaccida and C. pelagicawere registered as present but in low numbers inthe historical data while all among the dominant species in the moni-toring data.

4. Discussion

The Danish monitoring data revealed marked changes in the totalbiomass and composition of phytoplankton in the Kattegat, the BeltSea, the Sound and the western Baltic Sea since 1979. In the North Seaand the Baltic Sea recent studies have also shown changes in biomassand composition of phytoplankton and, in addition, changes inrecruitment of several species of fish (Reid et al., 1998; Wasmundand Uhlig, 2003; Beaugrand, 2004; Alheit et al., 2005). The mostdramatic changes occurred in the late 1980s and have generally beencoupled to changes in the NAO index from a period with negativewinter NAO values to consecutive years with positive NAO values. Thischange in the NAO will cause more pronounced westerly winds andmilder winters in northern Europe and the change has been reflectedin higher surface water temperatures in Danish waters (e.g. Carsten-sen, 2007a; Conley et al., 2007). Increases in water temperature havebeen most pronounced and significant during winter–spring andAugust–September (Fig. 9) where the largest decreases in phyto-plankton biomass were found.

Seasonal occurrences of the individual phytoplankton species canbe coupled to differences in temperature preferences (Karentz andSmayda, 1984; Edwards and Richardson, 2004). The water tempera-ture increase from the 1980s to the period after 1990 may thereforehave contributed to the observed changes in species composition.Thus, the cold water species Detonula confervaeae (Karentz andSmayda, 1984) formed characteristic spring blooms during the 1980swhile the biomass of this species was markedly lower during the early1990s and further reduced after themid 1990s. A similar decline in the

abundance of D. confervaceae during a period of increasing watertemperatures has been observed in Narragansett Bay from 1959 to1996 (Smayda et al., 2004).

Water temperature should, however, not be considered the onlydriving factor for changes in phytoplankton species composition.During the collection of plankton in 1897–1901 Ostenfeld (1913)recorded lower spring temperatures than those observed during themonitoring period 1979–2006, yet D. confervaceaewas not recorded inthe geographical area covered by the monitoring stations. Theplankton net tows employed by Ostenfeld (1913) are not directlycomparable to the quantitative samples collected during the monitor-ing. However, in February–March Ostenfeld registered D. confervaceaein the Limfjorden adjacent to the Kattegat and therefore it must be

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assumed that this species was not present or only present in very lownumbers in the Kattegat, the Belt Sea and the Sound during 1897–1901. Similarly, the occurrences of the warm water species C. pelagicacontradict that temperature alone controls what species dominate thephytoplankton community. The highest biomass measurements of C.pelagicawere found during the early and cold 1980s and subsequentlymuch lower biomass have been recorded.

In addition to direct effects on the growth of phytoplankton watertemperature will affect grazers of phytoplankton and thereby theenergy-flow through the pelagic ecosystem (Keller et al., 1999). Inmesocosm experiments using water from the Kiel Bight Aberle et al.(2007) showed increasing grazing rates of ciliates with increasingtemperatures during the spring bloom. The most pronounced changein water temperature during the Danish monitoring period was anincrease during winter–spring and late summer–autumn from the1980s till the period after 1990. Thus, the higher temperatures mayhave changed the grazing pressure on phytoplankton and affected thebiomass of the blooms. Unfortunately no data is available from themonitoring program to clarify this.

Nutrients are a prerequisite for the development of a highphytoplankton biomass. In the open Danish waters the growth ofphytoplankton is generally limited by the amount of available nitrogenduring the growth season (Carstensen, 2007b). Summer blooms ofphytoplankton in the Kattegat have been correlated with nitrogensupplies through wind-induced entrainment of nutrient rich bottomwater to the surface layer (Carstensen et al., 2004). The significantrelationship between inputs of nitrogen from land to the DanishStraits and phytoplankton biomass shows that the reduced nutrientloading to Danish waters has had a positive effect on the environ-mental conditions. The effect of reduced nutrient inputs on phyto-plankton biomass may, in areas susceptible to entrainment, have beenfurther enhanced by a general decline in wind speed since the 1980s(Conley et al., 2007).

The decrease in phytoplankton biomass at the Danish monitoringstations contradicts the trend of increased biomass and dominance bydinoflagellates during spring in the Baltic Sea since the late 1980s(Alheit et al., 2005). The observed trend in the Baltic Sea has beenexplained by a combination of the dependency of diatoms on watermixing and changed climatic conditions apparent through thechanges in the NAO. During cold winters the temperature of thesurfacewater drops below themaximum density temperature and thewater column stabilises. During spring heating of the surface water,convection and mixing down to the pycnocline is initiated resulting ina short spring bloom dominated by diatoms. Further heating of thewater will stabilise the water column and favour dinoflagellates. Incontrast, the surface water will not be cooled enough to reach thetemperature of maximum density in warmwinters. In these cases thewater column will stabilise from the first heating during spring andlead to dominance by dinoflagellates in the spring bloom (Wasmundet al., 1998). The monitoring stations in the Kattegat, the Belt Sea andthe Sound are all characterised by a pronounced halocline positionedmuch closer to the surface than the pycnocline in the Baltic Sea.Therefore the surface water can be mixed by wind without the needfor convection like in the Baltic Sea and an effect of warmwinters likethe one observed in the Baltic Sea can neither be expected nordetected in the monitoring data.

In the North-East Atlantic and the North Sea biogeochemicalchanges followed the change from a cold period during the 1960s–themid 1980s to a warm period after the mid 1980s (Beaugrand, 2004).Warm water species of copepods moved further north and aconspicuous change in the occurrence of phytoplankton took placein the late 1980s where the previous characteristic blooms duringspring and autumn expanded seasonally to cover the whole growthseason (Reid et al., 1998). These changes coincided with the changefromnegative to positive NAO index values and increased temperatureand salinity in the North Sea (Edwards et al., 2002). The increase in

salinity was caused by an unusual inflow of water from the Atlantic tothe North Sea which was repeated in 1998 (Holliday and Reid, 2001;Reid et al., 2001). The increase in phytoplankton biomass andcomposition following the inflow to the North Sea in the late 1980smay be attributed to a combination of higher concentrations ofnutrients and higher temperatures.

The unusual inflows of water from the Atlantic to the North Seamay have brought new phytoplankton species that through theSkagerrak could reach the Kattegat and the inner Danish waters. In1998 a bloom of the ichtyotoxic Chattonella sp. (=V. farcimen) coveredthe west coast of Jutland, the Skagerrak and the Kattegat. The origin ofthis species is unknown but subsequently it has occurred as part of orin connectionwith the spring bloom in the Kattegat almost every year.During the autumn–winter of 1999 a massive and unprecedentedbloom of the green dinoflagellate G. chlorophorum spread around theKattegat and Skagerrak. This species was previously recorded from theFrench Atlantic coast and the Channel and in 1990 the first bloom inthe North Sea was observed off Helgoland (Elbrächter and Schnepf,1996). It is possible that the spreading of G. chlorophorumwas coupledto changed climatic and hydrographical conditions leading to inflow ofoceanic water to the North Sea in 1989 and 1998.

The European Water Framework Directive requires that theecological status of all surface waters is at least “good” by 2012. Thismeans that the biological quality elements used for assessment showless than “moderate” deviations from undisturbed conditions. If this isnot the case actions to improve the ecological status are required. Aprerequisite for specifying such actions will be knowledge on thecoupling between anthropogenic pressures and the biologicalresponses of the marine ecosystem. For the biological quality elementphytoplankton the biomass, composition and bloom frequency shouldbe addressed in the assessment of ecological status. In Danish waterseutrophication is considered one of the main pressures on the marineecosystem and the monitoring data illustrate the coupling betweennutrient inputs and phytoplankton biomass. In addition, bloomfrequency in the Kattegat was shown to correlate with N inputs(Carstensen et al., 2004). In contrast the monitoring data onphytoplankton composition and long-term data on dominant speciesshow changes that are more complicated to correlate only withanthropogenic activities and therefore difficult to counteract throughaction plans. New species have been detected and at present ourknowledge on their origin and ecological preferences may beinsufficient to suggest measures that will restore previous conditions.Further and more sophisticated analyses are needed at severaltaxonomical levels (e.g. species/genus/class) before phytoplanktoncomposition can be related to specific anthropogenic disturbances.

5. Conclusions

The biomass of phytoplankton has decreased significantly since1979 in the Kattegat, the Belt Sea the Sound and the western BalticSea. The decrease correlated with reductions in N inputs to the DanishStraits but also with an increase in surface water temperature. It ispossible that higher grazing rates on the phytoplankton, induced byincreasing temperature, in combination with a general decrease inwind during the same period have enhanced the effects of the reducedN inputs. During the monitoring period 1979–2006, and in compar-ison with historical qualitative data, changes in the phytoplanktoncomposition were found that could not be explained by changingsurface water temperatures. Since the survey by Ostenfeld (1913) acentury ago several new species of phytoplankton have been recorded.Some of these species were present in the North Sea around 1900while others were not registered by Ostenfeld. Changing climateconditions and water inflows to the North Sea may have contributedto the spreading of new species of phytoplankton to Danish waters. Inrelation to the European Water Framework Directive the use ofphytoplankton composition for assessment of ecological status is

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made difficult by long-term changes in dominant species that are noteasily correlated only with anthropogenic activities and thereforedifficult to counteract through action plans. Furthermore our knowl-edge on the origin and ecological preferences of these species may beinsufficient to suggest measures that will restore previous conditions.

Acknowledgements

The constructive comments on an earlier version of themanuscriptby two anonymous reviewers and Hanneke Baretta-Bekker are grate-fully acknowledged.

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