Internal Ecosystem Feedbacks Enhance Nitrogen-fixing Cyanobacteria Blooms and Complicate Management in the Baltic Sea

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Internal Ecosystem Feedbacks Enhance Nitrogen-fixing Cyanobacteria Bloomsand Complicate Management in the Baltic SeaAuthor(s) Emil Vahtera Daniel J Conley Bo G Gustafsson Harri Kuosa Heikki Pitkaumlnen Oleg PSavchuk Timo Tamminen Markku Viitasalo Maren Voss Norbert Wasmund and Fredrik WulffSource AMBIO A Journal of the Human Environment 36(2)186-194 2007Published By Royal Swedish Academy of SciencesDOI httpdxdoiorg1015790044-7447(2007)36[186IEFENC]20CO2URL httpwwwbiooneorgdoifull1015790044-744728200729365B1863AIEFENC5D20CO3B2

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Emil Vahtera Daniel J Conley Bo G Gustafsson Harri Kuosa Heikki Pitkanen Oleg P SavchukTimo Tamminen Markku Viitasalo Maren Voss Norbert Wasmund and Fredrik Wulff

Internal Ecosystem Feedbacks EnhanceNitrogen-fixing Cyanobacteria Blooms andComplicate Management in the Baltic Sea

Eutrophication of the Baltic Sea has potentially increasedthe frequency and magnitude of cyanobacteria bloomsEutrophication leads to increased sedimentation of or-ganic material increasing the extent of anoxic bottomsand subsequently increasing the internal phosphorusloading In addition the hypoxic water volume displays anegative relationship with the total dissolved inorganicnitrogen pool suggesting greater overall nitrogen remov-al with increased hypoxia Enhanced internal loading ofphosphorus and the removal of dissolved inorganicnitrogen leads to lower nitrogen to phosphorus ratioswhich are one of the main factors promoting nitrogen-fixing cyanobacteria blooms Because cyanobacteriablooms in the open waters of the Baltic Sea seem to bestrongly regulated by internal processes the effects ofexternal nutrient reductions are scale-dependent Duringlonger time scales reductions in external phosphorusload may reduce cyanobacteria blooms however onshorter time scales the internal phosphorus loading cancounteract external phosphorus reductions The coupledprocesses inducing internal loading nitrogen removaland the prevalence of nitrogen-fixing cyanobacteria canqualitatively be described as a potentially self-sustaininglsquolsquovicious circlersquorsquo To effectively reduce cyanobacteriablooms and overall signs of eutrophication reductionsin both nitrogen and phosphorus external loads appearessential

INTRODUCTION

Cyanobacteria capable of biological fixation of dissolvedatmospheric dinitrogen gas (N2 fixation) form extensive bloomswhich have been a recurring phenomenon in the Baltic Sea sinceat least the 1960s (1) They are noxious and relevant to theecosystem and to society because of the formation of aconspicuous surface scum toxicity and large nitrogen inputsthrough N2 fixation Traditionally phosphorus alone has beenconsidered as the limiting nutrient for N2-fixing cyanobacteriaIn this article we present how elemental cycles of nitrogen andoxygen are interlinked with the phosphorus cycle in basin-wideand long-term processes To manage cyanobacteria blooms wemust resolve the relative importance of nutrient supply andinternal biogeochemical processes

Most of the nutrient load to the Baltic Sea arrives at the coastbut the most striking cyanobacteria blooms appear in offshorepelagic regions of the basin It is apparent that the actionscontrolling external nutrient loads except those concerningatmospheric load can directly affect coastal ecosystems in sourceregionsThe external loadsmaybe filtered by the coastal zone andpropagated offshore The Baltic Sea with long residence timesand strong internal nutrient recycling thus poses a challenge forecosystem research and the management of nutrient inputs Inthis article we summarize the prevailing knowledge on thecontrolling mechanisms of Baltic Sea cyanobacteria blooms and

highlight the gaps in the present knowledge for the long-termrestoration of this eutrophied ecosystem

BALTIC SEA CYANOBACTERIA

The dominant species of cyanobacteria in the open Baltic Seaare the heterocyte (2)-possessing N2-fixing filamentous speciesbelonging to the order Nostocales Nodularia spumigenaMertens (hepatotoxic) Aphanizomenon flos-aquae (L) Ralfs(presently regarded as nontoxic) (3 4) and Anabaena spp(potentially neurotoxic) (5) Along with the heterocyte-possess-ing filamentous species either filamentous or coccoid colony-forming species without heterocytes (not capable of N2 fixation)frequently occur The small coccoid species may also dominatepelagic cyanobacteria biomass (6 7) Filamentous specieswithout heterocytes or the colonial species which include toxicspecies like Microcystis are abundant in eutrophied coastalareas They can form extensive surface-accumulating bloomsbut it is the N2-fixing filamentous species that generally producethe conspicuous property of the large-scale pelagic bloomsPigments from sediment cores indicate that cyanobacteria havebeen present in the brackish Baltic Sea for 7000ndash8000 years (89) but anthropogenic nutrient loading may have intensifiedtheir blooms (1 10)

The extent intensity and species composition of cyanobac-teria blooms show temporal variation on interannual and intra-annual scales and spatial variation ranging from the scale ofLangmuir circulation to Baltic Seandashwide horizontal inhomoge-neities with distinct vertical distribution patterns within theeuphotic zone (11ndash16) Geographically the blooms are mainlyconfined to the Baltic Proper the Gulf of Finland and the Gulfof Riga with occasional blooms in the Bothnian Sea and theBelt Seas (11 12) This distribution pattern may be caused bythe low nitrogen to phosphorus (N P) ratios (17) andor themesohaline conditions (6 18) prevailing in the central andeastern Baltic Sea Satellite imagery shows that blooms cancover areas larger than 60000 km2 (11) which is approximately16 of the entire Baltic Sea surface area

The N2-fixing cyanobacteria start to grow primarily in Juneafter the exhaustion of dissolved inorganic nitrogen (DIN) andreach bloom concentrations in July or early August (19)Upwelling water rich in dissolved inorganic phosphate (DIP)may also initiate local blooms (20 21) Variations in theintensity and occurrence of blooms are dependent uponwintertime nutrient conditions (22 23) surface layer salinitytemperature and solar irradiation (18) summer stratificationconditions (21) upwelling (20) and frontal processes (21 24)

Nutrient limitation characteristics of the different cyanobac-teria diverge because of the N2-fixation capability of theheterocyte-possessing filamentous species The N2-fixing speciesare most likely limited by phosphorus availability (25 26) andgrowth may be inhibited by sulfate that impedes N2 fixation (6)The nonndashN2-fixing species are primarily limited by nitrogenavailability with phosphorus and iron as potential secondarylimiting factors (6 26) However as the dominant N2-fixing

186 Ambio Vol 36 No 2ndash3 April 2007 Royal Swedish Academy of Sciences 2007httpwwwambiokvase

species differ in their limitation patterns and stoichiometry thespecies composition and spatial and temporal occurrence ofblooms are affected by nutrient availability (27 28) Meteoro-logical conditions also shape the spatial occurrence of blooms(29) Sedimentary and grazing losses of filamentous species aregenerally small and most of the biomass is decomposed in thesurface layer (30ndash32) Blooms are terminated by several factorsincluding nutrient limitation mixing events decreased solarirradiation decreasing water temperature and possibly virallysis (18 33)

The amount of N2-fixing cyanobacteria increased from 1968to 1981 (34) and the increase in late-summer chlorophyll aconcentrations in the 1990s (35) may be related to increases in theabundance of cyanobacteria The N2-fixation capability of someof the cyanobacteria causes large additional nitrogen inputs tothe Baltic Sea during summer N2-fixation estimates span a widerange reflecting the patchy nature and interannual variability ofthe blooms as well as partly methodological difficulties Recentestimates suggest that cyanobacteria N2 fixation can introduce180 000ndash430 000 tonnes (19 36) of new nitrogen annually (valuesas high as 790 000 tonnes have been suggested [19]) supportingnew production during nitrogen-limited periods N2 fixation hassupported new production to a variable extent and has beenestimated to supply the phytoplankton community with enoughnitrogen to account for 27 of total nitrogen uptake duringsummer bloom conditions (37) In other studies 5ndash10 of totalfixed nitrogen was found in the picoplanktonic size fractionduring a bloom (38) and uptake was observed to be dominatedby regenerated forms of nitrogen (37 39) However more recentestimates show that N2 fixation can supply up to 50ndash90 of totalnitrogen demand (7 27) and can account for 18ndash23 of netprimary production during a 108-day period of new productionfrom 28 March to 13 July 2001 (40) and for 30ndash90 of netcommunity production from June to August (36) Also it isestimated that up to 45 of mesozooplankton nitrogen demandis contributed by nitrogen fixation through trophic vectors (41)Thus N2 fixation appears to have an important role insupporting production in nitrogen-deficient areas

Phosphorus availability is the most important factor settingthe maximum limits on the magnitude of cyanobacteria bloomsThe biomass of N2-fixing cyanobacteria is correlated with thewintertime phosphorus pools and the excess amount ofphosphorus remaining after the spring bloom which is basedon the assumption of a balanced Redfield-ratio uptake ofnutrients during the spring bloom (Excess DIPfrac14DIPndashDIN16in molar units) (22 23) Nevertheless the correlation is notubiquitous (19) and considerable temporal and spatial variationoccurs between years and in different basins of the Baltic Sea

Thus resolving how the coupled large-scale biogeochemicalcycles of nitrogen and phosphorus regulate cyanobacteriablooms is of great relevance Therefore we explored the poolsizes of nitrogen and phosphorus the regulation of these poolsand the balance of nitrogen and phosphorus supply to theproductive uppermixed layer on the scale of the entire Baltic Sea

NITROGEN AND PHOSPHORUS MASS BALANCES

Data and Methods

To examine the variation of water-column pools of nitrogen weapplied a basin-wide approach as previously done for phos-phorus (42) Nitrogen pools were summed up for threesubbasins where N2 fixation occurs the Baltic Proper and theGulfs of Finland and Riga Annually averaged pools of totalnitrogen (TN) and DIN as well as volumes of water confined bythe oxygen isosurfaces of 0 and 1 mL O2 L1 were computedwith the Data Assimilation System (43) on three-dimensional

fields reconstructed from observations found in the BalticEnvironment Database (BED) (Stockholm University Depart-ment of Systems Ecology Marine Ecosystems Modeling Grouphttpdataecologysusemodelsbedhtm) which includes avast amount of data from monitoring programs and scientificcruises in the region The time series of combined nitrogen inputto the Baltic Proper from land and atmospheric sources wascompiled from several sources including (44) unpublished datain BED the periodic load compilations by the HelsinkiCommission (eg 45) (46) and published and unpublisheddata from the Cooperative Programme for Monitoring andEvaluation of the Long-range Transmission of Air Pollutants inEurope (eg 47)

Results

The pool of phosphorus in the water column shows largevariation between years the variation being up to three timesthe size of the average annual allochthonous load (42) Thewinter-to-winter changes in the basin-wide DIP pool in theBaltic Proper are correlated to the changes in bottom areacovered by hypoxic water but not to changes in totalphosphorus load (42) Thus regarding the phosphorus avail-ability of N2-fixing cyanobacteria internal processes ie thesediment release of phosphorus into deep-water layers and theconveyance of this phosphorus pool to the upper mixed layerare the key factors The deep-water phosphate concentrations inthe Gulf of Finland and Baltic Proper have increasing trendsduring stagnation periods with low oxygen concentrations indeep waters (48 49) this is also mirrored in the winter mixedsurface layer concentrations (48 50)

Because N2-fixing cyanobacteria are dependent on theavailability of phosphorus and generally gain competitiveadvantage from low DIN DIP ratios (eg 17) the regulationof the nitrogen pool is also of importance next we examinefactors regulating the total DIN pool of the Baltic Sea

The long-term annual (mean 6 SD) load is 752000 6 98000tonnes nitrogen for the 33-year period examined during whichno clear and definite long-term trends were observed (Fig 1)Fluctuations can be explained by climatic variations particu-larly in freshwater runoff For the TN pool there is a long-termincreasing trend until the mid-1980s but there were severalproblems with analytical methods used in many of thelaboratories in the early 1970s so data from this period shouldbe taken with caution

The average year-to-year variation in nitrogen load is ca72 000 tonnes whereas the corresponding variation in the TNpool in the Gulfs of Finland and Riga and the Baltic Propercombined is about 225 000 tonnes No clear correlation betweenloads and either the pool itself or its year-to-year changes wereobserved The annual net exchange of TN between the BalticProper and adjacent basins is about 120 000 tonnes (51 52) andvaries between years by less than 30 000 tonnes Subsequentlyexchange processes cannot explain the variations in the TN poolHowever there is a significant negative relationship between theDIN pool and hypoxic water volume (Fig 2) The relationshipsuggests that losses of the DIN pool through nitrogen removalprocesses may be higher during periods of hypoxia The relativerole of nitrogen removal processes in the pelagic water column isunknown Denitrification has been observed at the interface ofanoxic and oxic waters in the stratified Baltic Proper (53 54) butthe importance of the process cannot be determined from thesemeasurements The loss of nitrogen through the anammoxprocess has been observed to occur in the oxygen-poor andammonia-rich environment of the eastern Gotland Basin andcould potentially be responsible for some nitrogen losses on aBaltic Sea scale as well

Ambio Vol 36 No 2ndash3 April 2007 187 Royal Swedish Academy of Sciences 2007httpwwwambiokvase

By simply relating the amount of nitrogen load to the studyarea surface layer volume we should see an increase in nitrogenconcentrations due to the external load If we assume that the752 000 tonnes of total nitrogen transported annually by riversand deposited from the atmosphere would be instantaneouslymixed into the 14 500 km3 of the surface layer (0ndash60 m) in theBaltic Proper the Gulf of Finland and the Gulf of Riga and thatthere would be no net exchange of nitrogen between the studyarea and the neighboring basins an annual increase of about 37lM nitrogen would be observed The amount would be evenlarger with N2 fixation added This hypothetical increase innitrogen concentration in surface waters has not been observed inlong-term observations (55) therefore a considerable sink ofnitrogen is postulated by models (56 57) and has been confirmedby empirical budgets (51 52) and direct measurements (53 58)

Denitrification in sandy coastal sediments has been suggest-ed as one of the major sinks for nitrogen entering the Baltic Sea(55) A loss of all river DIN discharging into the Baltic Properand the Gulfs of Finland and Riga (344 000 t y1) over thecoastal area of these basins shallower than 30 m (80 000 km2)would result in a loss of 084 mmol N m2 d1 roughlymatching denitrification rates as reported from deep bottomsediments of the Gulf of Finland (58) During the productiveseason autotrophic nitrate uptake and sedimentation ofparticulate organic nitrogen taking place in the coastal zoneexplains the low nitrate concentrations found already atrelatively short distances (tens of kilometers) from the coast(59 60) Coastal areas of the Baltic Sea shallower than 30 mreceive high nitrogen loads that are rapidly turned over duringthe productive season (60) In the northern parts of the BalticSea the terrestrial loads are however conveyed almost intacttoward the offshore system during winter months

Thus similar to phosphorus internal processes N2 fixationdenitrification anammox sedimentation and trophic transfercontrol the annual variations of nitrogen concentrations in theopen sea to a greater extent than external loads The net effectof these processes and the magnitudes of N2 fixation and N2

production counteracting each other cannot be estimated frommass balance calculations without direct measurements of theseprocesses

Nevertheless load reductions might have more pronouncedeffects on smaller spatial scales in subbasins The separatesubbasins have their own characteristic internal dynamics in theirnitrogen budgets For example in the Gulf of Finland a 35reduction of external nitrogen load from the late 1980s to the late1990s was observed (60) During the same period wintertimeDIN concentrations in the Gulf decreased by 20ndash30 (62)

Simultaneous decreases in external nitrogen load andwinterDINappear to have taken place also in the Gulf of Riga (63) Possiblereasons for this discrepancy between the Baltic Proper and theGulfs of Finland and Riga can be different ratios of load versusmean annual nitrogen content of a basin which were 1 26 forthe Gulf of Finland 1 19 for the Gulf of Riga and 1 52 for theBaltic Proper (52) Thus the shorter residence time of water andnitrogen in the Gulfs of Finland and Riga probably enable thedecreased loads to affect the basin-wide nitrogen dynamics morerapidly than in the Baltic Proper Furthermore denitrification ispossibly favored in the gulfs because of the relatively largeproportion of bottom sediments at depths of 30ndash60 m ie abovethe permanent halocline ensuring the availability of nitrate in thedenitrification process in the sediments

HYDROGRAPHIC AND BIOGEOCHEMICALCONTROLS OF CYANOBACTERIA BLOOMS

Data and Methods

We analyzed the annual development of nitrogen and phos-phorus pools and how they are related to hydrography andbiogeochemistry The data were acquired mainly from theSwedish Meteorological and Hydrological Institute but alsofrom monitoring data from other nations Data from the stationBY15 in the central Eastern Gotland basin for 1994ndash2005 wereused for analysis of the annual development of nutrientconcentrations The number of vertical profiles used rangesfrom 139 to 170 depending on the parameter The verticalaverage concentrations in Figure 3 are computed by firstinterpolating the measurements vertically to a 1-m resolutionthey are then integrated using the hypsographic function for theBaltic Proper excluding the Gulf of Finland the Gulf of Rigaand the Bornholm basin The monthly averages for specificdepth intervals presented in Figure 4 are based on 8ndash20 profilesper month with the highest measurement frequency being inAugust and the lowest in November and December Data forFigure 5 were acquired from BED

Results

The onset of the spring bloom is controlled by average lightconditions and stratification in the surface layer (64) At thetermination of the spring bloom most of the DIN and much ofthe DIP is consumed in the Baltic Proper on average down tothe permanent halocline (60 m) (Fig 3cd) In recent years thespring bloom is terminated because of the lack of available

Figure 1 Long-term variations of the annually averaged TN pool inthe Baltic Proper the Gulf of Finland and the Gulf of Riga andexternal annual nitrogen inputs (t TN y1) to the area

Figure 2 Relationship between total amounts of DIN in the BalticProper the Gulf of Finland and the Gulf of Riga and hypoxic watervolume confined by isosurfaces of 0 and 1 mL O2 L1 in the samebasins


DIN with excess DIP remaining in the surface layer HoweverDIP concentrations continue to decrease during the summer Inmost years DIP concentrations reach levels that limit phyto-plankton growth with some DIP available below the summerthermocline (15ndash20 m) (Fig 3d) After the spring bloomroughly 50 of the consumed inorganic nutrients remain in thesurface layer but in organic forms (Fig 3ef)

Significant increases in pelagic inorganic nutrient concentra-tions above the halocline occur again in October (Fig 3cd)From the average time series in the Baltic Proper about half ofthe winter surface pool is built up from the regeneration ofnutrients the nutrient load and possibly vertical diffusionbetween October and December whereas the remaining halfcomes with vertical mixing in January and February

A closer look at the integrated amount of nutrients in theupper 60 m reveals that on average DIP concentrationsincrease from 025 lM to 035 lM from September toDecember whereas total phosphorus (TP) remains constant(Fig 4) This means that remineralized phosphorus builds up asa bioavailable DIP pool instead of being used or lost through

burial or other processes An increase of ca 015 lM in bothDIP and TP concentrations occurs from December to Januarywith an additional increase of ca 010 lM reaching 060 lM inMarch (Fig 4) Dissolved inorganic nitrogen and TN follow thesame pattern an increase in DIN from about 1 lM inSeptember to 25 lM in December occurs with an insignificantchange in TN This change is followed by an increase of ca 2lM in both DIN and TN concentrations during the wintermonths (Fig 4)

Averaged over the same water volume the nutrient loads tothe Baltic Proper correspond to approximately 025 lM mo1

(or 3 lM y1) nitrogen (365000 t y1) and 0005 lM month1

(006 lM y1) phosphorus (18300 t y1) Contrasting to that ofnitrogen the monthly load of TP is small relative to pool sizeand therefore does not cause detectable changes in concentra-tion on seasonal time scales

Neglecting loads and horizontal advection we estimate thatabout 40 of the winter DIP pool above 60 m comes fromregeneration in the upper water column and 60 from mixingadvection from below Roughly the same figures apply for DIN

Figure 3 Annual cycles of (a)salinity (PSU) (b) temperature(8C) (c) nitrate (lM) (d) phosphate(lM) (e) organic nitrogen (lM) and(f) organic phosphorus (lM) at acentral Baltic Sea monitoring sta-tion (BY15 eastern Gotland basin)Estimates for organic nutrientswere acquired by subtracting thedissolved inorganic fraction fromtotal nutrients Average values for1994ndash2004


but here atmospheric loads should be taken into accountAtmospheric deposition of nitrogen is about 2 g m2 y1 (eg47) or 25 lM y1 in a 60-m column Thus for the period fromOctober to March the atmospheric contribution should beabout 12 lM or 35 of the total increase

The increase in TN in the upper 20-m layer in July (Fig 4) isindicative of nitrogen fixation The fixed nitrogen is efficientlyremoved from the system as shown by the decreasing TNconcentrations beginning in August (Fig 4) Water columnincreases of DIN are observed by November TN and DINconcentrations have a rather similar annual pattern at deeperdepths in contrast to the upper 20-m layer which wouldindicate a loss of the fixed nitrogen in the upper (0ndash20 m) watercolumn Therefore fixed nitrogen seems to be removed by someprocess (potentially denitrification or anammox at intermediatedepths) from the offshore system before the winter periodRapid settling of particulate material can also remove fixednitrogen from the water column Baltic Sea deep waters (180m) have a depleted d15N-signal indicative of nitrogen fixation(65) and nitrogen has a greater sedimentary loss than carbon orphosphorus (66) However the relative contribution of settlinglosses of nitrogen introduced to the system by N2 fixation ispoorly known

The year-to-year variations in surface layer DIN and DIPare sensitive to hydrographic conditions because a largeproportion of the winter pools of both surface water DIN andDIP comes from vertical mixing and advection from below thehalocline as shown above In periods when the halocline isweak and well ventilated oxygen conditions are improved

resulting in lower DIP and higher DIN concentrations

especially nitrate in deep waters The opposite occurs when

the halocline is strong and hypoxiaanoxia reaches higher into

the water column DIP concentrations tend to be high whereas

nitrate concentrations are lower (Fig 5)

REGULATION OF PELAGIC COASTAL AND LOCAL

CYANOBACTERIA BLOOMS

The excess phosphorus that is regulated by internal processes

governs the offshore pelagic cyanobacteria blooms This

phosphorus is channeled to the cyanobacteria through uptake

of DIP to cellular stores (27 36) and through recycling

processes within the planktonic food web (27 67) whereas

coastal and local blooms might mainly be regulated by different

factors

Coastal blooms are either laterally advected from the open

sea or they can develop in situ The in situ formation is often

preceded by additional inputs of phosphorus to the surface

layer by upwelling and followed by calm conditions The

response time-scale in biomass is measured in weeks because of

the slow growth of filamentous cyanobacteria Coastal blooms

generated by upwellings are dominated by Aphanizomenon in

the Gulf of Finland (20 29) However several cyanobacteria

species can co-occur in coastal blooms and niche separation for

the N2-fixing Aphanizomenon and Nodularia suggested by

Niemisto et al (15) reflects their different nutritional and

physiological properties (21 27 28 36)

Figure 4 Monthly averages of vertical means for the years 1994ndash2004 of observations from a central Baltic Sea monitoring station (BY15eastern Gotland basin) in different depth intervals The vertical means are computed using the hypsographic function for the Baltic Properexcluding the Gulfs of Finland and Riga and Bornholm and Arkona basins


Local blooms are more variable in space and time than theoffshore or coastal blooms Occasional large blooms may occurin sheltered basins in archipelagos often affected by local land-based nutrient inputs with a more variable species compositionthan offshore or coastal blooms Blooms often include Micro-

cystis Planktothrix Oscillatoria and Pseudanabaena species (1and references therein) which are nonndashN2-fixing species andconsequently compete for DIN with other phytoplankton taxaThe main triggering factor for these blooms may be exception-ally strong stratification and warm water as well as selectivegrazing favoring cyanobacteria

A VICIOUS CIRCLE

The Baltic Sea basins where the conspicuous cyanobacteriablooms occur have been generally nitrogen-limited through-out the growth season (68ndash71) which gives cyanobacteria acompetitive advantage during summer months but also affectsthe seasonal dynamics of planktonic production and sedimen-tation The loading of nitrogen directly enhances productionduring the spring bloom which is quantitatively the mostimportant production period annually both in the offshoreBaltic Proper (40) and even more so in coastal regions (30 6672) A large part of this nitrogen-fueled production is lostfrom the upper mixed layer through sedimentation and itcomprises the major sedimentation event on a seasonal scale(30 72 73)

When decomposed in bottom waters of the stratified BalticSea sedimenting biomass consumes near-bottom water oxygenPhosphate is released from the sediments during hypoxic andanoxic conditions External nitrogen loading thus appears toboost internal phosphorus loading through these seasonalfeedbacks Recent studies suggest that repeated hypoxic eventslead to an increase in further hypoxia (74) creating a regimeshift in benthic communities and changes in organic matterprocessing (75) This feedback creates a persistent internalloading of phosphate even if external nutrient loads arereduced When phosphate that is released from sedimentsreaches the surface waters because of annual turnovers orsummertime upwellings the occurrences of cyanobacteriablooms are potentially increased Major saltwater inflows havealso been noted to stimulate cyanobacteria blooms by lifting upphosphate-rich deep waters (76) Increased blooms of N2-fixingcyanobacteria again incur further anoxia through increased

Figure 6 A schematic presentationof main feedback processes thatinhibit recovery from eutrophica-tion and favor cyanobacteriablooms in the Baltic Sea Thevicious circle is potentially sus-tained by nitrogen(N)-limited pro-duction and sedimentation ofphytoplankton especially duringthe spring bloom and subsequentoxygen depletion in bottom wa-ters causing internal loading ofphosphorus (P) Physical transportof released phosphorus to surfacelayers would enhance N2 fixationby diazotrophic cyanobacteriaThese seasonal feedbacks be-tween biogeochemical cycles ofnitrogen phosphorus and oxygencan effectively counteract reduc-tions in the external phosphorusloading to the system if nitrogenloading is not reduced as wellGrey arrows depict material flowsThin arrows depict causal relation-ships and successive eventsSeveral potential feedback mecha-nisms and limiting factors areomitted for clarity For detailssee text

Figure 5 Vertical distribution of nitrate and nitrite and phosphateconcentrations from the central Baltic Sea (monitoring station BY15eastern Gotland basin) in relation to oxygen conditions (blackcontours 0ndash2 mL O2 L1) Values are 90-day averages


nitrogen input to the generally nitrogen-limited summer-timepelagic ecosystem

In addition to affecting sediment release of phosphorus thehypoxic water volume has a negative relationship with the totalDIN pool of the Baltic Sea Therefore the same conditions thatincrease internal loading of phosphorus tend to increasenitrogen removal further facilitating the occurrence of N2-fixing cyanobacteria by lowering the DIN DIP ratio Theincreased nitrogen removal with increasing hypoxia might berelated to the increasing area of the oxic and anoxic interfacearea where denitrification is possible and nitrate supply is notlimiting the process

These connections accentuate the internal regulation of thepresent eutrophied state of the Baltic Sea which might bequalitatively described as a vicious circle (71) The vicious circle(Fig 6) depicts the relationships between the nitrogenphosphorus and oxygen cycles and how the feedbacks betweenthese elements may work It is forced and controlled by bothexternal and internal nutrient loading and physical forcing Thepotentially self-sustaining vicious circle can effectively counter-act reductions in the external phosphorus loading to the systemas is evidenced in the Gulf of Finland (61) Because of thesefeedbacks the Baltic Sea seems to be in a state of inhibitedrecovery regarding eutrophication

The nitrogen inputs through N2 fixation and other sourcesare approximately balanced by the losses (denitrificationincluding anammox and permanent burial) This is suggestedby the relatively constant winter DIN concentrations But onlya few measurements on DIN loss rates have been made in thepelagic Baltic Proper (54ndash56 79ndash81) and the regulation of theloss rates by either organic matter supply (53) or reduced sulfurcompounds (77) is unknown How the feedback between inputand removal of DIN works in detail is an important subject forfuture work

Phosphorus losses are coupled with the state of anoxia in thebasin By moderating the area of reducing sediments and thevolume of anoxic water DIP concentrations will decline Sincethe magnitude of the DIN-limited spring bloom affects theamount of sedimenting organic material to a large extentannually the external load of both nitrogen and phosphoruswill have to be reduced to curb anoxia and the amount of N2-fixing cyanobacteria

CONCLUSIONS

The size of the total nitrogen pool in the Baltic Sea is governedby internal processes (N2 fixation denitrification anammoxtrophic transfer permanent burial resuspension) to a largerextent than by external loading as evidenced by the consider-able amplitude of the annual variation in the TN pool inrelation to average annual loads Hypoxic water volume showsa negative relationship with the DIN pool however the relativeimportance of each individual process governing the nitrogenpool size remains to be resolved

Wintertime DIN and DIP pools are largely governed byhydrography in the offshore system Approximately 40 of theannual replenishment of DIP in the surface layer stems fromremineralization of organic phosphorus originating from theprevious growth season and 60 from deep water by mixingevents For DIN the internal sources have a similar relationwhereas an additional input from atmospheric sources duringOctober to March constitutes 35 of the wintertime totalincrease The nitrogen input caused by biological N2 fixation isremoved by internal processes either by burial trophictransfers denitrification or anammox

Both phosphorus and nitrogen transformations includingphysicochemical and biological reactions which are mediated

by microbial activity are indirectly connected to oxygenconditions controlled by organic matter sedimentation andhydrography The pelagic nutrient budgets for both nitrogenand phosphorus are largely unaffected by short-term changes inexternal loads as shown by much larger variations ininterannual changes in total nutrients relative to estimates ofexternal loads Thus offshore cyanobacteria blooms arestrongly regulated by internal processes External nutrient loadsmore directly affect the coastal and local blooms The rim ofsouthern sandy coastal sediments seems to remove much of theexternal nitrogen loads through denitrification This can affectthe outcome of load reduction responses and thus possiblyshape the species composition of bloom communities on anonshorendashoffshore gradient

Because of the interconnected cycles of oxygen phosphorusand nitrogen the Baltic Sea is in a state of inhibited recoveryregarding eutrophication Ongoing eutrophication induces widespread hypoxia and large permanently reducing bottom areasmainly through sedimentation of the intense nitrogen-limitedspring bloom thus facilitating internal phosphorus loadingThis state of the system promotes the occurrence of N2-fixingcyanobacteria and tends to counteract the effects of externalphosphorus load reductions on shorter time scales To alleviatethe adverse effects of eutrophication in the Baltic Sea nitrogenand phosphorus emissions should be reduced

References and Notes

1 Finni T Kononen K Olsonen R and Wallstrom K 2001 The history ofcyanobacterial blooms in the Baltic Sea Ambio 30 172ndash178

2 We use the term heterocyte for the specialized cells of the filamentous cyanobacteriawhere nitrogen fixation occurs instead of the also widely used heterocyst The latter termimplies that the cells are cysts which they are not

3 Sivonen K 1996 Cyanobacterial toxins and toxin production Phycologia 35 12ndash244 Laamanen MJ Forsstrom L and Sivonen K 2002 Diversity of Aphanizomenon flos-

aquae (Cyanobacterium) populations along a Baltic Sea salinity gradient Appl EnvironMicrobiol 68 5296ndash5303

5 Karlsson KM Kankaanpaa H Huttunen M and Meriluoto J 2005 Firstobservation of microcystin-LR in pelagic cyanobacterial blooms in the northern BalticSea Harmful Algae 4 163ndash166

6 Stal LJ Staal M and Villbrandt M 1999 Nutrient control of cyanobacterial bloomsin the Baltic Sea Aquat Microb Ecol 18 165ndash173

7 Stal LJ Albertano P Bergman B von Brockel K Gallon JR Hayes PKSivonen K and Walsby AE 2003 BASIC Baltic Sea cyanobacteria An investigationof the structure and dynamics of water blooms of cyanobacteria in the Baltic Seamdashresponses to a changing environment Continental Shelf Research 23 1695ndash1714

8 Poutanen E-L and Nikkila K 2001 Carotenoid pigments as tracers of cyanobacterialblooms in recent and post-glacial sediments of the Baltic Sea Ambio 30 179ndash183

9 Bianchi TS Engelhaupt E Westman P Andren T Rolff C and Elmgren R 2000Cyanobacterial blooms in the Baltic Sea natural or human-induced Limnol Oceanogr45 716ndash726

10 Westman P Borgendahl J Bianchi TS and Chen N 2003 Probable causes forcyanobacterial expansion in the Baltic Sea role of anoxia and phosphorus retentionEstuaries 26 680ndash689

11 Kahru M Horstmann U and Rud O 1994 Satellite detection of increasedcyanobacteria blooms in the Baltic Sea natural fluctuation or ecosystem changeAmbio 23 469ndash472

12 Kahru M Leppanen J-M Rud O and Savchuk OP 2000 Cyanobacteria blooms inthe Gulf of Finland triggered by saltwater inflow into the Baltic Sea Mar Ecol ProgSer 207 13ndash18

13 Kononen K and Leppanen J-M 1997 Patchiness scales and controlling mechanismsof cyanobacterial blooms in the Baltic Sea application of a multiscale research strategyIn Monitoring Algal Blooms New Techniques for Detecting Large-scale EnvironmentalChange Kahru M and Brown CW (eds) Landes Bioscience Austin p 63ndash84

14 Kononen K and Nommann S 1992 Spatio-temporal dynamics of the cyanobacterialblooms in the Gulf of Finland Baltic Sea In Marine Pelagic CyanobacteriaTrichodesmium and Other Diazotrophs Carpenter EJ Capone DG and RueterJG (eds) Kluwer Acaemic Publishers-NATO ASI Dordrecht p 95ndash113

15 Niemisto L Rinne I Melvasalo T and Niemi A 1989 Blue-green algae and theirnitrogen fixation in the Baltic Sea in 1980 1982 and 1984 Meri 17 3ndash59

16 Kononen K Hallfors S Kokkonen M Kuosa H Laanemets J Pavelson J andAutio R 1998 Development of a subsurface chlorophyll maximum at the entrance tothe Gulf of Finland Baltic Sea Limnol Oceanogr 43 1089ndash1106

17 Niemi A 1979 Blue-green algal blooms and NP ratio in the Baltic Sea Acta Bot Fenn110 57ndash61

18 Wasmund N 1997 Occurrence of cyanobacterial blooms in the Baltic Sea in relation toenvironmental conditions Int Revue ges Hydrobiol 82 169ndash184

19 Wasmund N Nausch G Scneider B Nagel K and Voss M 2005 Comparison ofnitrogen fixation rates determined with different methods a study in the Baltic ProperMar Ecol Prog Ser 297 23ndash31

20 Vahtera E Laanemets J Pavelson J Huttunen M and Kononen K 2005 Effect ofupwelling on the pelagic environment and bloom-forming cyanobacteria in the westernGulf of Finland Baltic Sea J Mar Sys 58 67ndash82

21 Kononen K Kuparinen J Makela K Laanemets J Pavelson J and N~ommann S1996 Initiation of cyanobacterial blooms in a frontal region at the entrance to the Gulfof Finland Baltic Sea Limnol Oceanogr 41 98ndash112

22 Jansen F Neumann T and Schmidt M 2004 Inter-annual variability incyanobacteria blooms in the Baltic Sea controlled by wintertime hydrographicconditions Mar Ecol Prog Ser 275 59ndash68


23 Laanemets J Lilover M-J Raudsepp U Autio R Vahtera E Lips I and Lips U2006 A fuzzy logic model to describe the cyanobacteria Nodularia spumigena blooms inthe Gulf of Finland Baltic Sea Hydrobiologia 554 31ndash45

24 Moisander PH Rantajarvi E Huttunen M and Kononen K 1997 Phytoplanktoncommunity in relation to salinity fronts at the entrance to the Gulf of Finland BalticSea Ophelia 463 187ndash203

25 Rydin E Hyenstrand P Gunnerhed M and Blomqvist P 2002 Nutrient limitationof cyanobacterial blooms an enclosure experiment from the coastal zone of the NWBaltic proper Mar Ecol Prog Ser 239 31ndash36

26 Moisander PH Steppe TF Hall NS Kuparinen J and Paerl HW 2003Variability in nitrogen and phosphorus limitation for Baltic Sea phytoplankton duringnitrogen-fixing cyanobacterial blooms Mar Ecol Prog Ser 262 81ndash95

27 Kangro K Olli K Tamminen T and Lignell R 2007 Species-specific responses of acyanobacteria-dominated phytoplankton community to artificial nutrient limitation aBaltic Sea coastal mesocosm study Mar Ecol Prog Ser (In press)

28 Vahtera E Laamanen M and Rintala J-M Submitted manuscript Use of differentphosphorus sources by the bloom-forming cyanobacteria Aphanizomenon flos-aquae andNodularia spumigena Aquat Microb Ecol (In Press)

29 Kanoshina I Lips U and Leppanen J-M 2003 The influence of weather conditions(temperature and wind) on cyanobacterial bloom development in the Gulf of Finland(Baltic Sea) Harmful Algae 2 29ndash41

30 Heiskanen A-S and Kononen K 1994 Sedimentation of vernal and late summerphytoplankton communities in the coastal Baltic Sea Arch Hydrobiol 13 175ndash198

31 Sellner KG Olson MM and Kononen K 1994 Copepod grazing in a summercyanobacteria bloom in the Gulf of Finland Hydrobiologia 292293 249ndash254

32 Engstrom J Viherluoto M and Viitasalo M 2001 Effects of toxic and non-toxiccyanobacteria on grazing zooplanktivory and survival of the mysid shrimp Mysis mixtaJ Exp Mar Biol Ecol 257 269ndash280

33 Simis SGH Tijdens M Hoogveld HL and Gons HJ 2005 Optical changesassociated with cyanobacterial bloom termination by viral lysis J Plankton Res 27937ndash949

34 Kononen K and Niemi A 1984 Long-term variation of the phytoplanktoncomposition at the entrance to the Gulf of Finland Ophelia 3 101ndash110

35 Raateoja M Seppala J Kuosa H and Myrberg K 2005 Recent changes in trophicstate of the Baltic Sea along SW coast of Finland Ambio 34 188ndash191

36 Larsson U Hajdu S Walve J and Elmgren R 2001 Baltic Sea nitrogen fixationestimated from the summer increase in upper mixed layer total nitrogen LimnolOceanogr 46 811ndash820

37 Sorensson F and Sahlsten E 1987 Nitrogen dynamics of a cyanobacteria bloom in theBaltic Sea new versus regenerated production Mar Ecol Prog Ser 37 277ndash284

38 Ohlendieck U Stuhr A and Siegmund H 2000 Nitrogen fixation by diazotrophiccyanobacteria in the Baltic Sea and transfer of the newly fixed nitrogen to picoplanktonorganisms J Mar Sys 25 213ndash219

39 Sahlsten E and Sorensson F 1989 Planktonic nitrogen transformations during adeclining cyanobacteria bloom in the Baltic Sea J Plankton Res 11 1117ndash1128

40 Wasmund N Nausch G and Schneider B 2005 Primary production rates calculatedby different conceptsmdashan opportunity to study the complex production system in theBaltic Proper J Sea Res 54 244ndash255

41 Sommer F Hansen T and Sommer U 2006 Transfer of diazotrophic nitrogen tomesozooplankton in Kiel Fjord Western Baltic Sea a mesocosm study Mar EcolProg Ser 324 105ndash112

42 Conley DJ Humborg C Rahm L Savchuk OP and Wulff F 2002 Hypoxia inthe Baltic Sea and basin-scale changes in phosphorus biogeochemistry Environ SciTechnol 36 5315ndash5320

43 Sokolov A Andrejev AA Wulff F and Rodriguez-Medina M 1997 The DataAssimilation System for data analysis in the Baltic Sea Systems Ecology Contributions 366

44 Stalnacke P Grimvall A Sundblad K and Tonderski A 1999 Estimation ofriverine loads of nitrogen and phosphorus to the Baltic Sea 1970ndash1993 Environ MonitAssess 582 173ndash200

45 HELCOM 2004 The fourth Baltic Sea pollution load compilation (PLC-4) In BalticSea Environment Proceedings 93 HELCOM Helsinki 188 pp

46 Granat L 2001 Deposition of nitrate and ammonium from the atmosphere to theBaltic Sea In A Systems Analysis of the Baltic Sea 2001 Wulff F Rahm L andLarsson P (eds) Springer-Verlag Berlin Heidelberg p 133ndash148

47 HELCOM 2005 Atmospheric supply of nitrogen lead cadmium mercury and lindaneto the Baltic Sea over the period 1996ndash2000 Baltic Sea Environment Proceedings 101HELCOM Helsinki 75 pp

48 Hille S Nausch G and Leipe T 2005 Sedimentary deposition and reflux ofphosphorus (P) in the Eastern Gotland Basin and their coupling with P concentrations inthe water column Oceanologia 474 663ndash679

49 Nausch G Matthaus W and Feistel R 2003 Hydrographic and hydrochemicalconditions in the Gotland Deep area between 1992 and 2003 Oceanologia 45 557ndash569

50 Suikkanen S Laamanen M and Huttunen M Long-term changes in summerphytoplankton communities of the open northern Baltic Sea Estuarine Coastal andShelf Science (In press)

51 Wulff F Rahm L Hallin A-K and Sandberg J 2001 A nutrient budget model ofthe Baltic Sea In A Systems Analysis of the Baltic Sea 2001 Wulff F Rahm L andLarsson P (eds) Springer-Verlag Berlin Heidelberg p 353ndash372

52 Savchuk OP 2005 Resolving the Baltic Sea into seven subbasins N and P budgets for1991ndash1999 J Mar Sys 56 1ndash15

53 Brettar I and Rheinheimer G 1992 Influence of carbon availability on denitrificationin the central Baltic Sea Limnol Oceanogr 37 1146ndash1163

54 Ronner U and Sorensson F 1985 Denitrification rates in the low-oxygen waters of thestratified Baltic Proper Appl Environ Microbiol 50 801ndash806

55 Voss M Emeis K-C Hille S Neumann T and Dippner JW 2005 Nitrogen cycleof the Baltic Sea from an isotopic perspective Global Biogeochemical Cycles 19 GB3001doi1010292004GB002338

56 Neumann T 2000 Towards a 3D-ecosystem model of the Baltic Sea J Mar Sys 25405ndash420

57 Stigebrandt A 1985 A model for the seasonal pycnocline in rotating systems withapplication to the Baltic proper J Phys Oceanogr 15 1392ndash1404

58 Tuominen L Heinanen A Kuparinen J and Nielsen LP 1998 Spatial and temporalvariability of denitrification in the sediments of the northern Baltic Proper Mar EcolProg Ser 172 13ndash24

59 Kuuppo P Tamminen T Voss M Schulte U and Heiskanen A-S 2006Nitrogenous discharges from River Neva and St Petersburg elemental flows stableisotope signatures and their estuarine modification in the Gulf of Finland the BalticSea J Mar Sys 63 191ndash208

60 Voss M Liskow I Pastuszak M Russ D Schulte U and Dippner JW 2005Riverine discharge into a coastal bay a stable isotope study in the Gulf of GdanskBaltic Sea J Mar Sys 57 127ndash145

61 Pitkanen H Lehtoranta J and Raike A 2001 Internal nutrient fluxes counteractdecreases in external load the case of the estuarial eastern Gulf of Finland Baltic SeaAmbio 30 195ndash201

62 Pitkanen H Kauppila P and Laine Y 2001 Nutrients In The State of the FinnishCoastal Waters The Finnish Environment no 472 Kauppila P and Back S (eds)Finnish Environment Institute Vammala p 37ndash60

63 Yurkovskis A 2004 Long-term land-based and internal forcing of the nutrient state ofthe Gulf of Riga (Baltic Sea) J Mar Sys 50 181ndash197

64 Wasmund N Nausch G and Matthaus W 1998 Phytoplankton spring blooms in thesouthern Baltic Seamdashspatio-temporal development and long-term trends J PlanktonRes 20 1099ndash1117

65 Struck U Pollehne F Bauerfeind E and Bodungen BV 2004 Sources of nitrogenfor the vertical particle flux in the Gotland Sea (Baltic Proper)mdashresults from sedimenttrap studies J Mar Sys 45 91ndash101

66 Heiskanen A-S and Tallberg P 1999 Sedimentation and particulate nutrient dynamicsalong a coastal gradient from a fjord-like bay to the open sea Hydrobiologia 39 127ndash140

67 Tamminen T 1989 Dissolved organic phosphorus regeneration by bacterioplankton5rsquo-nucleotidase activity and subsequent phosphate uptake in a mesocosm enrichmentexperiment Mar Ecol Prog Ser 58 89ndash100

68 Graneli E Wallstrom K Larsson U Graneli W and Elmgren R 1990 Nutrientlimitation of primary production in the Baltic Sea area Ambio 19 142ndash151

69 Kivi K Kaitala S Kuosa H Kuparinen J Leskinen E Lignell R Marcussen Band Tamminen T 1993 Nutrient limitation and grazing control of the Baltic planktoncommunity during annual succession Limnol Oceanogr 38 893ndash905

70 Lignell R Seppala J Kuuppo P Tamminen T Andersen T and Gismervik I2003 Beyond bulk properties responses of coastal summer plankton communities tonutrient enrichment in the northern Baltic Sea Limnol Oceanogr 48 189ndash209

71 Tamminen T and Andersen T 2006 Seasonal phytoplankton nutrient limitationpatterns as revealed by bioassays over Baltic Sea gradients of salinity andeutrophication Mar Ecol Prog Ser (In press)

72 Lignell R Heiskanen A-S Kuosa H Gundersen K Kuuppo-Leinikki PPajuniemi R and Uitto A 1993 Fate of a phytoplankton spring bloom sedimentationand carbon flow in the planktonic food web in the northern BalticMar Ecol Prog Ser94 239ndash252

73 Heiskanen A-S and Leppanen J-M 1995 Estimation of export production in thecoastal Baltic Sea effect of resuspension and microbial decomposition on sedimentationmeasurements Hydrobiologia 31 211ndash224

74 Conley DJ Carstensen J AEligrtebjerg G Christensen PB Dalsgaard T HansenJLS and Josefson AB 2007 Long-term changes and impacts of hypoxia in Danishcoastal waters Ecol Appl 17 (In Press)

75 Diaz RJ and Rosenberg R 1995 Marine benthic hypoxia a review of its ecologicaleffects and the behavioural responses of benthic macrofauna Oceanography and MarineBiology Annual Review 33 245ndash303

76 Kahru M 1997 Using satellites to monitor large-scale environmental change s casestudy of cyanobacteria blooms in the Baltic Sea In Monitoring Algal Blooms NewTechniques for Detecting Large-scale Environmental Change 1997 Kahru M andBrown C (eds) Springer Berlin p 43ndash61

77 Brettar I and Rheinheimer G 1991 Denitrification in the central Baltic evidence forH2S-oxidation as motor of denitrification at the oxic-anoxic interface Mar Ecol ProgSer 77 157ndash169

78 Hietanen S Moisander PH Kuparinen J and Tuominen L 2002 No sign ofdenitrification in a Baltic Sea cyanobacterial bloom Mar Ecol Prog Ser 242 73ndashgt82

79 Tuomainen JM Hietanen S Kuparinen J Martikainen PJ and Servomaa K2003 Baltic Sea cyanobacterial bloom contains denitrification and nitrification genesbut has negligible denitrification activity FEMS Microbiol Ecol 45 83ndash96

80 E Vahtera acknowledges the funding provided by the Maj and Tor Nessling foundationD Conley and T Tamminen would like to thank the EU FF6 project THRESHOLDS(GOCE-003900) B Gustafsson O Savchuk and F Wulff were funded by MAREwhich is funded by the Swedish Fund of Environmental Strategic Research (MISTRA)MARE also funded the workshop that initiated this paper


Emil Vahtera is a researcher at the Finnish Institute of MarineResearch He works mainly on questions regarding Baltic Seaeutrophication and specifically the phosphorus dynamics ofcyanobacteria bloom communities His address Department ofBiological Oceanography Finnish Institute of Marine ResearchPO Box 2 FI-00650 Helsinki FinlandE-mail emilvahterafimrfi

Daniel J Conley is a professor and holds a Marie Curie Chair atthe Geobiosphere Centre at Lund University His researchfocuses on nutrient biogeochemical cycles and the impacts ofglobal change He is engaged in providing links between scienceand the management of aquatic ecosystems His addressGeobiosphere Centre Department of Geology Lund UniversitySolvegatan 12 SE-223 62 Lund Sweden

Bo G Gustafsson is an associate professor in Oceanography atthe Earth Science Center Goteborg University Current Baltic Searesearch activities involve not only eutrophication but also mixingand circulation processes climate change and effects thereofand numerical models He has been highly involved in thedevelopment of the mechanistic models used in MARE Hisaddress Oceanography Earth Science Center Goteborg Uni-versity Box 460 SE-405 30 Goteborg SwedenE-mail boguoceguse

Harri Kuosa is a professor in Baltic Sea research at TvarminneZoological Station University of Helsinki His work includes theevaluation of the responses of the Baltic Sea ecosystem toeutrophication and the studies on Baltic Sea sea-ice biota Hisaddress Tvarminne Zoological Station FI 10900 Hanko FinlandE-mail harrikuosahelsinkifi

Heikki Pitkanen is Chief Scientist at the Finnish EnvironmentInstitute He is studying the behavior and budgets of nutrients inriver catchments estuaries and coastal waters His addressFinnish Environment Institute PO Box 140 FI-00251 HelsinkiFinlandE-mail heikkipitkanenenvironmentfi

Oleg P Savchuk is a visiting researcher at the Department ofSystems Ecology Stockholm University Sweden and is on leaveof absence from the St Petersburg branch of the StateOceanographic Institute Russia where he is head of theLaboratory of the Baltic Sea Problems He is also associateprofessor at the Department of Oceanology St Petersburg StateUniversity Russia He uses mathematical modeling as a tool tostudy marine ecosystems with an emphasis on nutrient biogeo-chemical cycles His address Department of Systems EcologyStockholm University SE 10691 Stockholm SwedenE-mail olegecologysuse

Timo Tamminen is a senior scientist at SYKE (Finnish Environ-ment Institute) working with plankton ecology and eutrophicationof the Baltic Sea presently within the EU 6th FP projectTHRESHOLDS (GOCE-003900) His address Finnish Environ-ment Institute PO Box 140 FI-00251 Helsinki FinlandE-mail timotamminenenvironmentfi

Markku Viitasalo is a professor and head of the Department ofBiological Oceanography in FIMR From 2003 to 2006 he acted asthe leader of the Baltic Sea Research Programme (BIREME)research consortium Cyanobacteria Research in the Baltic Seafrom Genetics to Open Sea Ecosystem Response (CYBER) Hisaddress Department of Biological Oceanography Finnish Insti-tute of Marine Research PO Box 2 FI-00561 HelsingforsFinland

Maren Voss is a senior scientist in the Department of BiologicalOceanography at Baltic Sea Research Institute Warnemundesince 1997 Her research area is the marine nitrogen cycle with anemphasis on nitrogen fixation in the Baltic Sea and tropicaloceanic regions Linking riverine nitrogen loads with the coastalecosystems is another research focus She teaches isotopeecology at the University of Rostock Her address Baltic SeaResearch Institute Warnemunde Seestrasse 15 18119 Rostock-Warnemunde Germany

Norbert Wasmund is senior scientist at the Baltic Sea ResearchInstitute Warnemunde His main research includes phytoplanktonecology evaluation of spatial and temporal patterns of speciescomposition in relation with hydrological and chemical parame-ters bloom dynamics primary production and nitrogen fixationHe is the coordinator of the biological monitoring activities at IOWand chair of the HELCOM Phytoplankton Expert Group Hisaddress Baltic Sea Research Institute Seestr 15 D-18119Warnemunde GermanyE-mail norbertwasmundio-warnemuendede

Fredrik Wulff is a professor in marine systems ecology at theDepartment of Systems Ecology Stockholm University He alsoholds an adjunct position at the Centre for Marine Research at theUniversity of Queensland Australia He works mainly on the BalticSea linking ecology oceanography and biogeochemistry witheconomy He is the scientific coordinator for MARE He is alsoinvolved in global change research particularly studies on landndashocean interactions and coastal zone management His addressDepartment of Systems Ecology Stockholm University SE 10691 Stockholm SwedenE-mail Fredecologysuse


Emil Vahtera Daniel J Conley Bo G Gustafsson Harri Kuosa Heikki Pitkanen Oleg P SavchukTimo Tamminen Markku Viitasalo Maren Voss Norbert Wasmund and Fredrik Wulff

Internal Ecosystem Feedbacks EnhanceNitrogen-fixing Cyanobacteria Blooms andComplicate Management in the Baltic Sea

Eutrophication of the Baltic Sea has potentially increasedthe frequency and magnitude of cyanobacteria bloomsEutrophication leads to increased sedimentation of or-ganic material increasing the extent of anoxic bottomsand subsequently increasing the internal phosphorusloading In addition the hypoxic water volume displays anegative relationship with the total dissolved inorganicnitrogen pool suggesting greater overall nitrogen remov-al with increased hypoxia Enhanced internal loading ofphosphorus and the removal of dissolved inorganicnitrogen leads to lower nitrogen to phosphorus ratioswhich are one of the main factors promoting nitrogen-fixing cyanobacteria blooms Because cyanobacteriablooms in the open waters of the Baltic Sea seem to bestrongly regulated by internal processes the effects ofexternal nutrient reductions are scale-dependent Duringlonger time scales reductions in external phosphorusload may reduce cyanobacteria blooms however onshorter time scales the internal phosphorus loading cancounteract external phosphorus reductions The coupledprocesses inducing internal loading nitrogen removaland the prevalence of nitrogen-fixing cyanobacteria canqualitatively be described as a potentially self-sustaininglsquolsquovicious circlersquorsquo To effectively reduce cyanobacteriablooms and overall signs of eutrophication reductionsin both nitrogen and phosphorus external loads appearessential

INTRODUCTION

Cyanobacteria capable of biological fixation of dissolvedatmospheric dinitrogen gas (N2 fixation) form extensive bloomswhich have been a recurring phenomenon in the Baltic Sea sinceat least the 1960s (1) They are noxious and relevant to theecosystem and to society because of the formation of aconspicuous surface scum toxicity and large nitrogen inputsthrough N2 fixation Traditionally phosphorus alone has beenconsidered as the limiting nutrient for N2-fixing cyanobacteriaIn this article we present how elemental cycles of nitrogen andoxygen are interlinked with the phosphorus cycle in basin-wideand long-term processes To manage cyanobacteria blooms wemust resolve the relative importance of nutrient supply andinternal biogeochemical processes

Most of the nutrient load to the Baltic Sea arrives at the coastbut the most striking cyanobacteria blooms appear in offshorepelagic regions of the basin It is apparent that the actionscontrolling external nutrient loads except those concerningatmospheric load can directly affect coastal ecosystems in sourceregionsThe external loadsmaybe filtered by the coastal zone andpropagated offshore The Baltic Sea with long residence timesand strong internal nutrient recycling thus poses a challenge forecosystem research and the management of nutrient inputs Inthis article we summarize the prevailing knowledge on thecontrolling mechanisms of Baltic Sea cyanobacteria blooms and

highlight the gaps in the present knowledge for the long-termrestoration of this eutrophied ecosystem

BALTIC SEA CYANOBACTERIA

The dominant species of cyanobacteria in the open Baltic Seaare the heterocyte (2)-possessing N2-fixing filamentous speciesbelonging to the order Nostocales Nodularia spumigenaMertens (hepatotoxic) Aphanizomenon flos-aquae (L) Ralfs(presently regarded as nontoxic) (3 4) and Anabaena spp(potentially neurotoxic) (5) Along with the heterocyte-possess-ing filamentous species either filamentous or coccoid colony-forming species without heterocytes (not capable of N2 fixation)frequently occur The small coccoid species may also dominatepelagic cyanobacteria biomass (6 7) Filamentous specieswithout heterocytes or the colonial species which include toxicspecies like Microcystis are abundant in eutrophied coastalareas They can form extensive surface-accumulating bloomsbut it is the N2-fixing filamentous species that generally producethe conspicuous property of the large-scale pelagic bloomsPigments from sediment cores indicate that cyanobacteria havebeen present in the brackish Baltic Sea for 7000ndash8000 years (89) but anthropogenic nutrient loading may have intensifiedtheir blooms (1 10)

The extent intensity and species composition of cyanobac-teria blooms show temporal variation on interannual and intra-annual scales and spatial variation ranging from the scale ofLangmuir circulation to Baltic Seandashwide horizontal inhomoge-neities with distinct vertical distribution patterns within theeuphotic zone (11ndash16) Geographically the blooms are mainlyconfined to the Baltic Proper the Gulf of Finland and the Gulfof Riga with occasional blooms in the Bothnian Sea and theBelt Seas (11 12) This distribution pattern may be caused bythe low nitrogen to phosphorus (N P) ratios (17) andor themesohaline conditions (6 18) prevailing in the central andeastern Baltic Sea Satellite imagery shows that blooms cancover areas larger than 60000 km2 (11) which is approximately16 of the entire Baltic Sea surface area

The N2-fixing cyanobacteria start to grow primarily in Juneafter the exhaustion of dissolved inorganic nitrogen (DIN) andreach bloom concentrations in July or early August (19)Upwelling water rich in dissolved inorganic phosphate (DIP)may also initiate local blooms (20 21) Variations in theintensity and occurrence of blooms are dependent uponwintertime nutrient conditions (22 23) surface layer salinitytemperature and solar irradiation (18) summer stratificationconditions (21) upwelling (20) and frontal processes (21 24)

Nutrient limitation characteristics of the different cyanobac-teria diverge because of the N2-fixation capability of theheterocyte-possessing filamentous species The N2-fixing speciesare most likely limited by phosphorus availability (25 26) andgrowth may be inhibited by sulfate that impedes N2 fixation (6)The nonndashN2-fixing species are primarily limited by nitrogenavailability with phosphorus and iron as potential secondarylimiting factors (6 26) However as the dominant N2-fixing







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Documents

Internal Ecosystem Feedbacks Enhance Nitrogen-fixing Cyanobacteria Blooms and Complicate Management in the Baltic Sea