Emil Vahtera, Daniel J. Conley, Bo G. Gustafsson, Harri Kuosa, Heikki Pitkänen, Oleg P. Savchuk,
Timo Tamminen, Markku Viitasalo, Maren Voss, Norbert Wasmund and Fredrik Wulff
Internal Ecosystem Feedbacks Enhance
Nitrogen-fixing Cyanobacteria Blooms and
Complicate Management in the Baltic Sea
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Eutrophication of the Baltic Sea has potentially increased
the frequency and magnitude of cyanobacteria blooms.
Eutrophication leads to increased sedimentation of organic material, increasing the extent of anoxic bottoms
subsequently increasing the internal phosphorus loading.
In addition, the hypoxic water volume displays a negative
relationship with the total dissolved inorganic nitrogen
pool, suggesting greater overall nitrogen removal with
increased hypoxia. Enhanced internal loading of phosphorus and the removal of dissolved inorganic nitrogen
leads to lower nitrogen to phosphorus ratios, which are
one of the main factors promoting nitrogen-fixing cyanobacteria blooms. Because cyanobacteria blooms in the
open waters of the Baltic Sea seem to be strongly
regulated by internal processes, the effects of external
nutrient reductions are scale-dependent. During longer
time scales, reductions in external phosphorus load may
reduce cyanobacteria blooms; however, on shorter time
scales the internal phosphorus loading can counteract
external phosphorus reductions. The coupled processes
inducing internal loading, nitrogen removal, and the
prevalence of nitrogen-fixing cyanobacteria can qualitatively be described as a potentially self-sustaining ‘‘vicious circle.’’ To effectively reduce cyanobacteria blooms
and overall signs of eutrophication, reductions in both
nitrogen and phosphorus external loads appear essential.
INTRODUCTION
?5
Extensive blooms formed by cyanobacteria capable of biological fixation of dissolved atmospheric dinitrogen gas (N2
fixation) have been a recurring phenomenon in the Baltic Sea
since at least the 1960s (1). They are noxious and relevant to the
ecosystem and to society because of the formation of a
conspicuous surface scum, toxicity, and large nitrogen inputs
through N2 fixation. Traditionally, phosphorus alone has been
considered as the limiting nutrient for N2-fixing cyanobacteria.
In this article we present how elemental cycles of nitrogen and
oxygen are interlinked with the phosphorus cycle in basin-wide
and long-term processes. To manage cyanobacteria blooms, we
must resolve the relative importance of nutrient supply and
internal biogeochemical processes.
Most of the nutrient load to the Baltic Sea arrives at the coast,
but the most striking cyanobacteria blooms appear in offshore
pelagic regions of the basin. It is apparent that the actions
controlling external nutrient loads, except those concerning
atmospheric load, can directly affect coastal ecosystems in source
regions. The external loads may be filtered by the coastal zone and
propagated offshore. The Baltic Sea, with long residence times
and strong internal nutrient recycling, thus poses a challenge for
ecosystem research and the management of nutrient inputs. In
this article we summarize the prevailing knowledge on the
controlling mechanisms of Baltic Sea cyanobacteria blooms and
highlight the gaps in the present knowledge for the long-term
restoration of this eutrophied ecosystem.
Ambio Vol. 36, No. 2/3, Month 2007
BALTIC SEA CYANOBACTERIA
The dominant species of cyanobacteria in the open Baltic Sea
are the heterocyte (2)-possessing, N2-fixing, filamentous species
belonging to the order Nostocales; Nodularia spumigena
Mertens (hepatotoxic); Aphanizomenon flos-aquae (L.) Ralfs
(presently regarded as nontoxic) (3, 4); and Anabaena spp.
(potentially neurotoxic) (5). Along with the heterocyte-possessing filamentous species, either filamentous or coccoid colonyforming species without heterocytes (not capable of N2 fixation)
frequently occur. The small coccoid species may also dominate
pelagic cyanobacteria biomass (6, 7). Filamentous species
without heterocytes or the colonial species, which include toxic
species like Microcystis, are abundant in eutrophied coastal
areas. They can form extensive surface-accumulating blooms,
but it is the N2-fixing filamentous species that generally produce
the conspicuous property of the large-scale pelagic blooms.
Pigments from sediment cores indicate that cyanobacteria have
been present in the brackish Baltic Sea for 7000–8000 years (8,
9), but anthropogenic nutrient loading may have intensified
their blooms (1, 10).
The extent, intensity, and species composition of cyanobacteria blooms show temporal variation on interannual and intraannual scales and spatial variation ranging from the scale of
Langmuir circulation to Baltic Sea–wide horizontal inhomogeneities with distinct vertical distribution patterns within the
euphotic zone (11–16). Geographically, the blooms are mainly
confined to the Baltic Proper, the Gulf of Finland, and the Gulf
of Riga, with occasional blooms in the Bothnian Sea and the
Belt Seas (11, 12). This distribution pattern may be caused by
the low nitrogen to phosphorus (N : P) ratios (17) and/or the
mesohaline conditions (6, 18) prevailing in the central and
eastern Baltic Sea. Satellite imagery shows that blooms can
cover areas larger than 60,000 km2 (11), which is approximately
16% of the entire Baltic Sea surface area.
The N2-fixing cyanobacteria start to grow primarily in June
after the exhaustion of dissolved inorganic nitrogen (DIN) and
reach 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 the
intensity and occurrence of blooms are dependent upon
wintertime nutrient conditions (22, 23), surface layer salinity,
temperature and solar irradiation (18), summer stratification
conditions (21), upwelling (20), and frontal processes (21, 24).
Nutrient limitation characteristics of the different cyanobacteria diverge because of the N2-fixation capability of the
heterocyte-possessing filamentous species. The N2-fixing species
are most likely limited by phosphorus availability (25, 26), and
growth may be inhibited by sulfate that impedes N2 fixation (6).
The non–N2-fixing species are primarily limited by nitrogen
availability, with phosphorus and iron as potential secondary
limiting factors (6, 26). However, as the dominant N2-fixing
species differ in their limitation patterns and stoichiometry, the
species composition and spatial and temporal occurrence of
blooms are affected by nutrient availability (27, 28). Meteoro-
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1
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logical conditions also shape the spatial occurrence of blooms
(29). Sedimentary and grazing losses of filamentous species are
generally small, and most of the biomass is decomposed in the
surface layer (30–32). Blooms are terminated by several factors,
including nutrient limitation, mixing events, decreased solar
irradiation, decreasing water temperature, and possibly viral
lysis (18, 33).
The amount of N2-fixing cyanobacteria increased from 1968
to 1981 (34), and the increase in late-summer chlorophyll a
concentrations in the 1990s (35) may be related to increases in the
abundance of cyanobacteria. The N2-fixation capability of some
of the cyanobacteria causes large additional nitrogen inputs to
the Baltic Sea during summer. N2-fixation estimates span a wide
range, reflecting the patchy nature and interannual variability of
the blooms, as well as, partly, methodological difficulties. Recent
estimates suggest that cyanobacteria N2 fixation can introduce
180,000–430,000 tonnes (19, 36) of new nitrogen annually [values
as high as 790,000 tonnes have been suggested (19)], supporting
new production during nitrogen-limited periods. N2 fixation has
supported new production to a variable extent and has been
estimated to supply the phytoplankton community with enough
nitrogen to account for 27% of total nitrogen uptake during
summer bloom conditions (37). In other studies, 5–10% of total
fixed nitrogen was found in the picoplanktonic size fraction
during a bloom (38), and uptake was observed to be dominated
by regenerated forms of nitrogen (37, 39). However, more recent
estimates show that N2 fixation can supply up to 50–90% of total
nitrogen demand (7, 27) and can account for 18–23% of net
primary production during a 108-day period of new production
from 28 March to 13 July 2001 (40) and for 30–90% of net
community production from June to August (36). Also, it is
estimated that up to 45% of mesozooplankton nitrogen demand
is contributed by nitrogen fixation through trophic vectors (41).
Thus, N2 fixation appears to have an important role in
supporting production in nitrogen-deficient areas.
Phosphorus availability is the most important factor setting
the maximum limits on the magnitude of cyanobacteria blooms.
The biomass of N2-fixing cyanobacteria is correlated with the
wintertime phosphorus pools and the excess amount of
phosphorus remaining after the spring bloom, which is based
on the assumption of a balanced Redfield-ratio uptake of
nutrients during the spring bloom (Excess DIP ¼ DIP–DIN/16,
in molar units) (22, 23). Nevertheless, the correlation is not
ubiquitous (19), and considerable temporal and spatial variation
occurs between years and in different basins of the Baltic Sea.
Thus, resolving how the coupled large-scale biogeochemical
cycles of nitrogen and phosphorus regulate cyanobacteria
blooms is of great relevance. Therefore, we explored the pool
sizes of nitrogen and phosphorus, the regulation of these pools,
and the balance of nitrogen and phosphorus supply to the
productive upper mixed 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 we
applied a basin-wide approach as previously done for phosphorus (42). Nitrogen pools were summed up for three
subbasins where N2 fixation occurs: the Baltic Proper and the
Gulfs of Finland and Riga. Annually averaged pools of total
nitrogen (TN) and DIN as well as volumes of water confined by
the oxygen isosurfaces of 0 and 1 mL L1 were computed with
the Data Assimilation System (43) on three-dimensional fields
reconstructed from observations found in the Baltic Environment Database (BED) (Stockholm University, Department of
Systems Ecology, Marine Ecosystems Modeling Group, http://
2
data.ecology.su.se/models/bed.htm), which includes a vast
amount of data from monitoring programs and scientific cruises
in the region. The time series of combined nitrogen input to the
Baltic Proper from land and atmospheric sources was compiled
from several sources (44), including (45), unpublished data in
BED, the periodic load compilations by HELCOM (e.g. 46),
(47), and published and unpublished data from the Cooperative
Programme for Monitoring and Evaluation of the Long-range
Transmission of Air Pollutants in Europe (e.g. 48).
Results
The pool of phosphorus in the water column shows large
variation between years, the variation being up to three times
the size of the average annual allochthonous load (42). The
winter-to-winter changes in the basin-wide DIP pool in the
Baltic Proper are correlated to the changes in bottom area
covered by hypoxic water, but not to changes in total
phosphorus load (42). Thus, regarding the phosphorus availability of N2-fixing cyanobacteria, internal processes, i.e. the
sediment release of phosphorus into deep-water layers and the
conveyance of this phosphorus pool to the upper mixed layer,
are the key factors. The deep-water phosphate concentrations in
the Gulf of Finland and Baltic Proper have increasing trends
during stagnation periods with low oxygen concentrations in
deep waters (49, 50); this is also mirrored in the winter mixed
surface layer concentrations (49, 51).
Because N2-fixing cyanobacteria are dependent on the
availability of phosphorus and generally gain competitive
advantage from low DIN : DIP ratios (e.g. 17), the regulation
of the nitrogen pool is also of importance; next we examine
factors regulating the total DIN pool of the Baltic Sea.
The long-term annual (mean 6 SD) load is 752,000 6 98,000
tonnes nitrogen for the 33-year period examined, during which
no clear and definite long-term trends were observed (Fig. 1).
Fluctuations can be explained by climatic variations, particularly in freshwater runoff. For the TN pool there is a long-term
increasing trend until the mid-1980s, but there were several
problems with analytical methods used in many of the
laboratories in the early 1970s, so data from this period should
be taken with caution.
The average year-to-year variation in nitrogen load is ca.
72,000 tonnes, whereas the corresponding variation in the TN
pool in the Gulfs of Finland and Riga and the Baltic Proper
combined is about 225,000 tonnes. No clear correlation between
loads and either the pool itself or its year-to-year changes were
observed. The annual net exchange of TN between the Baltic
Proper and adjacent basins is about 120,000 tonnes (52, 53) and
varies between years by less than 30,000 tonnes (44). Subsequently, exchange processes cannot explain the variations in the
TN pool. However, there is a significant negative relationship
between the DIN pool and hypoxic water volume (Fig. 2). The
relationship suggests that losses of the DIN pool through
nitrogen removal processes may be higher during periods of
hypoxia. The relative role of nitrogen removal processes in the
pelagic water column is unknown. Denitrification has been
observed at the interface of anoxic and oxic waters in the
stratified Baltic Proper (54, 55), but the importance of the process
cannot be determined from these measurements. The loss of
nitrogen through the anammox process has been observed to
occur in the oxygen-poor and ammonia-rich environment of the
eastern Gotland Basin (56) and could potentially be responsible
for some nitrogen losses on a Baltic Sea scale as well.
By simply relating the amount of nitrogen load to the study
area surface layer volume we should see an increase in nitrogen
concentrations due to the external load. If we assume that the
752,000 tonnes of total nitrogen transported annually by rivers
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Ambio Vol. 36, No. 2/3, Month 2007
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Figure 1. Long-term variations of
the annually averaged TN pool in
the Baltic Proper, the Gulf of Finland, and the Gulf of Riga and
external annual nitrogen inputs (t
TN y1) to the area.
Figure 2. Relationship between
total amounts of DIN in the Baltic
Proper, the Gulf of Finland, and the
Gulf of Riga and hypoxic water
volume confined by isosurfaces of
0 and 1 mL O2 L1 in the same
basins.
and deposited from the atmosphere would be instantaneously
mixed into the 14,500 km3 of the surface layer (0–60 m) in the
Baltic Proper, the Gulf of Finland, and the Gulf of Riga and that
there would be no net exchange of nitrogen between the study
area and the neighboring basins, an annual increase of about 3.7
lM nitrogen would be observed. The amount would be even
larger with N2 fixation added. This hypothetical increase in
nitrogen concentration in surface waters has not been observed in
long-term observations (57); therefore a considerable sink of
nitrogen is postulated by models (58, 59) and has been confirmed
by empirical budgets (52, 53) and direct measurements (54, 60).
Denitrification in sandy coastal sediments has been suggested as one of the major sinks for nitrogen entering the Baltic Sea
(57). A loss of all river DIN discharging into the Baltic Proper
and the Gulfs of Finland and Riga (344,000 t y1) over the
coastal area of these basins shallower than 30 m (80,000 km2)
would result in a loss of 0.84 mmol N m2 d1, roughly
matching denitrification rates as reported from deep bottom
sediments of the Gulf of Finland (60). During the productive
season, autotrophic nitrate uptake and sedimentation of
particulate organic nitrogen taking place in the coastal zone
explains the low nitrate concentrations found already at
relatively short distances (tens of kilometers) from the coast
(61, 62). Coastal areas of the Baltic Sea shallower than 30 m
receive high nitrogen loads that are rapidly turned over during
the productive season (62). In the northern parts of the Baltic
Ambio Vol. 36, No. 2/3, Month 2007
Sea, the terrestrial loads are, however, conveyed almost intact
toward the offshore system during winter months.
Thus, similar to phosphorus, internal processes, N2 fixation,
denitrification, anammox, sedimentation, and trophic transfer
control the annual variations of nitrogen concentrations in the
open sea to a greater extent than external loads. The net effect
of these processes and the magnitudes of N2 fixation and N2
production counteracting each other cannot be estimated from
mass balance calculations without direct measurements of these
processes.
Nevertheless, load reductions might have more pronounced
effects on smaller spatial scales in subbasins. The separate
subbasins have their own characteristic internal dynamics in their
nitrogen budgets. For example, in the Gulf of Finland a 35%
reduction of external nitrogen load from the late 1980s to the late
1990s was observed (63). During the same period, wintertime
DIN concentrations in the Gulf decreased by 20–30% (64).
Simultaneous decreases in external nitrogen load and winter DIN
appear to have taken place also in the Gulf of Riga (65). Possible
reasons for this discrepancy between the Baltic Proper and the
Gulfs of Finland and Riga can be different ratios of load versus
mean annual nitrogen content of a basin, which were 1 : 2.6 for
the Gulf of Finland, 1 : 1.9 for the Gulf of Riga, and 1 : 5.2 for the
Baltic Proper (53). Thus, the shorter residence time of water and
nitrogen in the Gulfs of Finland and Riga probably enable the
decreased loads to affect the basin-wide nitrogen dynamics more
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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 a central Baltic Sea monitoring station (BY15, eastern Gotland basin). Estimates for organic nutrients were acquired by
subtracting the dissolved inorganic fraction from total nutrients. Average values for 1994–2004.
rapidly than in the Baltic Proper. Furthermore, denitrification is
possibly favored in the gulfs because of the relatively large
proportion of bottom sediments at depths of 30–60 m, i.e. above
the permanent halocline, ensuring the availability of nitrate in the
denitrification process in the sediments.
HYDROGRAPHIC AND BIOGEOCHEMICAL
CONTROLS OF CYANOBACTERIA BLOOMS
Data and Methods
We analyzed the annual development of nitrogen and phosphorus pools and how they are related to hydrography and
biogeochemistry. The data were acquired mainly from the
Swedish Meteorological and Hydrological Institute, but also
from monitoring data from other nations. Data from the station
BY15 in the central Eastern Gotland basin for 1994–2005 were
used for analysis of the annual development of nutrient
4
concentrations. The number of vertical profiles used ranges
from 139 to 170, depending on the parameter. The vertical
average concentrations in Figure 3 are computed by first
interpolating the measurements vertically to a 1-m resolution;
they are then integrated using the hypsographic function for the
Baltic Proper, excluding the Gulf of Finland, the Gulf of Riga,
and the Bornholm basin. The monthly averages for specific
depth intervals presented in Figure 4 are based on 8–20 profiles
per month, with the highest measurement frequency being in
August and the lowest in November and December. Data for
Figure 5 were acquired from BED.
Results
The onset of the spring bloom is controlled by average light
conditions and stratification in the surface layer (66). At the
termination of the spring bloom, most of the DIN and much of
the DIP is consumed in the Baltic Proper, on average down to
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Ambio Vol. 36, No. 2/3, Month 2007
Figure 4. Monthly averages of vertical means for the years 1994–2004 of observations from a central Baltic Sea monitoring station (BY15,
eastern Gotland basin) in different depth intervals. The vertical means are computed using the hypsographic function for the Baltic Proper,
excluding the Gulfs of Finland and Riga, and Bornholm and Arkona basins.
the permanent halocline (60 m) (Fig. 3c,d). In recent years the
spring bloom is terminated because of the lack of available
DIN, with excess DIP remaining in the surface layer. However,
DIP concentrations continue to decrease during the summer. In
most years DIP concentrations reach levels that limit phytoplankton growth, with some DIP available below the summer
thermocline (15–20 m) (Fig. 3d). After the spring bloom,
roughly 50% of the consumed inorganic nutrients remain in the
surface layer, but in organic forms (Fig. 3e,f).
Significant increases in pelagic inorganic nutrient concentrations above the halocline occur again in October (Fig. 3c,d).
From the average time series in the Baltic Proper, about half of
the winter surface pool is built up from the regeneration of
nutrients, the nutrient load, and, possibly, vertical diffusion
between October and December, whereas the remaining half
comes with vertical mixing in January and February.
A closer look at the integrated amount of nutrients in the
upper 60 m reveals that, on average, DIP concentrations
increase from 0.25 lM to 0.35 lM from September to
December, whereas total phosphorus (TP) remains constant
(Fig. 4). This means that remineralized phosphorus builds up as
a bioavailable DIP pool instead of being used or lost through
burial or other processes. An increase of ca. 0.15 lM in both
DIP and TP concentrations occurs from December to January,
with an additional increase of ca. 0.10 lM reaching 0.60 lM in
March (Fig. 4). Dissolved inorganic nitrogen and TN follow the
same pattern; an increase in DIN from about 1 lM in
September to 2.5 lM in December occurs with an insignificant
change in TN. This change is followed by an increase of ca. 2
lM in both DIN and TN concentrations during the winter
months (Fig. 4).
Averaged over the same water volume, the nutrient loads to
the Baltic Proper correspond to approximately 0.25 lM mo1
(or 3 lM y1) nitrogen (365,000 t y1) and 0.005 lM month1
(0.06 lM y1) phosphorus (18,300 t y1). Contrasting to that of
nitrogen, the monthly load of TP is small relative to pool size
Ambio Vol. 36, No. 2/3, Month 2007
and therefore does not cause detectable changes in concentration on seasonal time scales.
Neglecting loads and horizontal advection, we estimate that
about 40% of the winter DIP pool above 60 m comes from
regeneration in the upper water column and 60% from mixing/
advection from below. Roughly the same figures apply for DIN,
but here atmospheric loads should be taken into account.
Atmospheric deposition of nitrogen is about 2 g m2 y1 (e.g.
48) or 2.5 lM y1 in a 60-m column. Thus, for the period from
October to March the atmospheric contribution should be
about 1.2 lM, or 35% of the total increase.
The increase in TN in the upper 20-m layer in July (Fig. 4) is
indicative of nitrogen fixation. The fixed nitrogen is efficiently
removed from the system, as shown by the decreasing TN
concentrations beginning in August (Fig. 4). Water column
increases of DIN are observed by November. TN and DIN
concentrations have a rather similar annual pattern at deeper
depths in contrast to the upper 20-m layer, which would
indicate a loss of the fixed nitrogen in the upper (0–20 m) water
column. Therefore, fixed nitrogen seems to be removed by some
process (potentially denitrification or anammox at intermediate
depths) from the offshore system before the winter period.
Rapid settling of particulate material can also remove fixed
nitrogen from the water column. Baltic Sea deep waters (. 180
m) have a depleted d15N-signal, indicative of nitrogen fixation
(67), and nitrogen has a greater sedimentary loss than carbon or
phosphorus (68). However, the relative contribution of settling
losses of nitrogen introduced to the system by N2 fixation is
poorly known.
The year-to-year variations in surface layer DIN and DIP
are sensitive to hydrographic conditions because a large
proportion of the winter pools of both surface water DIN and
DIP comes from vertical mixing and advection from below the
halocline, as shown above. In periods when the halocline is
weak and well ventilated, oxygen conditions are improved,
resulting in lower DIP and higher DIN concentrations,
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5
Figure 5. Vertical distribution of
nitrate and nitrite and phosphate
concentrations from the central
Baltic Sea (monitoring station
BY15, eastern Gotland basin) in
relation to oxygen conditions
(black contours, 0–2 mL O2 L1).
Values are 90-day averages.
especially nitrate, in deep waters. The opposite occurs when the
halocline is strong and hypoxia/anoxia 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, 69), 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
6
the N2-fixing Aphanizomenon and Nodularia, suggested by
Niemistö et al. (15), reflects their different nutritional and
physiological properties (21, 27, 28, 36).
Local blooms are more variable in space and time than the
offshore or coastal blooms. Occasional large blooms may occur
in sheltered basins in archipelagos often affected by local landbased nutrient inputs, with a more variable species composition
than offshore or coastal blooms. Blooms often include Microcystis, Planktothrix, Oscillatoria, and Pseudanabaena species (1
and references therein), which are non–N2-fixing species and
consequently compete for DIN with other phytoplankton taxa.
The main triggering factor for these blooms may be exceptionally strong stratification and warm water, as well as selective
grazing favoring cyanobacteria.
A VICIOUS CIRCLE?
The Baltic Sea basins, where the conspicuous cyanobacteria
blooms occur, have been generally nitrogen-limited throughout
the growth season (70–73), which gives cyanobacteria a
competitive advantage during summer months, but also affects
the seasonal dynamics of planktonic production and sedimentation. The loading of nitrogen directly enhances production
during the spring bloom, which is quantitatively the most
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Ambio Vol. 36, No. 2/3, Month 2007
Figure 6. A schematic presentation of main feedback processes that inhibit recovery from eutrophication and favor cyanobacteria blooms in
the Baltic Sea. The vicious circle is potentially sustained by nitrogen(N)-limited production and sedimentation of phytoplankton, especially
during the spring bloom, and subsequent oxygen depletion in bottom waters, causing internal loading of phosphorus (P). Physical transport
of released phosphorus to surface layers would enhance N2 fixation by diazotrophic cyanobacteria. These seasonal feedbacks between
biogeochemical cycles of nitrogen, phosphorus, and oxygen can effectively counteract reductions in the external phosphorus loading to the
system if nitrogen loading is not reduced as well. Grey arrows depict material flows. Thin arrows depict causal relationships and successive
events. Several potential feedback mechanisms and limiting factors are omitted for clarity. For details, see text.
important production period annually both in the offshore
Baltic Proper (40), and even more so in coastal regions (30, 68,
74). A large part of this nitrogen-fueled production is lost from
the upper mixed layer through sedimentation, and it comprises
the major sedimentation event on a seasonal scale (30, 74, 75).
When decomposed in bottom waters of the stratified Baltic
Sea, sedimenting biomass consumes near-bottom water oxygen.
Phosphate is released from the sediments during hypoxic and
anoxic conditions. External nitrogen loading thus appears to
boost internal phosphorus loading through these seasonal
feedbacks. Recent studies suggest that repeated hypoxic events
lead to an increase in further hypoxia (76), creating a regime
shift in benthic communities and changes in organic matter
processing (77). This feedback creates a persistent internal
loading of phosphate even if external nutrient loads are
reduced. When phosphate that is released from sediments
reaches the surface waters because of annual turnovers or
summertime upwellings, the occurrences of cyanobacteria
blooms are potentially increased. Major saltwater inflows have
also been noted to stimulate cyanobacteria blooms by lifting up
phosphate-rich deep waters (78). Increased blooms of N2-fixing
cyanobacteria again incur further anoxia through increased
nitrogen input to the generally nitrogen-limited summer-time
pelagic ecosystem.
In addition to affecting sediment release of phosphorus, the
hypoxic water volume has a negative relationship with the total
DIN pool of the Baltic Sea. Therefore, the same conditions that
increase internal loading of phosphorus tend to increase
nitrogen removal, further facilitating the occurrence of N2fixing cyanobacteria by lowering the DIN : DIP ratio. The
increased nitrogen removal with increasing hypoxia might be
related to the increasing area of the oxic and anoxic interface
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area where denitrification is possible and nitrate supply is not
limiting the process.
These connections accentuate the internal regulation of the
present eutrophied state of the Baltic Sea, which might be
qualitatively described as a vicious circle (73). The vicious circle
(Fig. 6) depicts the relationships between the nitrogen,
phosphorus, and oxygen cycles and how the feedbacks between
these elements may work. It is forced and controlled by both
external and internal nutrient loading and physical forcing. The
potentially self-sustaining vicious circle can effectively counteract reductions in the external phosphorus loading to the system,
as is evidenced in the Gulf of Finland (63). Because of these
feedbacks, the Baltic Sea seems to be in a state of inhibited
recovery regarding eutrophication.
The nitrogen inputs through N2 fixation and other sources
are approximately balanced by the losses (denitrification,
including anammox, and permanent burial). This is suggested
by the relatively constant winter DIN concentrations. But, only
a few measurements on DIN loss rates have been made in the
pelagic Baltic Proper (54–56, 79–81) , and the regulation of the
loss rates by either organic matter supply (54) or reduced sulfur
compounds (79) is unknown. How the feedback between input
and removal of DIN works in detail is an important subject for
future work.
Phosphorus losses are coupled with the state of anoxia in the
basin. By moderating the area of reducing sediments and the
volume of anoxic water, DIP concentrations will decline. Since
the magnitude of the DIN-limited spring bloom affects the
amount of sedimenting organic material to a large extent
annually, the external load of both nitrogen and phosphorus
will have to be reduced to curb anoxia and the amount of N2fixing cyanobacteria.
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7
CONCLUSIONS
The size of the total nitrogen pool in the Baltic Sea is governed
by internal processes (N2 fixation, denitrification, anammox,
trophic transfer, permanent burial, resuspension) to a larger
extent than by external loading, as evidenced by the considerable amplitude of the annual variation in the TN pool in
relation to average annual loads. Hypoxic water volume shows
a negative relationship with the DIN pool; however, the relative
importance of each individual process governing the nitrogen
pool size remains to be resolved.
Wintertime DIN and DIP pools are largely governed by
hydrography in the offshore system. Approximately 40% of the
annual replenishment of DIP in the surface layer stems from
remineralization of organic phosphorus originating from the
previous growth season and 60% from deep water by mixing
events. For DIN the internal sources have a similar relation,
whereas an additional input from atmospheric sources during
October to March constitutes 35% of the wintertime total
increase. The nitrogen input caused by biological N2 fixation is
removed by internal processes, either by burial, trophic
transfers, denitrification, or anammox.
Both phosphorus and nitrogen transformations, including
physicochemical and biological reactions, which are mediated
by microbial activity, are indirectly connected to oxygen
conditions controlled by organic matter sedimentation and
hydrography. The pelagic nutrient budgets for both nitrogen
and phosphorus are largely unaffected by short-term changes in
external loads as shown by much larger variations in
interannual changes in total nutrients relative to estimates of
external loads. Thus, offshore cyanobacteria blooms are
strongly regulated by internal processes. External nutrient loads
more directly affect the coastal and local blooms. The rim of
southern sandy coastal sediments seems to remove much of the
external nitrogen loads through denitrification. This can affect
the outcome of load reduction responses, and thus possibly
shape the species composition of bloom communities on an
onshore–offshore gradient.
Because of the interconnected cycles of oxygen, phosphorus,
and nitrogen, the Baltic Sea is in a state of inhibited recovery
regarding eutrophication. Ongoing eutrophication induces wide
spread hypoxia and large permanently reducing bottom areas
mainly through sedimentation of the intense nitrogen-limited
spring bloom, thus facilitating internal phosphorus loading.
This state of the system promotes the occurrence of N2-fixing
cyanobacteria and tends to counteract the effects of external
phosphorus load reductions on shorter time scales. To alleviate
the adverse effects of eutrophication in the Baltic Sea, nitrogen
and phosphorus emissions should be reduced.
References and Notes
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82. E. Vahtera acknowledges the funding provided by the Maj and Tor Nessling foundation.
D. Conley and T. Tamminen would like to thank the EU 6th FFP project
THRESHOLDS (GOCE-003900). B. Gustafsson, O. Savchuk, and F. Wulff were
funded by MARE, which is funded by the Swedish Fund of Environmental Strategic
Research (MISTRA). MARE also funded the workshop that initiated this paper.
Ambio Vol. 36, No. 2/3, Month 2007
Emil Vahtera is a researcher at the Finnish Institute of Marine
Research. He works mainly on questions regarding Baltic Sea
eutrophication and specifically the phosphorus dynamics of
cyanobacteria bloom communities. His address: Department
of Biological Oceanography, Finnish Institute of Marine
Research, P.O. Box 2, FI-00650 Helsinki, Finland.
[email protected]
Daniel J. Conley is a professor and holds a Marie Curie Chair
at the Geobiosphere Centre at Lund University. His research
focuses on nutrient biogeochemical cycles and the impacts of
global change. He is engaged in providing links between
science and the management of aquatic ecosystems. His
address: Geobiosphere Centre, Department of Geology, Lund
University, Sölvegatan 12, SE-223 62 Lund, Sweden
Bo G. Gustafsson is an associate professor in Oceanography
at the Earth Science Center, Göteborg University. Current
Baltic Sea research activities involve not only eutrophication,
but also mixing and circulation processes, climate change and
effects thereof, and numerical models. He has been highly
involved in the development of the mechanistic models used in
MARE. His address: Oceanography, Earth Science Center,
Göteborg University, Box 460, SE-405 30 Göteborg, Sweden.
[email protected]
Harri Kuosa is a professor in Baltic Sea research at Tvärminne
Zoological Station, University of Helsinki. His work includes the
evaluation of the responses of the Baltic Sea ecosystem to
eutrophication and the studies on Baltic Sea sea-ice biota. His
address: Tvärminne Zoological Station, FI 10900 Hanko,
Finland.
[email protected]
Heikki Pitkänen is a senior scientist at the Finnish Environment
Institute. He is studying the behavior and budgets of nutrients
in river catchments, estuaries, and coastal waters. His
address: Finnish Environment Institute, P.O. Box 140, FI00251 Helsinki, Finland.
[email protected]
Oleg P. Savchuk is a visiting researcher at the Department of
Systems Ecology, Stockholm University, Sweden, and is on
leave of absence from the St. Petersburg branch of the State
Oceanographic Institute, Russia, where he is head of the
Laboratory of the Baltic Sea Problems. He is also associate
professor at the Department of Oceanology, St. Petersburg
State University, Russia. He uses mathematical modeling as a
tool to study marine ecosystems, with an emphasis on nutrient
biogeochemical cycles. His address: Department of Systems
Ecology, Stockholm University, SE 10691 Stockholm, Sweden.
[email protected]
Timo Tamminen is a senior scientist at SYKE (Finnish
Environment Institute), working with plankton ecology and
eutrophication of the Baltic Sea, presently within the EU 6th FP
project THRESHOLDS (GOCE-003900). His address: Finnish
Environment Institute, P.O. Box 140, FI-00251 Helsinki,
Finland.
[email protected]
Markku Viitasalo is a professor and head of the Department of
Biological Oceanography in FIMR. From 2003 to 2006 he
acted as the leader of the Baltic Sea Research Programme
(BIREME) research consortium Cyanobacteria Research in
the Baltic Sea from Genetics to Open Sea Ecosystem
Response (CYBER). His address: Department of Biological
Oceanography, Finnish Institute of Marine Research, P.O. Box
2, FI-00561 Helsingfors, Finland.
Maren Voss is a senior scientist in the Department of Biological
Oceanography at Baltic Sea Research Institute Warnemünde
since 1997. Her research area is the marine nitrogen cycle with
an emphasis on nitrogen fixation in the Baltic Sea and tropical
Ó Royal Swedish Academy of Sciences 2007
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9
oceanic regions. Linking riverine nitrogen loads with the
coastal ecosystems is another research focus. She teaches
isotope ecology at the University of Rostock. Her address:
Baltic Sea Research Institute Warnemünde, Seestrasse 15,
18119 Rostock-Warnemünde, Germany.
Norbert Wasmund is senior scientist at the Baltic Sea
Research Institute Warnemünde. His main research includes
phytoplankton ecology, evaluation of spatial and temporal
patterns of species composition in relation with hydrological
and chemical parameters, bloom dynamics, primary production, and nitrogen fixation. He is the coordinator of the
biological monitoring activities at IOW and chair of the
HELCOM Phytoplankton Expert Group. His address: Baltic
Sea Research Institute, Seestr. 15, D-18119 Warnemünde,
Germany.
[email protected]
10
Fredrik Wulff is a professor in marine systems ecology at the
Department of Systems Ecology, Stockholm University. He
also holds an adjunct position at the Centre for Marine
Research at the University of Queensland, Australia. He works
mainly on the Baltic Sea, linking ecology, oceanography, and
biogeochemistry with economy. He is the scientific coordinator
for MARE. He is also involved in global change research,
particularly studies on land–ocean interactions and coastal
zone management. His address: Department of Systems
Ecology, Stockholm University, SE 106 91 Stockholm,
Sweden.
[email protected]
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Ambio Vol. 36, No. 2/3, Month 2007