Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs

Filamentous, nitrogen-fixing cyanobacteria form extensive summer blooms in the Baltic Sea. Their ability to fix dissolved N₂ allows cyanobacteria to circumvent the general summer nitrogen limitation, while also generating a supply of novel bioavailable nitrogen for the food web. However, the fate of the nitrogen fixed by cyanobacteria remains unresolved, as does its importance for secondary production in the Baltic Sea. Here, we synthesize recent experimental and field studies providing strong empirical evidence that cyanobacterial nitrogen is efficiently assimilated and transferred in Baltic food webs via two major pathways: directly by grazing on fresh or decaying cyanobacteria and indirectly through the uptake by other phytoplankton and microbes of bioavailable nitrogen exuded from cyanobacterial cells. This information is an essential step toward guiding nutrient management to minimize noxious blooms without overly reducing secondary production, and ultimately most probably fish production in the Baltic Sea.     

Nitrogen fixation estimates for the Baltic Sea indicate high rates for the previously overlooked Bothnian Sea

Dense blooms of diazotrophic filamentous cyanobacteria are formed every summer in the Baltic Sea. We estimated their contribution to nitrogen fixation by combining two decades of cyanobacterial biovolume monitoring data with recently measured genera-specific nitrogen fixation rates. In the Bothnian Sea, estimated nitrogen fixation rates were 80 kt N year⁻¹, which has doubled during recent decades and now exceeds external loading from rivers and atmospheric deposition of 69 kt year⁻¹. The estimated contribution to the Baltic Proper was 399 kt N year⁻¹, which agrees well with previous estimates using other approaches and is greater than the external input of 374 kt N year⁻¹. Our approach can potentially be applied to continuously estimate nitrogen loads via nitrogen fixation. Those estimates are crucial for ecosystem adaptive management since internal nitrogen loading may counteract the positive effects of decreased external nutrient loading.     

Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea

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 and 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 nitrogenfixing 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.     

Hydroxylated and methoxylated polybrominated diphenyl ethers and polybrominated dibenzo-p-dioxins in red alga and cyanobacteria living in the Baltic Sea

Hydroxylated polybrominated diphenyl ethers (OH-PBDEs) and methoxylated polybrominated diphenyl ethers (MeO-PBDEs) are present in the ecosystem of the Baltic Sea. OH-PBDEs are known to be both natural products from marine environments and metabolites of the anthropogenic polybrominated diphenyl ethers (PBDEs), whereas, MeO-PBDEs appear to be solely natural in origin. Polybrominated dibenzo-p-dioxins (PBDDs) are by-products formed in connection with the combustion of brominated flame retardants (BFRs), but are also indicated as natural products in a red alga (Ceramium tenuicorne) and blue mussels living in the Baltic Sea. The aims of the present investigation were to quantify the OH-PBDEs and MeO-PBDEs present in C. tenuicorne; to verify the identities of PBDDs detected previously in this species of red alga and to investigate whether cyanobacteria living in this same region of the Baltic Sea contain OH-PBDEs, MeO-PBDEs and/or PBDDs. The red alga was confirmed to contain tribromodibenzo-p-dioxins (triBDDs), by accurate mass determination and additional PBDD congeners were also detected in this sample. This is the first time that PBDDs have been identified in a red alga. The SigmaOH-PBDEs and SigmaMeO-PBDEs concentrations, present in C. tenuicorne were 150 and 4.6 ng g(-1) dry weight, respectively. In the cyanobacteria 6 OH-PBDEs, 6 MeO-PBDEs and 4 PBDDs were detected by mass spectrometry (electron capture negative ionization (ECNI)). The PBDDs and OH-PBDEs and MeO-PBDEs detected in the red alga and cyanobacteria are most likely of natural origin.     

Extremes of Temperature, Oxygen and Blooms in the Baltic Sea in a Changing Climate

In the future, the Baltic Sea ecosystem will be impacted both by climate change and by riverine and atmospheric nutrient inputs. Multi-model ensemble simulations comprising one IPCC scenario (A1B), two global climate models, two regional climate models, and three Baltic Sea ecosystem models were performed to elucidate the combined effect of climate change and changes in nutrient inputs. This study focuses on the occurrence of extreme events in the projected future climate. Results suggest that the number of days favoring cyanobacteria blooms could increase, anoxic events may become more frequent and last longer, and salinity may tend to decrease. Nutrient load reductions following the Baltic Sea Action Plan can reduce the deterioration of oxygen conditions.     

Ecosystem consequences of cyanobacteria in the northern Baltic Sea

Cyanobacteria of the Baltic Sea have multiple effects on organisms that influence the food chain dynamics on several trophic levels. Cyanobacteria contain several bioactive compounds, such as alkaloids, peptides, and lipopolysaccharides. A group of nonribosomally produced oligopeptides, namely microcystins and nodularin, are tumor promoters and cause oxidative stress in the affected cells. Zooplankton graze on cyanobacteria, and when ingested, the hepatotoxins (nodularin) decrease the egg production of, for example, copepods. However, the observed effects are very variable, because many crustaceans are tolerant to nodularin and because cyanobacteria may complement the diet of grazers in small amounts. Cyanobacterial toxins are transferred through the food web from one trophic level to another. The transfer rate is relatively low in the pelagic food web, but reduced feeding and growth rates of fish larvae have been observed. In the benthic food web, especially in blue mussels, nodularin concentrations are high, and benthic feeding juvenile flounders have been observed to disappear from bloom areas. In the littoral ecosystem, gammarids have shown increased mortality and weakening of reproductive success under cyanobacterial exposure. In contrast, mysid shrimps seem to be tolerant to cyanobacterial exposure. In fish larvae, detoxication of nodularin poses a metabolic cost that is reflected as decreased growth and condition, which may increase their susceptibility to predation. Cyanobacterial filaments and aggregates also interfere with both hydromechanical and visual feeding of planktivores. The feeding appendages of mysid shrimps may clog, and the filaments interfere with prey detection of pike larvae. On the other hand, a cyanobacterial bloom may provide a refuge for both zooplankton and small fish. As the decaying bloom also provides an ample source of organic carbon and nutrients for the organisms of the microbial loop, the zooplankton species capable of selective feeding may thrive in bloom conditions. Cyanobacteria also compete for nutrients with other primary producers and change the nitrogen (N): phosphorus (P) balance of their environment by their N-fixation. Further, the bioactive compounds of cyanobacteria directly influence other primary producers, favoring cyanobacteria, chlorophytes, dinoflagellates, and nanoflagellates and inhibiting cryptophytes. As the selective grazers also shift the grazing pressure on other species than cyanobacteria, changes in the structure and functioning of the Baltic Sea communities and ecosystems are likely to occur during the cyanobacterial bloom season.     

Nutrient Abatement Potential and Abatement Costs of Waste Water Treatment Plants in the Baltic Sea Region

We assess the physical potential to reduce nutrient loads from waste water treatment plants in the Baltic Sea region and determine the costs of abating nutrients based on the estimated potential. We take a sample of waste water treatment plants of different size classes and generalize its properties to the whole population of waste water treatment plants. Based on a detailed investment and operational cost data on actual plants, we develop the total and marginal abatement cost functions for both nutrients. To our knowledge, our study is the first of its kind; there is no other study on this issue which would take advantage of detailed data on waste water treatment plants at this extent. We demonstrate that the reduction potential of nutrients is huge in waste water treatment plants. Increasing the abatement in waste water treatment plants can result in 70 % of the Baltic Sea Action Plan nitrogen reduction target and 80 % of the Baltic Sea Action Plan phosphorus reduction target. Another good finding is that the costs of reducing both nutrients are much lower than previously thought. The large reduction of nitrogen would cost 670 million euros and of phosphorus 150 million euros. We show that especially for phosphorus the abatement costs in agriculture would be much higher than in waste water treatment plants.

Electronic supplementary material

The online version of this article (doi:10.1007/s13280-013-0435-1) contains supplementary material, which is available to authorized users.     

Microbial metagenomics in the Baltic Sea: Recent advancements and prospects for environmental monitoring

Metagenomics refers to the analysis of DNA from a whole community. Metagenomic sequencing of environmental DNA has greatly improved our knowledge of the identity and function of microorganisms in aquatic, terrestrial, and human biomes. Although open oceans have been the primary focus of studies on aquatic microbes, coastal and brackish ecosystems are now being surveyed. Here, we review so far published studies on microbes in the Baltic Sea, one of the world’s largest brackish water bodies, using high throughput sequencing of environmental DNA and RNA. Collectively the data illustrate that Baltic Sea microbes are unique and highly diverse, and well adapted to this brackish-water ecosystem, findings that represent a novel base-line knowledge necessary for monitoring purposes and a sustainable management. More specifically, the data relate to environmental drivers for microbial community composition and function, assessments of the microbial biodiversity, adaptations and role of microbes in the nitrogen cycle, and microbial genome assembly from metagenomic sequences. With these discoveries as background, prospects of using metagenomics for Baltic Sea environmental monitoring are discussed.     

Impact of Climate Change on Ecological Quality Indicators and Biogeochemical Fluxes in the Baltic Sea: A Multi-Model Ensemble Study

Multi-model ensemble simulations using three coupled physical-biogeochemical models were performed to calculate the combined impact of projected future climate change and plausible nutrient load changes on biogeochemical cycles in the Baltic Sea. Climate projections for 1961-2099 were combined with four nutrient load scenarios ranging from a pessimistic business-as-usual to a more optimistic case following the Helsinki Commission's (HELCOM) Baltic Sea Action Plan (BSAP). The model results suggest that in a future climate, water quality, characterized by ecological quality indicators like winter nutrient, summer bottom oxygen, and annual mean phytoplankton concentrations as well as annual mean Secchi depth (water transparency), will be deteriorated compared to present conditions. In case of nutrient load reductions required by the BSAP, water quality is only slightly improved. Based on the analysis of biogeochemical fluxes, we find that in warmer and more anoxic waters, internal feedbacks could be reinforced. Increased phosphorus fluxes out of the sediments, reduced denitrification efficiency and increased nitrogen fixation may partly counteract nutrient load abatement strategies.     

Denitrification in the river estuaries of the northern Baltic Sea

Estuaries have been suggested to have an important role in reducing the nitrogen load transported to the sea. We measured denitrification rates in six estuaries of the northern Baltic Sea. Four of them were river mouths in the Bothnian Bay (northern Gulf of Bothnia), and two were estuary bays, one in the Archipelago Sea (southern Gulf of Bothnia) and the other in the Gulf of Finland. Denitrification rates in the four river mouths varied between 330 and 905 micromol N m(-2) d(-1). The estuary bays at the Archipelago Sea and the Gulf of Bothnia had denitrification rates from 90 micromol N m(-2) d(-1) to 910 micromol N m(-2) d(-1) and from 230 micromol N m(-2) d(-1) to 320 micromol N m(-2) d(-1), respectively. Denitrification removed 3.6-9.0% of the total nitrogen loading in the river mouths and in the estuary bay in the Gulf of Finland, where the residence times were short. In the estuary bay with a long residence time, in the Archipelago Sea, up to 4.5% of nitrate loading and 19% of nitrogen loading were removed before entering the sea. According to our results, the sediments of the fast-flowing rivers and the estuary areas with short residence times have a limited capacity to reduce the nitrogen load to the Baltic Sea.     

Atmospheric Nutrient Input to the Baltic Sea from 1850 to 2006: A Reconstruction from Modeling Results and Historical Data

In this study, a consistent basin-wise monthly time series of the atmospheric nutrient load to the Baltic Sea during 1850-2006 was compiled. Due to the lack of a long time series (1850-1960) of nutrient deposition to the Baltic Sea, the data set was compiled by combining a time series of deposition data at the Baltic Nest Institute from 1970 to 2006, published historical monitoring data and deposition estimates, as well as recent modeled Representative Concentration Pathways (RCP) emission estimates. The procedure for nitrogen compounds included estimation of the deposition in a few intermediate reference years, linear interpolation between them, and the decomposition of annual deposition into a seasonal deposition pattern. As no reliable monitoring results were found for the atmospheric deposition of phosphorus during the early period of our study, we used published estimates for the temporal and spatial pattern of the phosphorus load.     

Interannual variability of phyto-bacterioplankton biomass and production in coastal and offshore waters of the Baltic Sea

The microbial part of the pelagic food web is seldom characterized in models despite its major contribution to biogeochemical cycles. In the Baltic Sea, spatial and temporal high frequency sampling over three years revealed changes in heterotrophic bacteria and phytoplankton coupling (biomass and production) related to hydrographic properties of the ecosystem. Phyto- and bacterioplankton were bottom-up driven in both coastal and offshore areas. Cold winter temperature was essential for phytoplankton to conform to the successional sequence in temperate waters. In terms of annual carbon production, the loss of the spring bloom (diatoms and dinoflagellates) after mild winters tended not to be compensated for by other taxa, not even summer cyanobacteria. These results improve our ability to project Baltic Sea ecosystem response to short- and long-term environmental changes.     

Tradeoffs between environmental goals and urban development: the case of nitrogen load from the Stockholm County to the Baltic Sea

Urban dwellers depend on the generation of ecosystem services for their welfare. The city of Stockholm is growing, and a 25% increase in population is projected by 2030. The effects of urban development were estimated through the quantification of nitrogen (N) leakage to the Baltic Sea under two urban development scenarios. We found that total net N load will increase by 6% or 8%, depending on which growth scenario is applied, and population increase by itself will contribute at least 15% of the point source N leakage. Technical improvements in sewage treatment could, according to our results, decrease total N load to the Baltic Sea by 4%. Based on our results, we conclude that proactive measures such as spatial urban planning can provide a constructive tool for sustainable urban development on regional as well as national and international scales, depending on geographical context as well as the ecosystem services' scale of operation.     

Brominated phenols,anisoles, and dioxins present in blue mussels from the Swedish coastline

Introduction  

Naturally occurring hydroxylated polybrominated diphenyl ethers (OH-PBDEs), their methoxylated counterparts (MeO-PBDEs), and polybrominated dibenzo-p-dioxins (PBDDs), together with their potential precursors polybrominated phenols (PBPs) and polybrominated anisoles (PBAs), were analyzed in blue mussels (Mytilus edulis) gathered along the east coast (bordering the Baltic Sea) and west coast of Sweden (bordering the North Sea). Brown algae (Dictyosiphon foenicolaceus) and cyanobacteria (Nodularia spumigena) from the Baltic Sea, considered to be among the primary producers of these compounds, were also analyzed for comparison.     

Baltic Sea management: Successes and failures

Severe environmental problems documented in the Baltic Sea in the 1960s led to the 1974 creation of the Helsinki Convention for the Protection of the Marine Environment of the Baltic Sea Area. We introduce this special issue by briefly summarizing successes and failures of Baltic environmental management in the following 40 years. The loads of many polluting substances have been greatly reduced, but legacy pollution slows recovery. Top predator populations have recovered, and human exposure to potential toxins has been reduced. The cod stock has partially recovered. Nutrient loads are decreasing, but deep-water anoxia and cyanobacterial blooms remain extensive, and climate change threatens the advances made. Ecosystem-based management is the agreed principle, but in practice the various environmental problems are still handled separately, since we still lack both basic ecological knowledge and appropriate governance structures for managing them together, in a true ecosystem approach.     

Future Nutrient Load Scenarios for the Baltic Sea Due to Climate and Lifestyle Changes

Dynamic model simulations of the future climate and projections of future lifestyles within the Baltic Sea Drainage Basin (BSDB) were considered in this study to estimate potential trends in future nutrient loads to the Baltic Sea. Total nitrogen and total phosphorus loads were estimated using a simple proxy based only on human population (to account for nutrient sources) and stream discharges (to account for nutrient transport). This population-discharge proxy provided a good estimate for nutrient loads across the seven sub-basins of the BSDB considered. All climate scenarios considered here produced increased nutrient loads to the Baltic Sea over the next 100 years. There was variation between the climate scenarios such that sub-basin and regional differences were seen in future nutrient runoff depending on the climate model and scenario considered. Regardless, the results of this study indicate that changes in lifestyle brought about through shifts in consumption and population potentially overshadow the climate effects on future nutrient runoff for the entire BSDB. Regionally, however, lifestyle changes appear relatively more important in the southern regions of the BSDB while climatic changes appear more important in the northern regions with regards to future increases in nutrient loads. From a whole-ecosystem management perspective of the BSDB, this implies that implementation of improved and targeted management practices can still bring about improved conditions in the Baltic Sea in the face of a warmer and wetter future climate.     

Management options and effects on a marine ecosystem: assessing the future of the Baltic

We are using the coupled models in a decision support system, Nest, to evaluate the response of the marine ecosystem to changes in external loads through various management options. The models address all the seven major marine basins and the entire drainage basin of the Baltic Sea. A series of future scenarios have been developed, in close collaboration with the Helsinki Commission, to see the possible effects of improved wastewater treatment and manure handling, phosphorus-free detergents, and less intensive land use and live stocks. Improved wastewater treatment and the use of phosphorus-free detergents in the entire region would drastically decrease phosphorus loads and improve the marine environment, particularly the occurrence of cyanobacterial blooms. However, the Baltic Sea will remain eutrophic, and to reduce other effects, a substantial reduction of nitrogen emissions must be implemented. This can only be obtained in these scenarios by drastically changing land use. In a final scenario, we have turned 50% of all agricultural lands into grasslands, together with efficient wastewater treatments and a ban of phosphorus in detergents. This scenario will substantially reduce primary production and the extension of hypoxic bottoms, increase water transparency in the most eutrophied basins, and virtually eliminate extensive cyanobacterial blooms.     

The potential future contribution of shipping to acidification of the Baltic Sea

International regulation of the emission of acidic sulphur and nitrogen oxides from commercial shipping has focused on the risks to human health, with little attention paid to the consequences for the marine environment. The introduction of stricter regulations in northern Europe has led to substantial investment in scrubbers that absorb the sulphur oxides in a counterflow of seawater. This paper examines the consequences of smokestack and scrubber release of acidic oxides in the Baltic Sea according to a range of scenarios for the coming decades. While shipping is projected to become a major source of strong acid deposition to the Baltic Sea by 2050, the long-term effect on the pH and alkalinity is projected to be significantly smaller than estimated from previous scoping studies. A significant contribution to this difference is the efficient export of surface water acidification to the North Sea on a timescale of 15–20 years.     

Heterogeneity of nodularin bioaccumulation in northern Baltic Sea flounders in 2002

The cyanobacterial hepatotoxin nodularin is abundantly produced by the cyanobacterium Nodularia spumigena in the Baltic Sea during July-August. Nodularin is a potent hepatotoxin and a tumour promoter, distributed in various Baltic Sea environmental compartments, especially food webs involving mussels. Flounders receive nodularin through consumption of blue mussels. In this study nodularin concentrations in individual flounders (liver) were examined between July and September 2002 (six sample sets, four to 10 samples/set), providing information about contribution of sampling on estimates of bioaccumulation intensity. Toxin was determined using liquid chromatography/mass spectrometry (LC/MS) and enzyme-linked immunosorbent assay (ELISA). Additionally, liver histopathology was examined. Observed toxin concentrations were ND-390 microg kg(-1) dw (LC/MS) and 20-2230 microg kg(-1) dw (ELISA), with maximum concentrations in September (ELISA). The ELISA protocol generally resulted in higher, up to approximately 10-fold, toxin concentrations than LC/MS, with increasing difference toward September. This difference may have originated from different extraction solvents in LC/MS and ELISA, ion suppression in LC/MS, and temporal increase in nodularin metabolites detectable with ELISA. The differences in toxin concentrations between individual liver samples were considerable with relative standard deviation values of 20-154% (LC/MS) and 28-106% (ELISA). Since the precision of the ELISA method employed was <25% and that of LC/MS <10%, it can be concluded that the largest source of error in bioaccumulation estimates may be an inadequate number of samples. Although there were tissue lesions in several liver samples, occurrence of lesions was not related to toxin concentrations.