Final publishable summary report BONUS COCOA PROJECT. Objectives and expected results from BONUS COCOA project

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1 BONUS COCOA PROJECT Actual submission date: 28 February 2018 Period covered: 1 January December 2017 Objectives and expected results from BONUS COCOA project The overall objective of BONUS COCOA was to identify the major pathways of nutrients and organic material across the diversity of Baltic coastal ecosystems, covering river-dominated estuaries, lagoons, archipelagos, and embayments with restricted water exchange. BONUS COCOA was expected to 1) improve current understanding of the transformations of the nutrient cocktail (C/N/P/Si) across the land-sea continuum, 2) quantify the processes that transform and accumulate these elements, 3) estimate nutrient retention across coastal ecosystems, 4) investigate potential feed-back processes leading to alternative stable states, 5) analyse how nutrient processing may have changed over time, 6) evaluate consequences of altered nutrient pathways on ecosystem services, and 7) identify possible management responses for present and future projections. A major aim was to advance our present understanding of how biology modulates biogeochemical cycles from experimental studies and scale up this information at the level of the coastal ecosystem through modelling. Ultimately, BONUS COCOA aimed at quantifying the importance of nutrient retention along the Baltic Sea coastal rim. Work carried out in the project Sampling campaigns have been carried out at seven learning sites. Roskilde Fjord (DK), Puck Bay (PL), Curonian Lagoon(LT), and Tvärminne (FI) have been intensively studied over multiple years and seasons, because these sites were in the vicinity of partner institutions facilitating frequent sampling. The Vistula plume (PL), Eastern Gulf of Finland (RU), Öre River Estuary (SE) and Stockholm Archipelago (SE) were sampled on fewer occasions, but these specific campaigns included more intense spatial sampling involving several partners covering different expertise. The four more frequently sampled learning sites have, in addition to the more continuous monitoring, also had some more intensive campaigns. Nutrient and oxygen fluxes at the sediment-water interface have been measured in collaborative efforts between several partners, ensuring a large degree of consistency and high quality of the measurements. In Roskilde Fjord, three campaigns have been carried out to measure nutrient fluxes in eelgrass meadows and compare these with fluxes from neighbouring bare sandy and muddy

2 sediments. In Tvärminne, experiments have been carried out to measure nutrient fluxes in relation to different macrofaunal manipulations, and the eelgrass experiment from Roskilde Fjord was replicated. Benthic-pelagic fluxes have measured during several campaigns in Curonian Lagoon, and the potential effect of microphytobenthos and benthic bioturbating fauna was studied. A bioturbation experiment with chironomid larvae in soft sediments and an incubation experiment with zebra mussel (Dreissena polymorpha) were carried out. In Puck Bay, nutrient fluxes were investigated in relation to macrofaunal diversity and traits by sampling across gradients, from shallow sandy sediments towards deeper muddy sediments with low oxygen. Long-term sediment traps were deployed for one year in Puck Bay to characterise the quantity and quality of sinking organic particles. In the Eastern Gulf of Finland, focus was on studying the effect of the invasive polychaete species Marenzelleria arctia for bioturbating sediments and enhancing water-sediment fluxes. This learning site was affected by upwelling hypoxic bottom water following the Major Baltic Inflow in December Nitrification and denitrification rates were measured across different sediment types and nutrient Figure 1: Sampling with the GEMAX corer at Tvärminne in Finland. Photo: Dana Hellemann, University of Helsinki. concentrations in Öre River Estuary, Vistula plume and Tvärminne (Fig. 1). Phosphorus sorption has been studied in Öre River Estuary and the Vistula plume. Dissolved Organic Carbon and optical fingerprints of Dissolved Organic Matter (DOM) has been measured in sediments pore water and bottom waters in Roskilde Fjord, Öre River Estuary, Puck Bay, Curonian Lagoon and Tvärminne. Gradients of DOM quantity and quality have been studied for Roskilde Fjord and Tvärminne. An experiment for examining the potential exudation of DOM from phytoplankton was carried out in Roskilde Fjord, and a high-frequency monitoring program (almost daily samples) of phytoplankton, nutrients and respiration measurements from a pier in Roskilde Fjord was also carried out. Finally, sediment cores have been sampled in Roskilde Fjord, Curonian Lagoon, Stockholm Archipelago and Puck Bay for measuring sedimentation rates of C/N/P/Si, using 210 Pb and 137 Cs for dating. The above-mentioned experimental and sampling activities at the learning sites provides a nonexhaustive overview of the diversity of data collection carried out in BONUS COCOA. Existing simulation models with coupled hydrodynamic-biogeochemical processes have been extended with process modules for macrofauna, macrophyte and microphytobenthic primary producers (Fig. 2). Complex process formulations for feeding, irrigation and particle mixing activity by benthic fauna as well as production/respiration of benthic primary producers were incorporated in the models, and sensitivity analyses were used to assess the impact on nutrient fluxes and denitrification. These advances models, with different components, have been calibrated for Roskilde Fjord, Curonian Lagoon, Eastern Gulf of Finland, Öre River Estuary, Vistula plume (including Puck Bay) and Stockholm Archipelago. Furthermore, the Swedish coastal zone model (SCM) has been set up for all water bodies along the Swedish coast, and estimates of nitrogen and phosphorus retention have been calculated. A one-dimensional (1-D) model was calibrated for Tvärminne, as the hydrography of the archipelago area posed a major challenge. These model improvements have been used to investigate the potential effects of different biological components in the coastal ecosystems.

3 Fauna Primary producers Final publishable summary report 1. Nutrient uptake 1. Oxygen production Biomass production, retention 2. Sediment stabilization, enhanced sedimentation 3. Filtration (uptake) 4. Biodeposition (egestion) 5. Nutrient excretion 5. Respiration Biomass production, retention 6. Bioturbation 7. Bioirrigation Figure 2: Biological components and processes affecting the biogeochemical cycles in coastal ecosystems. These components and processes have been added to existing biogeochemical models. From D5.2 and Ehrnsten et al. (in prep.). The existing national definitions of water bodies for the European Water Framework Directive (WFD) have been combined with geographical information on bathymetry, sediment characteristics and physical exposure as well as monitoring data on nutrient inputs and physical, chemical and biological monitoring variables. Furthermore, boundary conditions for physical and chemical variables have been calculated from an open-water hydrodynamic-biogeochemical model (RCO-SCOBI). This information has been used to categorise 1068 coastal ecosystems into different types, for extrapolating results from well-studied systems to understudied or even unstudied coastal ecosystems. Denitrification rates and phosphorus burial rates from published literature, unpublished data from past projects and from BONUS COCOA have been analysed in combination with this categorisation to assess the removal of nitrogen and phosphorus in different coastal ecosystem types. Gradients in nutrients, organic matter, and the carbonate system from land to sea have been investigated from combining freshwater and marine monitoring data, using deviations from conservative mixing to assess possible sources and sinks in the coastal zone. The development and testing of measurement techniques in BONUS COCOA has been used to propose indicators of ecosystem function. The categorisation of WFD water bodies using common criteria across all countries was used to test the relevance of current national WFD intercalibration types and suggest possible improvements. The improved understanding of nutrient removal in the coastal zone has been used to assess consequences for HELCOMs nutrient reduction scheme in the Baltic Sea Action Plan (BSAP), particularly denitrification in the major lagoons. Finally, BONUS COCOA has addressed the effect of projected future changes in nutrient loads and climate forcing on the filtering capacity of the coastal zone during the coming century, through transient scenario simulations with high coastal resolution performed in the Stockholm Archipelago. Main results achieved during the project During the four years of the project, BONUS COCOA has produced 40 deliverables, including 5 status reports; 66 articles have been published, 17 manuscripts are currently under review and several additional manuscripts are in preparation for submission. Many of the papers have been published in high-ranked

4 journals, including Science, Nature Geoscience, Nature Climate Change, Trends in Ecology & Evolution, Biological Reviews, Global Change Biology, Science Advances, Limnology & Oceanography, and Environmental Science & Technology. Moreover, COCOA partners have presented their results at numerous conferences and disseminated their knowledge to policy makers at various stakeholder meetings. Scientific highlights from BONUS COCOA are (numbers link to project objectives listed above): Denitrification in the oligotrophic coastal areas of the northern Baltic Sea is generally limited by organic carbon in spring and nitrate availability in summer. Coupled nitrification-denitrification appears to the most important pathway for N removal (Hellemann et al. 2017; #1,2). Chemolithoautotrophs fractionate N and O isotopes differently from heterotrophic denitrifiers. The importance of this group can explain observed fractionation of nitrate (Frey et al. 2015; #1). Episodic cyanobacterial blooms, a prominent features of the brackish Curonian Lagoon, cause high sedimentation of organic matter, but most of the nitrogen fixed by the cyanobacteria is released back to the water column as dissolved organic nitrogen and only a minor fraction is denitrified (Zilius et al. 2016; #1,2,6,7). Sediments with high reactive Mn pools can buffer the effects of phosphate release during short-term events of anoxia, which are observed in shallow and highly productive coastal lagoons such as the Curonian Lagoon (Zilius et al. 2015; #1,2). Sedimentation fluxes of Si can be high and variable in coastal areas, but approximately half of the flux is released back into the water column with the highest rates in summer and lowest in early spring. This internal Si recycling sustains continued diatom blooms in coastal ecosystems (Tallberg et al. 2017; #1,2). The coastal zone significantly alters the composition of DOM along the salinity continuum, but residence time alone cannot explain deviations from conservative mixing. Variability in freshwater end-member add complexity to mixing relationships (Asmala et al. 2015; #1,2). Phytoplankton-derived DOM changes seasonally, most likely due to shifts from phosphorus to nitrogen limited growth, demonstrating the environmental conditions regulate DOM pathways (Asmala et al. 2018; #1,2). Sediment resuspension varies significantly in relation to abiotic sediment properties as well as biota inhabiting the sediments. The clam Macoma balthica stabilise the sediment surface, but destabilise the sediment sub-surface. Compacted sediments are more resistant to erosion, which has repercussions for the internal nutrient inputs to the water column (Joensuu et al. 2018; #1,4). Irrigation carried out by the invasive species Marenzelleria arctia increases oxygenation of the sediments causing enhanced sediment phosphorus retention in the Eastern Gulf of Finland (Isaev et al. 2017; #1,2,4). Marenzelleria and other macrofauna species could account for up to 92% of the variation in the sediment-water fluxes. Oxygen and nutrient fluxes were higher in summer and low in winter, and the seasonal variability is important for assessing nutrient budgets and model calibration (Kauppi et al. 2017; #2,4,6,7). Chironomid larvae are bioturbators in brackish sediments, but their effect on nutrient fluxes appears to be element specific, with smaller increases on N and P fluxes and stimulated inorganic Si regeneration (Benelli et al. 2018; #1,2). Biodiversity of benthic macrofauna has also an impact on ecosystem function. The combination of macrofauna abundance, biomass and diversity could explain changing solute fluxes in the Finnish Archipelago (Gammal et al. 2016; #2,4,6,7). Benthic plant communities have varying effects on ecosystem functioning, but their effect on nutrient fluxes is understudied. An experiment at Tvärminne showed that fluxes of inorganic nitrogen did not change in the presence of plants (nine different species), but the aquatic plants enhanced the flux of dissolved organic nitrogen (Gustafsson & Norkko 2016; #1,2,6).

5 Sediment burial of macroalgae contribute significantly to carbon sequestration in coastal environments, which has largely been overlooked (Krause-Jensen & Duarte 2016; #2,6). The large Stockholm Archipelago is an efficient filter for both N and P, removing 72% and 65% of N and P input from land. Nitrogen was mainly removed by benthic denitrification (92%), whereas burial (8%) and pelagic denitrification (1%) contributed relatively less (Almroth-Rosell et al. 2016; #2,3,4,5,7). Sedimentation and respiration of organic material following cyanobacteria blooms in the Curonian Lagoon enhances the release of phosphate from sediments. The internal P input can be of similar magnitude as P input from land, but it is highly variable across years (Petkuviene et al. 2016, Vybernaite-Lubiene et al. 2017; #2,3,4); The efficiency of the coastal filter is highly variable, but coastal lagoons are relatively effective in removing nitrogen whereas archipelagos are efficient in trapping phosphorus. Phosphorus burial is tightly linked to sedimentation rates. Across the entire Baltic Sea, the coastal filter removes approximately 16% of nitrogen and 53% of phosphorus inputs from land (Asmala et al. 2017; #2,3,7). Coastal hypoxia was also a prominent feature in different periods during the Holocene, although mainly associated with warming periods and altered hydrophysical forcing after the post-glacial rebound (Ning et al. 2016; van Helmond et al. 2017; #5). Changes in the composition of nutrient effluents from wastewater treatment plants has large effects on the receiving coastal water body. Dissolved organic nitrogen stimulates bacterial production more than phytoplankton growth, whereas dissolved inorganic nitrogen changes this pattern. Managing WWTP effluents has consequences for the autotrophy/heterotrophy of coastal ecosystems (Vaquer- Sunyer et al. 2016; #6,7). Biological responses of coastal ecosystems to reduced nutrient inputs are characterised by nonlinearity, delays and memory effects that slow down or even prevent (in case of hypoxia) recovery (Riemann et al. 2017; #4,5,7). Coastal ecosystems experiencing reduced nutrient inputs, such as Roskilde Fjord, typically display a combination of fast and slow responses in ecosystem metabolism, involving higher net autotrophy by expanding benthic primary producers (Staehr et al. 2017; #3,4,5,6,7). The results from BONUS COCOA has had a strong scientific impact on our understanding of the coastal zone as a biogeochemical reactor and the importance of benthic vegetation and fauna for stimulating nutrient removal processes and other associated ecosystem services. The project has established a better overview of the broad ranges in various biogeochemical processes across the different types of coastal ecosystems as well as different types of biological habitats. These quantitative estimates of biogeochemical processes has improved current models for the coastal zone. The results from BONUS COCOA has had a substantial impact on environmental policies by ensuring that management decisions are based on a scientifically informed basis. This applies specifically to strong engagement in policy discussions on geoengineering approaches to mitigate coastal hypoxia. The project has contributed to improving status reporting through suggesting new and revising existing ecological indicators, adding information on nutrient and carbon pathways that have previously been disregarded despite the importance for assessing ecosystem functioning. BONUS COCOA has also emphasised the role of the coastal filter in relation to the BSAP, particularly the large nitrogen removal that occurs in coastal lagoons. Throughout the project, BONUS COCOA participants have been involved in various working groups under HELCOM, ICES and national environmental agencies to transfer state-of-the-art scientific knowledge into environmental policies. BONUS COCOA has advanced the use of new measurement technologies in coastal environments. The project has made use of a variety of high-frequency sensors and developed algorithms for processing such data. Techniques for measuring fluxes in sandy sediments and sediments inhabited by macrophytes have been

6 refined, extending our knowledge from deep dark muddy sediments to the majority of habitats in coastal environments. These advancements will be of great value in future marine spatial planning and the designation of coastal marine protected areas. The continuity plan of the project BONUS COCOA has improved our understanding of biogeochemical transformations and removal of C/N/P/Si in the coastal zone, but this improved understanding has opened new research questions that will be pursued in the future. Experiences from the project with new technologies will benefit the pursuit of these research questions. BONUS COCOA has established a collaborative network among key partners around the Baltic Sea that will be useful for addressing scientific and environmental policy challenges in the future. In the near future, BONUS COCOA will: Continue the legacy of BONUS COCOA through scientific publications. A total of 17 manuscripts are currently under review and additional manuscripts are in preparation. Key scientists from BONUS COCOA will produce a synthesis manuscript in A workshop has been planned for June BONUS COCOA partners are actively involved in upcoming BONUS Synthesis-projects utilizing information from several completed and ongoing BONUS projects. BONUS COCOA partners continue to be involved in stakeholder activities, including HELCOM and ICES working groups. New research initiatives have been developed and applied for at national and multi-national level. Some follow-up research projects have already been granted and the fate of other proposal is yet unknown. Acknowledgements BONUS COCOA project has received funding from BONUS (Art 185), funded jointly by the EU and national research funding agencies in Denmark (Innovation Fund Denmark), Finland (Academy of Finland), Germany (Forschungszentrum Jülich), Lithuania (Research Council of Lithuania), Poland (National Centre for Research and Development), Russia (Russian Foundation for Basic Research), and Sweden (Swedish Agency for Marine and Water Management, Swedish Environmental Protection Agency, Swedish Research Council).