Edited by: Xosé Anxelu G. Morán, King Abdullah University of Science and Technology, Saudi Arabia
Reviewed by: Samuli Korpinen, Finnish Environment Institute (SYKE), Finland; Angel Pérez-Ruzafa, University of Murcia, Spain
This article was submitted to Marine Ecosystem Ecology, a section of the journal Frontiers in Marine Science
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Eutrophication is one of the most important anthropogenic pressures impacting coastal seas. In Europe, several legislations and management measures have been implemented to halt nutrient overloading in marine ecosystems. This study evaluates the impact of freshwater nutrient control measures on higher trophic levels (HTL) in European marine ecosystems following descriptors and criteria as defined by the Marine Strategy Framework Directive (MSFD). We used a novel pan-European marine modeling ensemble of fourteen HTL models, covering almost all the EU seas, under two nutrient management scenarios. Results from our projections suggest that the proposed nutrient reduction measures may not have a significant impact on the structure and function of European marine ecosystems. Among the assessed criteria, the spawning stock biomass of commercially important fish stocks and the biomass of small pelagic fishes would be the most impacted, albeit with values lower than 2.5%. For the other criteria/indicators, such as species diversity and trophic level indicators, the impact was lower. The Black Sea and the North-East Atlantic were the most negatively impacted regions, while the Baltic Sea was the only region showing signs of improvement. Coastal and shelf areas were more sensitive to environmental changes than large regional and sub-regional ecosystems that also include open seas. This is the first pan-European multi-model comparison study used to assess the impacts of land-based measures on marine and coastal European ecosystems through a set of selected ecological indicators. Since anthropogenic pressures are expanding apace in the marine environment and policy makers need to use rapid and effective policy measures for fast-changing environments, this modeling framework is an essential asset in supporting and guiding EU policy needs and decisions.
Eutrophication is one of the most important anthropogenic pressures on coastal and estuarine waters (
Ecological models are powerful tools to address the complexity of these systems and highlight these relationships (
Several studies have used the E2EM framework to assess the impact of nutrient reduction or other stressors on HTL organisms and ecosystem functioning (
In particular we assess how changes in nutrient inputs and concentrations and consequently planktonic groups might impact the structure and function of the upper trophic levels of the food web. Classical food web theory suggests that nutrient enrichment affects the food web from the bottom-up along with top-down effects, through predation, controlling the biomass of all trophic levels of a system (
Our assessment follows MSFD descriptors (mainly the biodiversity related descriptors) and methodological standards, developed and agreed upon in the framework of European or international conventions (
The use of an ensemble of models is crucial to increase the reliability of model predictions, account for prediction uncertainty and better inform decision-makers about the range of effects of selected pressures/measures on biodiversity, ecosystems and their services in general (
The hydrodynamic-biogeochemical dynamics of the European seas resulting from different river scenarios have been simulated using an End to End Model called Modeling Framework (MF), developed at the European Commission by its science Directorate-General (DG), the Joint Research Centre (JRC). The MF consists of coupled (either offline or online) hydrological, hydrodynamic-biogeochemical, and food-web models (
The MF has been designed to simulate changes in the state of European marine ecosystems and derived services in response to different pressures and management scenarios with the overall goal of providing explicit support to the decision-making process. In particular, in relation to eutrophication, the MF has investigated two realistic nutrient management scenarios, following measures reported and suggested by Member States within the WFD implementation plans. The two scenarios covering inland water quantity and quality (nutrients) in Europe include: (1) actual nutrient loads from river discharge (reference scenario, REF) and (2) maximum technically feasible reduction (MTFR scenario) of nutrient input to surface water. The nutrient reductions can be achieved by, e.g., keeping the nutrient surplus in agricultural areas to a minimum, optimizing mineral fertilizer applications and upgrading waste water treatments to the highest level of nutrient removal (
The water flow and the effectiveness of measures for preventing water scarcity were simulated by the LISFLOOD model (
The MTFR scenario comprised increased water use efficiency in irrigation and domestic usage, changes in cooling water requirements and the implementation of wastewater re-use for irrigation (
The LTL module consisted of 3D hydrodynamic-biogeochemical models representing the four main MSFD regions (Mediterranean Sea, Black Sea, Baltic Sea and North East Atlantic). Details of the hydrodynamic-biogeochemical models can be found in
The HTL European marine ecosystems, HTL model type, acronym and HTL spatial extent (ranges of latitude and longitude), which was used to extract LTL models outputs (details in
Mediterranean: West | EwE (West_JRC/West_ICM) | 35.1–44.4°N and −5.9 to 16.2°E | −13.6 | −35.7 | −0.1 | −0.2 | −0.1 |
Mediterranean: West | Osmose (West_OSM) | 35.1–44.4°N and −5.9 to 16.2°E | −13.6 | −35.7 | −0.2 | −0.4 | −0.03 |
Mediterranean: Adriatic | EwE (Adri_JRC) | 39.7–45.8°N and 12.1–20.0°E | −21.8 | −28.6 | −0.5 | −3.4 | −1.5 |
Mediterranean: Adriatic | Osmose (Adri_OSM) | 39.7–45.8°N and 12.1–20.0°E | −21.8 | −28.6 | −2.6 | −4.5 | −2.2 |
North-East Adriatic Sea | EwE (NE_Adri) | 45.4–46.0°N and 13.0–14.0°E | −22.4 | −36.7 | −13.0 | −6.6 | −4.8 |
Mediterranean: Ionian | EwE (Ion_JRC) | 30.3–40.5°N and 10.0–24.1°E | −31.8 | −46.3 | 0.2 | −0.3 | −0.1 |
Mediterranean: Ionian | Osmose (Ion_OSM) | 30.3–40.5°N and 10.0–24.1°E | −31.8 | −46.3 | −0.2 | −0.3 | −0.09 |
Inner Ionian Archipelago | EwE (IIA) | 38.1–38.8°N and 20.5–21.1°E | −26.6 | −25.1 | −0.9 | −0.9 | −0.7 |
Mediterranean: Eastern | EwE (East_JRC) | 30.8–41.1°N and 22.2–36.2°E | −2.0 | −4.0 | 0.1 | −0.2 | −0.1 |
Mediterranean: Eastern | Osmose (East_OSM) | 30.8–41.1°N and 22.2–36.2°E | −2.0 | −4.0 | −0.2 | −0.2 | −0.06 |
Thermaikos Gulf | EwE (ThermG) | 39.9–40.4°N and 22.5–23.3°E | −27.0 | −30.7 | −1.9 | −0.6 | −0.5 |
Black Sea | EwE (Black) | 40.9–46.9°N and 27.4–41.8°E | −10.4 | −9.3 | −20.3 | 6.5 | −3.4 |
Baltic Proper | EwE (Baltic) | 54.1–60.5°N and 14.2–23.5°E | −8.6 | −13.7 | −1.7 | −0.2 | −0.3 |
North Sea | EwE (NorthS) | 50.8–57.5°N and −3.5 to 9.0°E | −19.2 | −27.6 | −10.2 | −8.7 | −2.9 |
Eastern English Channel | Atlantis (EnglishC_ATL) | 49.3–51.0°N and −2.1 to 2.0°E | −13.7 | −17.7 | −8.8 | −6.3 | −1.1 |
Eastern English Channel | Osmose (EnglishC_OSM) | 48.9–51.3°N and −2.1 to 2.6°E | −13.9 | −17.9 | −8.9 | −6.4 | −1.1 |
Celtic Sea | EwE (Celtic) | 48.0–52.5°N and −11.8 to −1.4°E | −17.7 | −21.6 | −2.1 | −1.5 | −0.3 |
Irish Sea | EwE (Irish) | 52.0–55.1°N and −7.6 to −2.9°E | −19.6 | −25.8 | −12.3 | −10.8 | −2.0 |
West Coast of Scotland | EwE (WScot) | 54.5–60.3°N and −10.5 to −4.0°E | −20.1 | −17.3 | −4.0 | −2.9 | −0.7 |
In addition, an example of the spatial output scenarios produced by the hydrological and hydrodynamic-biogeochemical models for the Mediterranean Sea, and integrated for the assessed period (2005–2012), is presented in
Fourteen HTL models were used to run the nutrient management scenarios, all covering either full MSFD regions, sub-regions, or smaller zones within single MSFD areas (
Map showing the location and spatial extent of the 14 ecosystems models included in the analysis. Light-blue background and Arabic numbers correspond to MSFD regions and sub-regions (1 = Mediterranean Sea; 2 = Black Sea; 3 = Baltic Sea; 4 = North Sea; 5 = Celtic Seas) while dashed background and Roman numbers refer to smaller areas within an MSFD region/sub-region (I = Western Mediterranean; II = North-East Adriatic; III = Inner Ionian Archipelago; IV = Thermaikos Gulf; V = Baltic Proper; VI = North Sea; VII = English Channel; VIII = Celtic Sea; IX = Irish Sea; X = West Coast of Scotland).
To run the nutrient simulations, each HTL model was forced with specific environmental output from the REF and MTFR scenarios of the MF hydrodynamic-biogeochemical module covering the 2005–2012 period. Each scenario was run separately by the individual HTL models using the 8-years (2005–2012) simulations from the LTL models as “forecast” scenarios (
To assess the impact of the nutrient management scenarios, a set of criteria from MSFD Descriptor 3 (D3: Commercially exploited species) and Descriptor 4 (D4: Food webs) were used. In particular, we chose criteria and species that would likely have a direct response to these scenarios, such as small pelagic fishes (e.g., herrings, sardines, anchovies) bottom-up controlled by primary production, and criteria that would be able to capture changes within the food web (e.g., species diversity). To be able to compare output across regions and models, we selected criteria common to most of the models (
List of selected descriptors/criteria as defined by the MSFD (2017/848/EC) together with the modeled derived indicators (MDI), definitions and references.
D3 Commercially exploited fish and shellfish | Spawning stock biomass of one commercial species within the small pelagic group | Species belonging to the Clupeidae family. See |
|
D4 Food webs | Species diversity index | Expresses species diversity by considering the biomass of those organisms with trophic levels 3 or higher ( |
|
Small pelagic fish biomass | Commercial and non- commercial small pelagic planktivorous fishes (total length < 30 cm; classification extracted from Fishbase; |
In addition to the MSFD criteria, two other indicators were assessed to test if nutrient scenarios would have an impact on the trophic structure of the ecosystems. These include the trophic level (TL) of the community, excluding TL < 2 (
where
where
Modeled criteria and indicators (I) were extracted annually (for the 8 years of simulations) for each HTL model and for both REF and MTFR scenarios. The relative mean change between these scenarios was calculated as:
and presented per descriptor-criterion/TL indicator and per model. For D3 the scale of assessment required by the GES (Good Environmental Status) Decision (
Only six of the HTL models used in this assessment had a spatial component; of these, three were built for the Mediterranean Sea, two covering the entire basin and one set up for the Western Mediterranean Sea (
Finally, coherence maps were created for the three indicators (the small pelagic fishes [D4C2] and the TLs) common to the models to evaluate the coherence of the projections. Trends of relative changes were compared per grid cell and per model, looking at the signs, indicating whether an increase (or decrease) in the selected indicator occurred under the MTFR scenario. The percentage of coherence was calculated for the whole sub-basin, the shelves (<200 m) and open waters (>200 m).
The scenario outputs showed differences between and commonalities among models, criteria, size and locations (
Box plots representing the mean change (%) and standard deviation between MTFR and REF scenario for the selected MSFD criteria:
Species diversity (D4C1) did not show a significant change (
Overall, the TL indicators did not show clear changes between the two nutrient scenarios (
Box plots representing the mean change (%) and standard deviation for TL indicators:
The spatial outputs produced by the HTL models for the two scenarios in the Western Mediterranean Sea highlighted differences and commonalities among models, criteria/indicators, and between the whole subregion, shelf areas and open waters (
Maps representing the mean change (%) for the Spawning stock biomass of a commercially important small pelagic fish (D3C2) per GSA (# 1. Northern Alboran Sea; 2. Alboran Island; 3. Southern Alboran Sea; 4. Algeria; 5. Balearic Islands; 6. Northern Spain; 7. Gulf of Lion; 8. Corsica; 9. Ligurian and Tyrrhenian Seas; 10. South and Central Tyrrhenian; 11.1. Sardinia West; 11.2. Sardinia East; 12. Northern Tunisia) and per model type.
Maps representing the mean change (%) for the Small pelagic fish biomass (D4C2) per model type. Mean values were calculated considering the whole Western sub-region, shelves (<200 m) and open waters (>200 m). Note that the color scale of D4C2_OSM is different from the one of D4C2_EwE_JRC/ICM.
The species diversity index (D4C1) (
The spatial coherence for the small pelagic fish biomass was heterogeneous for the whole sub-region with an approximate equal percentage of decrease (45%) and increase (55%) (
Coherence map for Small pelagic fish biomass (D4C2) which shows where all or most models (2 out of three) agree on the relative change trend.
The West_OSM and West_ICM models suggested a slight increase of both trophic level indicators (
Maps representing the mean change (%) for the Mean trophic level of the community (mTLco) per model type. Mean values were calculated considering the whole Western sub-region, shelves (<200 m) and open waters (>200 m). Note that the color scale of mTLco_EwE_JRC is different from the one of mTLco_EwE_ICM and mTLco_OSM.
The spatial coherence for the mTLco was extremely heterogeneous for all the areas (the whole sub-region, shelves and open waters). Here, 55% of the grid cells were associated with a decrease in mTLco while 45% were associated with an increase (
This study provides a first pan-European assessment of the impact of nutrient management scenarios on marine ecosystems and related marine resources. The reduction of nutrients from river run-off showed no substantial changes in the structure and function of the HTL ecosystem models included. From a regional MSFD perspective, the mean change of SSB of commercially important small pelagic fish species (D3C2) and small pelagic fish biomass (D4C2) showed the highest decrease if only with values below 2.5%. Interestingly, all the available models confirmed a decline in the biomass of commercial small pelagic fish species among the main MSFD regions, suggesting that a reduced primary production as a result of nutrient reductions (
This phenomenon has already been observed in other systems as shown by
When looking at the biomass of commercial stocks and non-commercial small pelagic fish species, the pattern was similar to the mean change of SSB of commercially important stocks (D3C2), but with larger variability across regions/sub-regions/small areas within an MSFD region. Variability across models might be related to the structure of the available models (e.g., some models might have more commercially important small pelagics than non-commercial species, or
For species diversity (D4C1), no clear responses were observed at a regional or sub-regional scale, except in the Baltic Sea with a slight increase and in the North-East Adriatic Sea with a decrease in diversity. The Baltic Proper was the only area that showed a slight increase in the two food-web criteria compared to the reference scenario; this might be related to the highly eutrophic nature of this ecosystem and the fact that a reduction of nutrient inputs might lead to an improvement of the marine environment e.g., better bottom oxygen levels, as observed in
The reason why these systems responded differently to a reduction in nutrient load is probably because the level of eutrophication observed in the Baltic Sea is worse than in other regional seas, as shown also by
The size and location of the studied ecosystems are also important. Coastal and shelf areas are more sensitive to environmental changes than larger sub-regional or regional ecosystems, since the former are at the interface between land and sea, and are subjected to a variety of anthropogenic pressures (e.g., eutrophication, fishing pressure, pollutants;
The relative contribution of river input in the total provision of nutrients, and hence primary production in the marine environment, may also control to a large extent the intensity of impacts affecting the pelagic fish community. For instance, the larger decline in small pelagic fishes observed in the North Sea compared to the Celtic Sea might be the result of the North Sea having proportionally larger riverine discharges and greater levels of mixing (
However,
In addition, the stronger reduction in total nitrogen and phosphorus in the land-sea interface rather than in the dissolved nutrients at sea, [as shown in
The TL indices assessed in this study, the trophic level of the community (mTLco) and the trophic level of landed catches (TLc), showed little variation (depending on the scale considered) when applying these nutrient management measures.
In addition, the weak responses of some of the criteria/indicators to changes in nutrients might be due to the short time series of forcing data utilized in this assessment. It is well known that ecosystems that accumulated nutrients during eutrophication require long recovery times to see large effects of load changes on ecosystem dynamics (
It is also important to acknowledge that coastal processes are not well represented by the spatial models available here (which include both HTL and LTL models), e.g., the responses of species fished near the coast such as European seabass,
This study assessed the impact of changes in nutrient concentrations on the spatially explicit ecosystem model of the Western Mediterranean sub-region. Our analysis confirmed that coastal and shelf ecosystems will be the most impacted when nutrients are reduced. Two out of three models suggested a slight decrease, more or less pronounced depending on the model/area considered, along the coasts/shelves of the Western Mediterranean Sea. These results are in line with previous studies that showed how freshwater pollution control measures will not impact the NW Mediterranean marine ecosystem at large, given the relatively smaller importance of river-borne nutrients for the marine productivity in the area (
When inspecting change in the spawning stock biomass of European pilchard (D3C2) or the biomass of small pelagic fishes (D4C2), the two available spatial EwE models confirmed a slight decline along the continental shelf for both criteria and a marginal increase in open waters for small pelagic fishes. Yet, spatial differences were detected between the two models which could be related to the model structure and/or to the drivers used to spatially distribute the marine species and condition growth and consumption (such as changes in sea temperature). Ecosystem productivity, together with other environmental drivers such as temperature and salinity, are important factors affecting the distribution of small pelagic fishes (
Overall our study confirmed that spatial modeling is still a challenging component of HTL ecosystem approaches as previously shown (
This study investigated the effects of applied inland management measures that aim to reduce nutrient pollution in the marine environment. Using a broad set of HTL marine ecosystem models covering most of the European seas, this study was able to assess the response of these marine ecosystems to land-based measures using the criteria defined by the GES Decision (
Another important aspect where ecosystem models can support policy is in the setting of meaningful threshold/target values. As highlighted by
This study suggests that improved nutrient management, in line within European directives to preserve and/or recover the status of coastal and marine water status, will have little impact on the assessed HTL marine ecosystems. Riverine nutrient discharge, though, is just one of many stressors impacting our seas and further modeling studies should investigate the impact from synergistic and antagonistic stressors. Pressures like climate change, overfishing, chemical pollutants and plastics are expanding rapidly throughout the world (
In 2019, the United Nations (UN) declared the Decade on Ecosystem Restoration with the purpose of “recognizing the need to massively accelerate global restoration of degraded ecosystems, to fight the climate heating crisis, enhance food security, provide clean water and protect biodiversity on the planet” and in 2021, the UN Decade of Ocean Science for Sustainable Development will begin, aiming to “developing scientific knowledge, building infrastructure and fostering relationships for a sustainable and healthy ocean.” It is now time to utilize these modeling tools to better guide and support decisions making by managers and policy makers.
The original contributions presented in the study are included in the article/
CP developed the protocol, led the data analysis, plotting, and writing of the manuscript. BG provided riverine nutrient inputs. DM, EG-G, RF, SM, and OP provided nutrients and phytoplankton data at sea. All authors contributed to the writing of the article, provided model results and, discussions on the analysis.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The Supplementary Material for this article can be found online at:
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