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Development of indicators of ecosystem functioning in a temperate shelf sea: a combined fieldwork and modelling approach

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Abstract

A conceptual model of the main carbon and nitrogen flows through pelagic and benthic food webs was used to identify the key biogeochemical processes representing ecosystem functioning, and to select indicators of each of these processes. A combined fieldwork and modelling approach was used to provide the data required to evaluate the indicators in terms of their suitability for assessing and managing the impacts of climate change and demersal trawling. Four of our 16 proposed indicators (phytoplankton production and productivity, near-bed oxygen concentrations and oxygen penetration of the seabed) met the majority of criteria we used for evaluating indicators. Five indicators (depth of anoxic sediment, zoobenthos biomass, production, productivity and bioturbation potential) did not comply with sufficient criteria to be considered as good indicators. Six of our proposed indicators (zooplankton biomass, size structure, production and productivity; ecosystem productivity; ecosystem balance) could not be assessed for sensitivity and specificity using our models, and therefore need to be addressed in future work aimed at improving both the models and the fieldwork. Our results indicate that evaluation of indicators is difficult, because of the number and variety of human pressures which need to be considered in reality, and the interactions between these pressures and the ecosystem components which they affect. The challenge will be to establish if there are indeed any indicators which are able to meet the majority of criteria for good indicators in holistic ecosystem-based assessments.

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References

  • Allen JI, Holt JT, Blackford J, Proctor R (2007) Error quantification of a high-resolution coupled hydrodynamic-ecosystem coastal-ocean model: part 2. Chlorophyll-a, nutrients and SPM. J Mar Syst 68:381–404. doi:10.1016/j.jmarsys.2007.01.005

    Article  Google Scholar 

  • Andersen JH, Axe P, Backer H, Carstensen J, Claussen U, Fleming-Lehtinen V, Järvinen M, Kaartokallio H, Knuuttila S, Korpinen S et al (2010) Getting the measure of eutrophication in the Baltic Sea: towards improved assessment principles and methods. Biogeochemistry. doi:10.1007/s10533-010-9508-4

    Google Scholar 

  • Atkins JP, Burdon D, Elliott M, Gregory AJ (2011) Management of the marine environment: integrating ecosystem services and societal benefits with the DPSIR framework in a system approach. Mar Pollut Bull 62:215–226

    Article  Google Scholar 

  • Aubry A, Elliott M (2006) The use of Environmental Integrative Indicators to assess seabed disturbance in estuaries and coasts: application to the Humber Estuary, UK. Mar Pollut Bull 53(1–4):175–185

    Article  Google Scholar 

  • Avila TR, de Souza Machado AA, Bianchini A (2012) Estimation of zooplankton secondary production in estuarine waters: comparison between the enzymatic (chitobiase) method and mathematical models using crustaceans. J Exp Mar Biol Ecol 416–417:144–152

    Article  Google Scholar 

  • Barange M, O’Boyle R, Cochrane KL, De Moor CL, Fogarty MJ, Jarre A, Kell LT, King JR, Reid K, Sinclair M, Yatsu A (2010) Marine resources management in the face of change: from ecosystem science to ecosystem-based management. In: Barange M, Field JG, Harris RH, Hofmann E, Perry RI, Werner F (eds) Global change and marine ecosystems. Oxford University Press, Oxford, pp 253–283

    Chapter  Google Scholar 

  • Baretta JW, Ebenhöh W, Ruardij P (1995) The European Regional Seas Ecosystem Model, a complex marine ecosystem model. J Sea Res 33:233–246

    Article  Google Scholar 

  • Beaugrand G, Kirby R (2010) Climate, plankton and cod. Glob Change Biol 16:1268–1280

    Article  Google Scholar 

  • Birchenough SNR, Parker ER, Bolam SG (2012a) SPI-ing on the seafloor: assessing benthic systems with traditional and in situ observations. Biogeochemistry (under review)

  • Birchenough SNR, Parker ER, McManus E, Barry J (2012b) Combining bioturbation and redox metrics: potential tools for assessing seabed function. Ecol Ind 12:8–16. doi:10.1016/j.ecolind.2011.03.015

    Article  Google Scholar 

  • Bolam SG, Barrio Frojan CRS, Eggleton J (2010) Macrofaunal production along the UK continental shelf. J Sea Res 64:166–179

    Article  Google Scholar 

  • Borja Á, Dauer DM (2008) Assessing the environmental quality status in estuarine and coastal systems: comparing methodologies and indices. Ecol Ind 8:331–337

    Article  Google Scholar 

  • Borja Á, Bricker SB, Dauer DM, Demetriades NT, Ferreira JG, Forbes AT, Hutchings P, Jia X, Kenchingotn R, Marques JC, Zhu C (2008) Overview of integrative tools and methods in asssessing ecological integrity in estuarine and coastal systems worldwide. Mar Pollut Bull 56:1519–1537

    Article  Google Scholar 

  • Borja Á, Elliott M, Carstensen J, Heiskanen A-S, van de Bund W (2010) Marine management—towards an integrated implementation of the European Marine Strategy Framework and the Water Framework Directives. Mar Pollut Bull 60:2175–2186

    Article  Google Scholar 

  • Brander K, Botsford LW, Ciannelli L, Fogarty MJ, Heath MR, Planque B, Shannon LJ, Wieland K (2010). Human impacts on marine ecosystems. In: Marine ecosystems and global change. Oxford University Press, Oxford, pp. 41–71. ISBN 0199558027

  • Brandsma J, Martinez JM, Slagter H, Evans C, Brussaard C (2012). Summer distribution of microorganisms in the North Sea. Biogeochemistry (submitted)

  • Bricker SB, Ferreira JG, Simas T (2003) An integrated methodology for Assessment of Estuarine Trophic Status. Ecol Model 169:39–60

    Article  Google Scholar 

  • Bristow LA, Jickells T, Weston K, Marca-Bell A, Parker R, Andrews J (2012). Tracing estuarine organic matter sources into the southern North Sea using C and N isotopic signatures. Biogeochemistry. doi:10.1007/s10533-012-9758-4

  • Burchard H, Bolding K, Villareal MR (1999). GOTM—a general ocean turbulence model. Theory, applications and test cases. Technical report EUR 18745 EN, European Commission

  • Capuzzo E, Painting SJ, Forster R, Greenwood N (2012). Variability in the sub-surface light climate at ecohydrodynamically distinct sites in the North Sea. Biogeochemistry. doi:10.1007/s10533-012-9772-6

  • Cardoso AC, Cochrane S, Doerner H, Ferreira JG, Galgani F, Hagebro C, Hanke G, Hoepffner N, Keizer PD, Law R, Olenin S, Piet GJ, Rice J, Rogers SI, Swartenbroux F, Tasker ML, van de Bund J (2010) Scientific Support to the European Commission on the Marine Strategy Framework Directive—Management Group Report. EUR—Scientific and Technical Research Series. ISSN 1018-5593, EUR 24336 EN—Joint Research Centre

  • CEC (2008) DIRECTIVE 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive)

  • Collins M (2007) Ensembles and probabilities: a new era in the prediction of climate change. Philos Trans R Soc A 365:1957–1970. doi:10.1098/rsta.2007.2068

    Article  Google Scholar 

  • Conley DJ, Carstensen J, Ærtebjerg G, Christensen PB, Dalsgaard T, Hansen JLS, Josefson AB (2007) Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol Appl 17:165–184

    Article  Google Scholar 

  • Cooper KM, Barrio Froján CRS, Defew E, Curtis M, Fleddum A, Brooks L, Paterson DM (2008) Assessment of ecosystem function following marine aggregate dredging. J Exp Mar Biol Ecol 366:82–91

    Article  Google Scholar 

  • Couceiro F, Fones GR, Thompson CEL, Statham PJ, Sivyer DB, Parker R, Kelly-Gerreyn BA, Amos CL (2012) Impact of resuspension of cohesive sediments at the Oyster Grounds (North Sea) on nutrient exchange across the sediment–water interface. Biogeochemistry. doi:10.1007/s10533-012-9710-7

    Google Scholar 

  • Coughlan C, van der Molen J, Aldridge J, Parker R, Stephens D (2011) Marine Ecosystem Connections: essential indicators of healthy, productive and biologically diverse seas (contract ME3205). Report: impacts of climate variability and trawling on ecosystem dynamics: GIS and ERSEM model analysis. Milestone Report 5a, ME3205: 11/05a, Defra

  • Devlin M, Bricker S, Painting S (2011) Comparison of five methods for assessing impacts of nutrient enrichment using estuarine case studies. Biogeochemistry. doi:10.1007/s10533-011-9588-9

    Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. doi:1126/science.1156401

    Article  Google Scholar 

  • Dulvy NK, Jennings S, Rogers SI, Maxwell DL (2006) Threat and decline in fishes: an indicator of marine biodiversity. Can J Fish Aquat Sci 63:1267–1275. doi:10.1139/F06-035

    Article  Google Scholar 

  • Elliott M (2011) Marine science and management means tackling exogenic unmanaged pressures and endogenic managed pressures—a numbered guide. Mar Pollut Bull 62:651–655

    Article  Google Scholar 

  • Fairweather PG (1999) Determining the ‘health’ of estuaries: proiorities for ecological research. Aust J Ecol 24:441–451

    Article  Google Scholar 

  • Ferreira JG, Andersen JH, Borja A, Bricker SB, Camp J, da Silva MC, Garcés E, Heiskanen A-S, Humborg C, Ignatiades L, Lancelot C, Menesguen A, Tett P, Hoepffner N, Claussen U (2011) Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive. Estuar Coast Shelf Sci 93(2011):117–131

    Article  Google Scholar 

  • Foden J, Devlin MJ, Mills DK, Malcolm SJ (2011) Searching for undesirable disturbance: an application of the OSPAR eutrophication assessment method to marine waters of England and Wales. Biogeochemistry 106:157–175. doi:10.1007/s10533-010-9475-9

    Article  Google Scholar 

  • Garcia SM, Zerbi A, Aliaume C, Do Chi T, Lasserre G (2003) The ecosystem approach to fisheries. Issues, terminology, principles, institutional foundations, implementation and outlook. FAO Fisheries Technical Paper No. 443. FAO, Rome

  • Glibert PM, Anderson DM, Entien PG, Graneli E, Sellner K (2005) The global, complex phenomena of harmful algal blooms. Oceanography 18(2):147

    Google Scholar 

  • Greene CH, Pershing AJ, Cronin TM, Ceci N (2008) Arctic climate change and its impact on the ecology of the North Atlantic. Ecology 89:s24–s38

    Article  Google Scholar 

  • Greenwood N, Parker ER, Fernand L, Sivyer DB, Weston K, Painting SJ, Kröger S, Forster RM, Lees HE, Mills DK, Laane RWPM (2010) Detection of low bottom water oxygen concentrations in the North Sea; implications for monitoring and assessment of ecosystem health. Biogeosciences 7:1357–1373

    Article  Google Scholar 

  • Hiddink JG, Jennings S, Kaiser MJ, Queiros AM, Duplisea DE, Piet GJ (2006) Cumulative impacts of seabed trawl disturbance on benthic biomass, production, and species richness in different habitats. Can J Fish Aquat Sci 63:721–736

    Article  Google Scholar 

  • ICES (2001) Report of the ICES Advisory Committee on Ecosystems, 2001. ICES Cooperative Research Report 249:15–59

    Google Scholar 

  • Jennings S, Nicholson MD, Dinmore TA, Lancaster J (2002) The effect of chronic trawling disturbance on the production of infaunal communities. Mar Ecol Prog Ser 243:251–260

    Article  Google Scholar 

  • Johnson MT, Greenwood N, Sivyer DB, Thomson M, Reeve A, Jickells TD (2012) Characterising the seasonal cycle of dissolved organic nitrogen in the Southern North Sea using Cefas SmartBuoy high-resolution time-series samples. Biogeochemistry. doi:10.1007/s10533-012-9738-8

    Google Scholar 

  • Kürten B, Painting SJ, Struck U, Polunin NVC, Middelburg JJ (2011) Tracking seasonal changes in North Sea zooplankton trophic dynamics using stable isotope. Biogeochemistry. doi:10.1007/s10533-011-9630-y

    Google Scholar 

  • Kürten B, Frutos I, Struck U, Painting SJ, Polunin NVC, Middelburg JJ (2012) Trophodynamics and functional feeding groups of North Sea fauna: a combined stable isotope and fatty acid approach. Biogeochemistry. doi:10.1007/s10533-012-9701-8

    Google Scholar 

  • Kutti T, Ervik A, Hoisaeter T (2008) Effects of organic effluents from a salmon farm on a Fjordic system. III. Linking deposition rates of organic matter and benthic productivity. Aquaculture 282:47–53

    Article  Google Scholar 

  • Moloney CL, Field JG (1991) The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows. J Plankton Res 13:1003–1038

    Article  Google Scholar 

  • Murphy JM, Booth BBB, Collins M, Harris GR, Sexton DMH, Webb MJ (2007) A methodology for probabilistic predictions of regional climate change from perturbed physics ensembles. Philos Trans R Soc A 365:1993–2028. doi:10.1098/rsta.2007.2077

    Article  Google Scholar 

  • Nations United (1992) Convention on Biological Diversity. UN, New York

    Google Scholar 

  • Neubacher E, Trimmer M, Parker R (2012) The potential effect of sustained hypoxia on nitrogen cycling in sediment from the southern North Sea: a mesocosm experiment. Biogeochemistry. doi:10.1007/s10533-012-9749-5

    Google Scholar 

  • Nicholson M, Jennings S (2003) Testing candidate indicators to support ecosystem-based management: the power of monitoring surveys to detect temporal trends in fish community metrics. ICES J Mar Sci 61:35–42

    Article  Google Scholar 

  • Oosterhuis SS, Baars MA, Klein Breteler WCM (2000) Release of the enzyme chitobiase by the copepod Temora longicornis: characteristics and potential tool for estimating crustacean biomass production in the sea. Mar Ecol Prog Ser 196:195–206

    Article  Google Scholar 

  • OSPAR ICG-MSFD(1) (2011) Terminology of the MSFD. 11/04/01

  • Painting SJ, Moloney CL, Lucas MI (1993) Simulation and field measurements of phytoplankton–bacteria–zooplankton interactions in the southern Benguela upwelling region. Mar Ecol Prog Ser 100:55–69

    Article  Google Scholar 

  • Painting SJ, Devlin MJ, Rogers SI, Mills DK, Parker ER, Rees HL (2005) Assessing the suitability of OSPAR EcoQOs for eutrophication vs ICES Criteria for England and Wales. Mar Pollut Bull 50(12):1569–1584

    Article  Google Scholar 

  • Painting S, Neubacher E, Birchenough S, Bolam S, Fernand L (2010) Marine Ecosystem Connections: essential indicators of healthy, productive and biologically diverse seas (contract ME3205). Report: Results of field work to quantify key processes affecting the flow of C, N, O and Si at study sites. Milestone Report 3, ME3205: 10/03, Defra

  • Painting SJ, van der Molen J, Coughlan C, Parker R, Birchenough S, Bolam S, Forster R, Aldridge J, Greenwood N (2011) Marine Ecosystem Connections: essential indicators of healthy, productive and biologically diverse seas (contract ME3205). Report: Development of indicators of ecosystem function. Milestone Report 4. ME3205: 11/04, Defra

  • Painting SJ, Montagnes D, Garnacho E, Downes-Tettmar N, Mikkelsen O, Fernand LJ, Forster RM, Sivyer DB, Greenwood N, Milligan SP, Baars MA, Oosterhuis SS (2012) Structure and function of pelagic food webs at 3 ecohydrodynamically distinct sites in the North Sea. Biogeochemistry (submitted)

  • Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic pollution. Oceanogr Mar Biol 16:229–311

    Google Scholar 

  • Platt T, White III GN, Zhai L, Sathyendranath S, Roy S (2009) The phenology of phytoplankton blooms: ecosystem indicators from remote sensing. Ecol Model 220(21):3057–3069

    Article  Google Scholar 

  • Pope V, Brown S, Clark R, Collins M, Collins W, Dearden C, Gunson J, Harris G, Jones C, Keen A, Lowe J, Ringer M, Senior C, Sitch S, Webb M, Woodward S (2007) The Met Office Hadley Centre climate modelling capability: the competing requirements for improved resolution, complexity and dealing with uncertainty. Philos Trans R Soc A 365:2635–2657. doi:10.1098/rsta.2007.2087

    Article  Google Scholar 

  • Queste BY, Fernand L, Jickells TD, Heywood KJ (2012) Spatial extent and historical context of North Sea oxygen depletion in August 2010. Biogeochemistry. doi:10.007/s10533-012-9729-9

    Google Scholar 

  • Rabalais NN, Diaz RJ, Levin LE, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused coastal hypoxia. Biogeosciences 7:585–619

    Article  Google Scholar 

  • Reid PC, Borges MF, Svendsen E (2001) A regime shift in the North Sea circa 1988 linked to changes in the North Sea horse mackerel fishery. Fish Res 50:163–171

    Article  Google Scholar 

  • Rice JC, Rochet M-J (2005) A framework for selecting a suite of indicators for fisheries management. ICES J Mar Sci 62(3):516–527

    Article  Google Scholar 

  • Ruardij P, van Raaphorst W (1995) Benthic nutrient regeneration in the ERSEM-BFM ecosystem model of the North Sea. Neth J Sea Res 33:453–483

    Article  Google Scholar 

  • Ruardij P, van Haren H, Ridderinkhof H (1997) The impact of thermal stratification on phytoplankton and nutrient dynamics in shelf seas: a model study. J Sea Res 38:311–331

    Article  Google Scholar 

  • Ruardij P, Veldhuis MJW, Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4:941–963

    Article  Google Scholar 

  • Salihoglu B et al (2012) Bridging marine ecosystem and biogeochemistry research: lessons and recommendations from comparative studies. J Mar Syst. doi:10.1016/j.jmarsys.2012.07.005

  • Sastri AR, Dower JF (2006) Field validation of an instantaneous estimate of in situ development and growth for marine copepod communities. Can J Fish Aquat Sci 63:2639–2647

    Article  Google Scholar 

  • Sastri AR, Dower JF (2009) Inter-annual variability in chitobiase-based production rates of the crustacean zooplankton community in the Strait of Georgia. Mar Ecol Prog Ser 388:147–157

    Article  Google Scholar 

  • Shin Y-J, Shannon LJ, Bundy A, Coll M, Aydin K, Bez N, Blanchard JL, Borges MF, Diallo I, Diaz E, Heymans JJ, Hill L, Johannesen E, Jouffre D, Kifani S, Labrosse P, Link JS, Mackinson S, Masski H, Mollmann C, Neira S, Ojaveer H, ould Mohammed Abdallahi K, Perry I,Thiao D, Yemane D, Cury P (2010) Using indicators for evaluating, comparing, and communicating the ecological status of exploited marine ecosystems. 2. Setting the scene. ICES J Mar Sci 67:692–716

  • Spencer M, Birchenough SNR, Mieszkowska N, Robinson LA, Simpson SD, Burrows MT, Capasso E, Cleall-Harding P, Crummy J, Duck C, Eloire D, Frost M, Hall AJ, Hawkins SJ, Johns DG, Sims DW, Smyth TJ, Frid CLJ (2010) Temporal change in UK marine communities: trends or regime shifts. Mar Ecol 32(Suppl. 1):1–15

    Google Scholar 

  • Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009) Interpretation of Fast Repetition Rate (FRR) fluorescence: signatures of community structure versus physiological state. Mar Ecol Prog Ser 376:1–19

    Article  Google Scholar 

  • Teal LR, Parker R, Fones G, Solan M (2009) Simultaneous determination of in situ vertical transitions of color, pore-water metals, and visualization of infaunal activity in marine sediments. Limnol Oceanogr 54(5):1801–1810

    Article  Google Scholar 

  • Tett P, Gowen R, Mills DM, Fernandes T, Gilpin L, Huxham M, Kennington K, Read P, Service M, Wilkinson M, Malcolm SJ (2007) Defining and detecting undesirable disturbance in the context of marine eutrophication. Mar Pollut Bull 55:282–297

    Google Scholar 

  • Thain JE, Vethaak AD, Hylland K (2008) Contaminants in marine ecosystems: developing an integrated indicator framework using biological-effect techniques. ICES J Mar Sci 65:1508–1514

    Article  Google Scholar 

  • United Nations (2002). Report of the World Summit on Sustainable Development. UN, Johannesburg, South Africa, 26 August–4 September 2002, ISBN 92-1-104521-5

  • van der Molen J, Aldridge J, Coughlan C, Parker R, Stephens D, Ruardij P (2012) Modelling marine ecosystem response to climate change and trawling in the North Sea. Biogeochemistry. doi:10.1007/s1053301297637

  • Van Hoey G, Borja A, Birchenough SNR, Degraer S, Fleischer D, Magni P, Muxika I, Reiss H, Rumohr H, Schröder A, Zettler M (2010) The use of benthic indicators in Europe: from the Water Framework Directive to the Marine Strategy Framework Directive. Mar Pollut Bull 60:2187–2196

    Article  Google Scholar 

  • Van Leeuwen SM, van der Molen J, Ruardij P, Fernand L, Jickells T (2012) Modelling the contribution of Deep Chlorophyll Maxima to annual primary production in the North Sea. Biogeochemistry. doi:10.1007/s10533-012-9704-5

    Google Scholar 

  • Vichi M, May W, Navarra A (2003) Response of a complex ecosystem model of the northern Adriatic Sea to a regional climate change scenario. Clim Res 24:141–158

    Article  Google Scholar 

  • Vichi M, Ruardij P, Baretta JW (2004) Link or sink: a modelling interpretation of the open Baltic biogeochemistry. Biogeosciences 1:79–100

    Article  Google Scholar 

  • Vichi M, Pinardi N, Masina S (2007) A generalized model of pelagic biogeochemistry for the global ocean ecosystem. Part I: theory. J Mar Syst 64:89–109

    Article  Google Scholar 

  • Wilber DH, Clarke DG (1998) Estimating secondary production and benthic consumption in monitoring studies: a case study of the impacts of dredged material disposal in Galveston Bay, Texas. Estuaries 21:230–245

    Article  Google Scholar 

  • Wilber DH, Clarke DG, Rees SI (2007) Responses of benthic macroinvertebrates to thin-layer disposal of dredged material in Mississippi Sound, USA. Mar Pollut Bull 54:42–52

    Article  Google Scholar 

  • Xiao Y, Ferreira J, Bricker S, Nunes JP, Zhu M, Zhang W (2007) Trophic assessment in Chinese coastal systems—review of methods and application to the Changjiang (Yangtze) estuary and Jiaozhou Bay. Estuar Coasts 30(6):901–918

    Google Scholar 

Download references

Acknowledgments

This work was largely supported by the UK Department for Environment, Food and Rural Affairs (Defra) contract ME3205 (Marine Ecosystems Connections: essential indicators of healthy, productive and biologically diverse seas). We are grateful to our colleagues who participated in the project, and for the constructive comments of anonymous reviewers on earlier versions of this manuscript. All views expressed here are those of the authors.

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  1. C. Coughlan

    Present address: CEC Joint Research Centre, Institute for Environment and Sustainability, Ispra, VA, Italy

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  1. The Centre for Fisheries, Environment and Aquaculture Science (Cefas), Pakefield Road, Lowestoft, Suffolk, NR33 0HT, UK

    S. J. Painting, J. van der Molen, E. R. Parker, C. Coughlan, S. Birchenough, S. Bolam, J. N. Aldridge, R. M. Forster & N. Greenwood

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Painting, S.J., van der Molen, J., Parker, E.R. et al. Development of indicators of ecosystem functioning in a temperate shelf sea: a combined fieldwork and modelling approach. Biogeochemistry 113, 237–257 (2013). https://doi.org/10.1007/s10533-012-9774-4

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