Oceanography The Official Magazine of
The Oceanography Society
Volume 27 Issue 04

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Volume 27, No. 4
Pages 116 - 133


Developing Ecosystem Indicators for Responses to Multiple Stressors

By Jennifer L. Boldt , Rebecca Martone, Jameal Samhouri , R. Ian Perry, Sachihiko Itoh, Ik Kyo Chung, Motomitsu Takahashi, and Naoki Yoshie 
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Article Abstract

Human activities in coastal and marine ecosystems provide a suite of benefits for people, but can also produce a number of stressors that can act additively, synergistically, or antagonistically to change ecosystem structure, function, and dynamics in ways that differ from single stressor responses. Scientific tools that can be used to evaluate the effects of multiple stressors are needed to assist decision making. In this paper, we review indicator selection methods and general approaches to assess indicator responses to multiple stressors and compare example ecosystem assessments. Recommendations are presented for choosing and assessing suites of indicators to characterize responses. Indicators should be chosen based upon defined criteria, conceptual models linking indicators to pressures and drivers, and defined strategic goals and ecological or management objectives. Indicators should be complementary and nonredundant, and they should integrate responses to multiple stressors and reflect the status of the ecosystem. An initial core set of indicators could include those that have been tested for the effects of climate and fishing and then expanded to include other pressures and ecosystem-specific, feature-pressure interactions. Identifying indicators and evaluating multiple stressors on marine ecosystems require a variety of approaches, such as empirical analyses, expert opinion, and model-based simulation. The goal is to identify a meaningful set of indicators that can be used to assist with the management of multiple types of human interactions with marine ecosystems.


Boldt, J.L., R. Martone, J. Samhouri, R.I. Perry, S. Itoh, I.K. Chung, M. Takahashi, and N. Yoshie. 2014. Developing ecosystem indicators for responses to multiple stressors. Oceanography 27(4):116–133, https://doi.org/10.5670/oceanog.2014.91.


Adams, K.L., and J.F. Wendel. 2005. Novel patterns of gene expression in polyploid plants. Trends in Genetics 21:539–543, https://doi.org/10.1016/j.tig.2005.07.009.

Adams, S.M. 2005. Assessing cause and effect of multiple stressors on marine systems. Marine Pollution Bulletin 51:649–657, https://doi.org/10.1016/j.marpolbul.2004.11.040.

Adams, S.M., and M.S. Greeley. 2000. Ecotoxic-ological indicators of water quality: Using multi- response indicators to assess the health of aquatic ecosystems. Water, Air, and Soil Pollution 123:103–115, https://doi.org/10.1023/A:1005217622959.

Allan, J.D., P.B. McIntyre, S.D.P. Smith, B.S. Halpern, G.L. Boyer, A. Buchsbaum, G.A. Burton Jr., L.M. Campbell, W.L. Chadderton, J.J.H. Ciborowski, and others. 2013. Joint analysis of stressors and ecosystem services to enhance restoration effectiveness. Proceedings of the National Academy of Sciences of the United States of America 110:372–377, https://doi.org/10.1073/pnas.1213841110.

Altman, I., A.M.H. Blakeslee, G.C. Osio, C.B. Rillahan, S.J. Teck, J.J. Meyer, J.E. Byers, and A.A. Rosenberg. 2011. A practical approach to implementation of ecosystem-based management: A case study using the Gulf of Maine marine ecosystem. Frontiers in Ecology and the Environment 9:183–189, https://doi.org/10.1890/080186.

Andrews, K.S., G.D. Williams, and V.V. Gertseva. 2013. Anthropogenic Drivers and Pressures. California Current Integrated Ecosystem Assessment: Phase II Report 2012, P.S. Levin, B.K. Wells, and M.B. Sheer, eds, http://www.noaa.gov/iea/Assets/iea/california/Report/pdf/Anthropogenic Drivers and Pressures CCIEA 2012.pdf.

Araujo, H.A., C. Holt, J.M.R. Curtis, R.I. Perry, J.R. Irvine, and C.G.J. Michielsens. 2013. Building an ecosystem model using mismatched and fragmented data: A probabilistic network of early marine survival for coho salmon Oncorhynchus kisutch in the Strait of Georgia. Progress in Oceanography 115:41–52, https://doi.org/10.1016/j.pocean.2013.05.022.

Ban, N.C., H.M. Alidina, and J.A. Ardron. 2010. Cumulative impact mapping: Advances, relevance and limitations to marine management and conservation, using Canada’s Pacific waters as a case study. Marine Policy 34:876–886, https://doi.org/10.1016/j.marpol.2010.01.010.

Ban, S.S., N.A.J. Graham, and S.R. Connolly. 2014. Evidence for multiple stressor interactions and effects on coral reefs. Global Change Biology 20:681–697, https://doi.org/10.1111/gcb.12453.

Barange, M., G. Merino, J.L. Blanchard, J. Scholtens, J. Harle, E.H. Allison, J.I. Allen, J. Holt, and S. Jennings. 2014. Impacts of climate change on marine ecosystem production in societies dependent on fisheries. Nature Climate Change 4:211–216, https://doi.org/10.1038/nclimate2119.

Biggs, R., S.R. Carpenter, and W.A. Brock. 2009. Turning back from the brink: Detecting an impending regime shift in time to avert it. Proceedings of the National Academy of Sciences of the United States of America 106:826–831, https://doi.org/10.1073/pnas.0811729106.

Birk, S., W. Bonne, A. Borja, S. Brucet, A. Courrat, S. Poikane, A. Solimini, W. van de Bund, N. Zampoukas, and D. Hering. 2012. Three hundred ways to assess Europe’s surface waters: An almost complete overview of biological methods to implement the Water Framework Directive. Ecological Indicators 18:31–41, https://doi.org/10.1016/j.ecolind.2011.10.009.

Blanchard, J.L., M. Coll, V.M. Trenkel, R. Vergnon, D. Yemane, D. Jouffre, J.S. Link, and Y.-J. Shin. 2010. Trend analysis of indicators: A comparison of recent changes in the status of marine ecosystems around the world. ICES Journal of Marine Science 67:732–744, https://doi.org/10.1093/icesjms/fsp282.

Boettiger, C., and A. Hastings. 2012. Quantifying limits to detection of early warning for critical transitions. Journal of the Royal Society Interface 9:2,527–2,539, https://doi.org/10.1098/rsif.2012.0125.

Borja, Á., S.B. Bricker, D.M. Dauer, N.T. Demetriades, J.G. Ferreira, A.T. Forbes, P. Hutchings, X. Jia, R. Kenchington, J.C. Marques, and C. Zhu. 2008. Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Marine Pollution Bulletin 56:1,519–1,537, https://doi.org/10.1016/j.marpolbul.2008.07.005.

Borja, Á., and D.M. Dauer. 2008. Assessing the environmental quality status in estuarine and coastal systems: Comparing methodologies and indices. Ecological Indicators 8:331–337, https://doi.org/10.1016/j.ecolind.2007.05.004.

Borja, Á., D. Dauer, M. Elliott, and C. Simenstad. 2010. Medium- and long-term recovery of estuarine and coastal ecosystems: Patterns, rates and restoration effectiveness. Estuaries and Coasts 33:1,249–1,260, https://doi.org/10.1007/s12237-010-9347-5.

Borja, Á., M. Elliott, J.H. Andersen, A.C. Cardoso, J. Carstensen, J.G. Ferreira, A.-S. Heiskanen, J.C. Marques, J.M. Neto, H. Teixeira, and others. 2013. Good Environmental Status of marine ecosystems: What is it and how do we know when we have attained it? Marine Pollution Bulletin 76:16–27, https://doi.org/10.1016/j.marpolbul.2013.08.042.

Borja, Á., I. Galparsoro, X. Irigoien, A. Iriondo, I. Menchaca, I. Muxika, M. Pascual, I. Quincoces, M. Revilla, J. Germán Rodríguez, and others. 2011. Implementation of the European Marine Strategy Framework Directive: A methodological approach for the assessment of environmental status, from the Basque Country (Bay of Biscay). Marine Pollution Bulletin 62:889–904, https://doi.org/10.1016/j.marpolbul.2011.03.031.

Bundy, A., M. Coll, L.J. Shannon, and Y.-J. Shin. 2012. Global assessments of the status of marine exploited ecosystems and their management: What more is needed? Current Opinion in Environmental Sustainability 4:292–296, https://doi.org/10.1016/j.cosust.2012.05.003.

Burke, B.J., W.T. Peterson, B.R. Beckman, C. Morgan, E.A. Daly, and M. Litz. 2013. Multivariate models of adult Pacific Salmon returns. PLoS ONE 8(1):e54134, https://doi.org/10.1371/journal.pone.0054134.

Canter, L.W., and S.F. Atkinson. 2011. Multiple uses of indicators and indices in cumulative effects assessment and management. Environmental Impact Assessment Review 31:491–501, https://doi.org/10.1016/j.eiar.2011.01.012.

Cardoso, A.C., S. Cochrane, H. Doemer, J.G. Ferreira, F. Galgani, C. Hagebro, G. Hanke, N. Hoepffner, P.D. Keizer, R. Law, and others. 2010. Scientific Support to the European Commission on the Marine Strategy Framework Directive. Management Group Report. EUR 24336 EN – Joint Research Centre, Luxembourg: Office for Official Publications of the European Communities, 57 pp.

Carignan, V., and M.-A. Villard. 2002. Selecting indicator species to monitor ecological integrity: A review. Environmental Monitoring and Assessment 78:45–61, https://doi.org/10.1023/A:1016136723584.

Carpenter, S.R., and W.A. Brock. 2006. Rising variance: a leading indicator of ecological transition. Ecology Letters 9(3):311–318, https://doi.org/10.1111/j.1461-0248.2005.00877.x.

Coll, M., L.J. Shannon, D. Yemane, J.S. Link, H. Ojaveer, S. Neira, D. Jouffre, P. Labrosse, J.J. Heymans, E.A. Fulton, and Y.-J. Shin. 2010. Ranking the ecological relative status of exploited marine ecosystems. ICES Journal of Marine Science 67:769–786, https://doi.org/10.1093/icesjms/fsp261.

COM (Commission of the European Communities). 2005a. Communication from the Commission to the Council and the European Parliament: Thematic Strategy on the Protection and Conservation of the Marine Environment. COM (2005), 504 final, SEC (2005), 1290, 9 pp, http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:52005DC0504&from=EN.

COM. 2005b. Proposal for a Directive of the European Parliament and of the Council Establishing a Framework for Community Action in the Field of Marine Environmental Policy (Marine Strategy Directive). COM (2005), 505 final, 2005/0211 (COD), SEC (2005), 1290, 31 pp, http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:52005PC0505&from=EN.

Contamin, R., and A.M. Ellison. 2009. Indicators of regime shifts in ecological systems: What do we need to know and when do we need to know it? Ecological Applications 19:799–816, https://doi.org/10.1890/08-0109.1.

Crain, C.M., K. Kroeker, and B.S. Halpern. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters 11:1,304–1,315, https://doi.org/10.1111/j.1461-0248.2008.01253.x.

Dakos, V., S.R. Carpenter, W.A. Brock, A.M. Ellison, V. Guttal, A.R. Ives, S. Kéfi, V. Livina, D.A. Seekell, E.H. van Nes, and M. Scheffer. 2012. Methods for detecting early warnings of critical transitions in time series illustrated using simulated ecological data. PLoS ONE 7:e41010, https://doi.org/10.1371/journal.pone.0041010.

Dakos, V., M. Scheffer, E.H. van Nes, V. Brovkin, V. Petoukhov, and H. Held. 2008. Slowing down as an early warning signal for abrupt climate change. Proceedings of the National Academy of Sciences of the United States of America 105:14,308–14,312, https://doi.org/10.1073/pnas.0802430105.

Dakos, V., E. van Nes, R. Donangelo, H. Fort, M. Scheffer. 2010. Spatial correlation as leading indicator of catastrophic shifts. Theoretical Ecology 3:163–174, https://doi.org/10.1007/s12080-009-0060-6.

Dale, V.H., and S.C. Beyeler. 2001. Challenges in the development and use of ecological indicators. Ecological Indicators 1:3–10, https://doi.org/10.1016/S1470-160X(01)00003-6.

Darling, E.S., and I.M. Côté. 2008. Quantifying the evidence for ecological synergies. Ecology Letters 11:1,278–1,286, https://doi.org/10.1111/j.1461-0248.2008.01243.x.

Daskalov, G.M., A.N. Grishin, S. Rodionov, and V. Mihneva. 2007. Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proceedings of the National Academy of Sciences of the United States of America 104:10,518–10,523, https://doi.org/10.1073/pnas.0701100104.

deYoung, B., R. Harris, J. Alheit, G. Beaugrand, N. Mantua, and L. Shannon. 2004. Detecting regime shifts in the ocean: Data considerations. Progress in Oceanography 60:143–164, https://doi.org/10.1016/j.pocean.2004.02.017.

DFO (Department of Fisheries and Oceans Canada). 2007. A New Ecosystem Science Framework in Support of Integrated Management. DFO/2007-1296. Communications Branch, Fisheries and Oceans Canada, Ottawa, Ontario K1A 0E6, 18 pp, http://www.dfo-mpo.gc.ca/science/publications/ecosystem/index-eng.htm.

DFO. 2012. Risk-Based Assessment Framework to Identify Priorities for Ecosystem-Based Oceans Management in the Pacific Region. DFO Canadian Science Advisory Secretariat Science Advisory Report 2012/044, 13 pp.

DFO. 2013. Risk-Based Assessment of Climate Change Impacts and Risks on the Biological Systems and Infrastructure within Fisheries and Oceans Canada’s Mandate - Pacific Large Aquatic Basin. DFO Canadian Science Advisory Secretariat Science Advisory Report 2013/016, 43 pp.

Dickey-Collas, M. 2014. Why the complex nature of integrated ecosystem assessments requires a flexible and adaptive approach. ICES Journal of Marine Science 71:1,174–1,182, https://doi.org/10.1093/icesjms/fsu027.

Ditlevsen, P.D., and S.J. Johnsen. 2010. Tipping points: Early warning and wishful thinking. Geophysical Research Letters 37, L19703, https://doi.org/10.1029/2010GL044486.

Doren, R.F., J.C. Trexler, A.D. Gottlieb, and M.C. Harwell. 2009. Ecological indicators for system-wide assessment of the greater everglades ecosystem restoration program. Ecological Indicators 9S:S2–S16, https://doi.org/10.1016/j.ecolind.2008.08.009.

Drake, J.M., and B.D. Griffen. 2010. Early warning signals of extinction in deteriorating environments. Nature 467:456–459, https://doi.org/10.1038/nature09389.

Duarte, C., Á. Borja, J. Carstensen, M. Elliott, D. Krause-Jensen, and N. Marbà. 2013. Paradigms in the recovery of estuarine and coastal ecosystems. Estuaries and Coasts, https://doi.org/10.1007/s12237-013-9750-9.

Duarte, C., D. Conley, J. Carstensen, and M. Sánchez-Camacho. 2009. Return to Neverland: Shifting baselines affect eutrophication restoration targets. Estuaries and Coasts 32:29–36, https://doi.org/10.1007/s12237-008-9111-2.

Elliot, M. 2002. The role of the DPSIR approach and conceptual models in marine environmental management: An example for offshore wind power. Marine Pollution Bulletin 44:iii–vii, https://doi.org/10.1016/S0025-326X(02)00146-7.

Elliot, M. 2011. Marine science and management means tackling exogenic unmanaged pressures and endogenic managed pressures: A numbered guide. Marine Pollution Bulletin 62:651–655, https://doi.org/10.1016/j.marpolbul.2010.11.033.

European Commission. 2010. 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). Official Journal of the European Union L 164:19–40, http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32008L0056&from=EN.

Feary, D.A., A.M. Fowler, and T.J. Ward. 2014. Developing a rapid method for undertaking the World Ocean Assessment in data-poor regions: A case study using the South China Sea large marine ecosystem. Ocean and Coastal Management 95:129–137, https://doi.org/10.1016/j.ocecoaman.2014.04.006.

Fulton, E.A., A.D.M. Smith, and A.E. Punt. 2005. Which ecological indicators can robustly detect effects of fishing? ICES Journal of Marine Science 62:540–551, https://doi.org/10.1016/j.icesjms.2004.12.012.

Fu, C., S. Gaichas, J.S. Link, A. Bundy, J.L. Boldt, A.M. Cook, R. Gamble, K.R. Utne, H. Liu, and K.D. Friedland. 2012. Relative importance of fisheries, trophodynamic and environmental drivers in a series of marine ecosystems. Marine Ecological Progress Series 459:169–184, https://doi.org/10.3354/meps09805.

Fu, C., R.I. Perry, Y.-J. Shin, J. Schweigert, and H. Liu. 2013. An ecosystem modelling framework for incorporating climate regime shifts into fisheries management. Progress in Oceanography 115:53–64, https://doi.org/10.1016/j.pocean.2013.03.003.

Goberville, E., G. Beaugrand, B. Sautour, P. Treguer, and SOMLIT Team. 2010. Climate-driven changes in coastal marine systems of western Europe. Marine Ecological Progress Series 408:129–147, http://www.int-res.com/abstracts/meps/v408/p129-148.

Grech, A., R. Coles, and H. Marsh. 2011. A broad scale assessment of the risk to coastal seagrasses from cumulative threats. Marine Policy 35:560–567, https://doi.org/10.1016/j.marpol.2011.03.003.

Greenstreet, S.P.R., H.M. Fraser, S.I. Rogers, V.M. Trenkel, S.D. Simpson, and J.K. Pinnegar. 2012. Redundancy in metrics describing the composition, structure, and functioning of the North Sea demersal fish community. ICES Journal of Marine Science 69:8–22, https://doi.org/10.1093/icesjms/fsr188.

Håkanson, L., and C.M. Duarte. 2008. Data variability and uncertainty limits the capacity to identify and predict critical changes in coastal systems: A review of key concepts. Ocean and Coastal Management 51(10):671–688, https://doi.org/10.1016/j.ocecoaman.2008.07.003.

Halpern, B.S., and R. Fujita. 2013. Assumptions, challenges, and future directions in cumulative impact analysis. Ecosphere 4(10):131, https://doi.org/10.1890/ES13-00181.1.

Halpern, B.S., C. Longo, D. Hardy, K.L. McLeod, J.F. Samhouri, S.K. Katona, K. Kleisner, S.E. Lester, J. O’Leary, M. Ranelletti, and others. 2012. An index to assess the health and benefits of the global ocean. Nature 488:622, https://doi.org/10.1038/nature11397.

Halpern, B.S., K.A. Selcoe, F. Micheli, and C.V. Kappel. 2007. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conservation Biology 21:1,301–1,315, https://doi.org/10.1111/j.1523-1739.2007.00752.x.

Halpern, B.S., S. Walbridge, K.A. Selkoe, C.V. Kappel, F. Micheli, C. D’Agrosa, J.F. Bruno, K.S. Casey, C. Ebert, H.E. Fox, and others. 2008. A global map of human impact on marine ecosystems. Science 319:948–952, https://doi.org/10.1126/science.1149345.

Harwell, M.A., V. Myers, T. Young, A. Bartuska, N. Gassman, J.H. Gentile, C.C. Harwell, S. Appelbaum, J. Barko, B. Causey, and others. 1999. A framework for an ecosystem integrity report card. BioScience 49:543–556, https://doi.org/10.2307/1313475.

Hayes, E.H., and W.G. Landis. 2004. Regional ecological risk assessment of a near shore marine environment: Cherry Point, WA. Human and Ecological Risk Assessment 10:299–325, https://doi.org/10.1080/10807030490438256.

Hayes, K.R., J.M. Dambacher, V. Lyne, R. Sharples, W.A. Rochester, L.X.C. Dutra, and R. Smith. 2012. Ecological Indicators for Australia’s Exclusive Economic Zone: Rationale and Approach with Application to the South West Marine Region. A report prepared for the Australian Government Department of Sustainability, Environment, Water, Population and Communities. CSIRO Wealth from Oceans Flagship, Hobart, 219 pp.

Hazen, E.L., I.D. Schroeder, J. Peterson, W.T. Peterson, W.J. Sydeman, S.A. Thompson, B.K. Wells, and S.J. Bograd. 2013. Oceanographic and Climatic Drivers and Pressures. California Current Integrated Ecosystem Assessment: Phase II Report 2012, 56 pp, http://www.noaa.gov/iea/Assets/iea/california/Report/pdf/Ocean and Climate CCIEA 2012.pdf.

Hegmann, G., C. Cocklin, R. Creasey, S. Dupuis, A. Kennedy, L. Kingsley, W. Ross, H. Spaling, and D. Stalker. 1999. Cumulative Effects Assessment Practitioners Guide. Prepared by AXYS Environmental Consulting Ltd. and the CEA Working Group for the Canadian Environmental Assessment Agency, Hull, Quebec, 134 pp.

HELCOM (Helsinki Commission). 2010. Towards a Tool for Quantifying Anthropogenic Pressures and Potential Impacts on the Baltic Sea Marine Environment: A Background Document on the Method, Data and Testing of the Baltic Sea Pressure and Impact Indices. Baltic Sea Environment Proceedings 125, 72 pp.

HELCOM. 2013. HELCOM Core Indicators: Final Report of the HELCOM CORESET Project. Baltic Sea Environment Proceedings No. 136, 71 pp.

Hewitt, J.E., and S.F. Thrush. 2010. Empirical evidence of an approaching alternate state produced by intrinsic community dynamics, climatic variability and management actions. Marine Ecological Progress Series 413:267–276, https://doi.org/10.3354/meps08626.

Hobday, A.J., A.D.M. Smith, I.C. Stobutzki, C. Bulman, R. Daley, J.M. Dambacher, R.A. Deng, J. Dowdney, M. Fuller, D. Furlani, and others. 2011. Ecological risk assessment for the effects of fishing. Fisheries Research 108:372–284, https://doi.org/10.1016/j.fishres.2011.01.013.

Hughes, T.P., C. Linares, V. Dakos, I.A. van de Leemput, and E.H. van Nes. 2013. Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends in Ecology and Evolution 28:149–155, https://doi.org/10.1016/j.tree.2012.08.022.

ICES (International Council for the Exploration of the Sea). 2013. ICES Annual Report 2012. International Council for the Exploration of the Sea, Copenhagen V, Denmark, 98 pp.

Jackson, L.E., J.C. Kurtz, and W.S. Fisher, eds. 2000. Evaluation Guidelines for Ecological Indicators. EPA/620/R-99/005. U.S. Environmental Protection Agency, Office of Research and Development, Research Triangle Park, NC, pp. 107.

Jamieson, G., P. Livingston, and C.-I. Zhang. 2010. Report of Working Group 19 on Ecosystem-Based Management Science and Its Application to the North Pacific. PICES Scientific Report No. 37, 166 pp.

Kappel, C.V., B.S. Halpern, and N. Napoli. 2012. Mapping Cumulative Impacts of Human Activities on Marine Ecosystems. Coastal and Marine Spatial Planning Research Report 03.NCEAS.12, Boston: SeaPlan, 107 pp, http://www.seaplan.org/wp-content/uploads/mapping_cumulative_indicators-nceas-12.pdf.

Kershner, J., J.F. Samhouri, C.A. James, and P.S. Levin. 2011. Selecting indicator portfolios for marine species and food webs: A Puget Sound case study. PLOS ONE 6(10):e25248, https://doi.org/10.1371/journal.pone.0025248.

King, J.R., V.N. Agostini, C.J. Harvey, G.A. McFarlane, M.G.G. Foreman, J.E. Overland, E. Di Lorenzo, N.A. Bond, and K.Y. Aydin. 2011. Climate forcing and the California Current ecosystem. ICES Journal of Marine Science 68:1,199–1,216, https://doi.org/10.1093/icesjms/fsr009.

Knights, A.M., R.S. Koss, and L.A. Robinson. 2013. Identifying common pressure pathways from a complex network of human activities to support ecosystem-based management. Ecological Applications 23:755–765, https://doi.org/10.1890/12-1137.1.

Korpinen, S., L. Meski, J.H. Andersen, and M. Laamanen. 2012. Human pressures and their potential impact on the Baltic Sea ecosystem. Ecological Indicators 15:105–114, https://doi.org/10.1016/j.ecolind.2011.09.023.

Kurtz, J.C., L.E. Jackson, and W.S. Fisher. 2001. Strategies for evaluating indicators based on guidelines from the Environmental Protection Agency’s Office of Research and Development. Ecological Indicators 1:49–60, https://doi.org/10.1016/S1470-160X(01)00004-8.

Lawson, J.W., and V. Lesage. 2013. A Draft Framework to Quantify and Cumulate Risks of Impacts from Large Development Projects for Marine Mammal Populations: A Case Study Using Shipping Associated with the Mary River Iron Mine Project. DFO Canadian Science Advisory Secretariat Research Document 2012/154 iv +, 22 pp.

Levin, P.S., M.J. Fogarty, S.A. Murawski, and D. Fluharty. 2009. Integrated ecosystem assessments: Developing the scientific basis for ecosystem-based management of the ocean. PLOS Biology 7(10):1000014, https://doi.org/10.1371/journal.pbio.1000014.

Levin, P.S., C.R. Kelble, R.L. Shuford, C. Ainsworth, Y. deReynier, R. Dunsmore, M.J. Fogarty, K. Holsman, E.A. Howell, M.E. Monaco, and others. 2014. Guidance for implementation of integrated ecosystem assessments: A US perspective. ICES Journal of Marine Science 71:1,198–1,204, https://doi.org/10.1093/icesjms/fst112.

Link, J. 2002. Does food web theory work for marine ecosystems? Marine Ecological Progress Series 230:1–9, https://doi.org/10.3354/meps230001.

Link, J. 2005. Translating ecosystem indicators into decision criteria. ICES Journal of Marine Science 62:569–576, https://doi.org/10.1016/j.icesjms.2004.12.015.

Link, J.S., and H.I. Browman. 2014. Integrating what? Levels of marine ecosystem-based assessment and management. ICES Journal of Marine Science 71:1,170–1,173, https://doi.org/10.1093/icesjms/fsu026.

Link, J.S., S. Gaichas, T.J. Miller, T. Essington, A. Bundy, J. Boldt, K.F. Drinkwater, and E. Moksness. 2012. Synthesizing lessons learned from comparing fisheries production in 13 northern hemisphere ecosystems: Emergent fundamental features. Marine Ecological Progress Series 459:293–302, https://doi.org/10.3354/meps09829.

Link, J.S., W.T. Stockhausen, G. Skaret, W. Overholtz, B.A. Megrey, H. Gjøsaeter, S. Gaichas, A. Dommasnes, J. Falk-Petersen, J. Kane, and others. 2009. A comparison of biological trends from four marine ecosystems: Synchronies, differences, and commonalities. Progress in Oceanography 81:29-46, https://doi.org/10.1016/j.pocean.2009.04.004.

Liquete, C., C. Piroddi, E.G. Drakou, L. Gurney, S. Katsanevakis, A. Charef, and B. Egoh. 2013. Current status and future prospects for the assessment of marine and coastal ecosystem services: A systematic review. PLoS ONE 8(7):e67737, https://doi.org/10.1371/journal.pone.0067737.

Livingston, P.A., K. Aydin, J.L. Boldt, A.B. Hollowed, and J.M. Napp. 2011. Alaska marine fisheries management: Advances and linkages to ecosystem research. Pp. 113–152 in Ecosystem Based Management for Marine Fisheries: An Evolving Perspective. A. Belgrano and C.W. Fowler, eds, Cambridge University Press.

Mantua, N.J., N.G. Taylor, G.T. Ruggerone, K.W. Myers, D. Preikshot, X. Augerot, N.D. Davis, B. Dorner, R. Hilborn, R.M. Peterman, and others. 2007. The Salmon MALBEC Project: A North Pacific-Scale Study to Support Salmon Conservation Planning. NPAFC Doc. 1060, School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA, 49 pp,http://www.npafc.org/new/publications/Documents/PDF 2007/1060(USA).pdf.

Maxwell, S.M., E.L. Hazen, S.J. Bograd, B.S. Halpern, G.A. Breed, B. Nickel, N.M. Teutschel, L.B. Crowder, S. Benson, P.H. Dutton, and others. 2013. Cumulative human impacts on marine predators. Nature Communications 4:2,688, https://doi.org/10.1038/ncomms3688.

McCarty, L.S., and K.R. Munkittrick. 1996. Environmental biomarkers in aquatic toxicology: Fiction, fantasy, or functional? Human and Ecological Risk Assessment 2:268–274, https://doi.org/10.1080/10807039609383607.

Mee, L.D., R.L. Jefferson, D.d’A. Laffoley, and M. Elliott. 2008. How good is good? Human values and Europe’s proposed Marine Strategy Directive. Marine Pollution Bulletin 56:187–204, https://doi.org/10.1016/j.marpolbul.2007.09.038.

Megrey, B.A., K.A. Rose, S.-I. Ito, D.E. Hay, F.E. Werner, Y. Yamanaka, and M.N. Aita. 2007. North Pacific basin-scale differences in lower and higher trophic level marine ecosystem responses to climate impacts using a nutrient-phytoplankton–zooplankton model coupled to a fish bioenergetics model. Ecological Modelling 202:196–210, https://doi.org/10.1016/j.ecolmodel.2006.08.018.

Micheli, F., B.S. Halpern, S. Walbridge, S. Ciriaco, F. Ferretti, S. Fraschetti, R. Lewison, L. Nykjaer, and A.A. Rosenberg. 2013. Cumulative human impacts on Mediterranean and Black Sea marine ecosystems: Assessing current pressures and opportunities. PLoS ONE 8:e79889, https://doi.org/10.1371/journal.pone.0079889.

Millennium Ecosystem Assessment. 2005. Ecosystems and Human Well-being: Biodiversity Synthesis. World Resources Institute, Washington, DC, 86 pp.

Mussali-Galante, P., E. Tovar-Sánchez, M. Valverde, and E. Rojas del Castillo. 2013. Biomarkers of exposure for assessing environmental metal pollution from molecules to ecosytems. La Revista Internacional de Contaminación Ambiental 29(1):117–140.

Niemeijer, D., and R.S. deGroot. 2008. A conceptual framework for selecting environmental indicator sets. Ecological Indicators 8:14–25, https://doi.org/10.1016/j.ecolind.2006.11.012.

Niemi, G.J., and M.E. McDonald. 2004. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35:89–111, https://doi.org/10.1146/annurev.ecolsys.35.112202.130132.

NOAA (National Oceanic and Atmospheric Administration). 2006. Evolving an Ecosystem Approach to Science and Management through NOAA and Its Partners. Final Report: The External Review of NOAA’s Ecosystem Research and Science Enterprise, A Report to the NOAA Science Advisory Board, 85 pp, http://www.sab.noaa.gov/Reports/eETT_Final_1006.pdf.

Norman, K.C., and D.S. Holland. 2013. Resilient and Economically Viable Coastal Communities. California Current Integrated Ecosystem Assessment: Phase II Report 2012, P.S. Levin, B.K. Wells, and M.B. Sheer, eds, 24 pp., http://www.noaa.gov/iea/Assets/iea/california/Report/pdf/Human Dimensions CCIEA 2012.pdf.

Noss, R.F. 1990. Indicators for monitoring biodiversity: A hierarchical approach. Conservation Biology 4:355–364, https://doi.org/10.1111/j.1523-1739.1990.tb00309.x.

OECD (Organization for Economic Co-operation and Development). 1999. Environmental Indicators for Agriculture: Volume 1. Concepts and Framework. Organization for Economic Co-operation and Development, Paris, 45 pp., http://www.oecd.org/greengrowth/sustainable-agriculture/40680795.pdf.

OECD. 2003. OECD Environmental Indicators: Development, Measurement and Use. Organization for Economic Co-operation and Development, Paris, 37 pp., http://www.oecd.org/environment/indicators-modelling-outlooks/24993546.pdf.

Painting, S.J., J. van der Molen, E.R. Parker, C. Coughlan, S. Birchenough, S. Bolam, J.N. Aldridge, R.M. Forster, and N. Greenwood. 2013. Development of indicators of ecosystem functioning in a temperate shelf sea: A combined fieldwork and modelling approach. Biogeochemistry 113:237–257, https://doi.org/10.1007/s10533-012-9774-4.

Perry, R.I., P. Cury, K. Brander, S. Jennings, C. Möllman, and B. Planque. 2010a. Sensitivity of marine systems to climate and fishing: Concepts, issues and management responses. Journal of Marine Systems 79:427–435, https://doi.org/10.1016/j.jmarsys.2008.12.017.

Perry, R.I., P. Livingston, and E.A. Fulton. 2010b. Ecosystem indicators. Pp. 83–89 in Report of Working Group 19 on Ecosystem-Based Management Science and Its Application to the North Pacific. G. Jamieson, P. Livingston, and C.-I. Zhang, eds, PICES Scientific Report No. 37, 166 pp.

Peterson, W.T., C.A. Morgan, J.P. Fisher, and E. Casillas. 2010. Ocean distribution and habitat associations of yearling coho (Oncorhynchus kisutch) and Chinook (O. tshawytscha) salmon in the northern California Current. Fisheries Oceanography 19(6):508–525, https://doi.org/10.1111/j.1365-2419.2010.00560.x.

Peterson, W.T., C.A. Morgan, J.O. Peterson, J.L. Fisher, B.J. Burke, and K. Fresh. 2013. Ocean Ecosystem Indicators of Salmon Marine Survival in the Northern California Current. http://www.nwfsc. noaa.gov/research/divisions/fe/estuarine/oeip/g-forecast.cfm.

Power, M. 1997. Assessing the effects of environmental stressors on fish populations. Aquatic Toxicology 39:151–169, https://doi.org/10.1016/S0166-445X(97)00020-9.

Puget Sound Partnership. 2013. 2013 State of the Sound: A Biennial Report on the Recovery of Puget Sound. Tacoma, Washington, 177 pp.

Rapport, D.J., H.A. Regier, and T.C. Hutchinson. 1985. Ecosystem behavior under stress. The American Naturalist 125:617–640.

Rice, J.C., and M.-J. Rochet. 2005. A framework for selecting a suite of indicators for fisheries management. ICES Journal of Marine Science 62:516–527, https://doi.org/10.1016/j.icesjms.2005.01.003.

Rohr, J.R., T. Sager, T.M. Sesterhenn, and B.D. Palmer. 2006. Exposure, postexposure, and density-mediated effects of atrazine on amphibians: Breaking down net effects into their parts. Environmental Health Perspectives 114:46–50, https://doi.org/10.1289/ehp.8405.

Rombouts, I., G. Beaugrand, L.F. Artigasa, J.-C. Dauvin, F. Gevaert, E. Goberville, D. Kopp, S. Lefebvre, C. Luczak, N. Spilmont, and others. 2013. Evaluating marine ecosystem health: Case studies of indicators using direct observations and modelling methods. Ecological Indicators 24:353–365, https://doi.org/10.1016/j.ecolind.2012.07.001.

Samhouri, J.F., A.J. Haupt, P.S. Levin, J.S. Link, and R. Shuford. 2014. Lessons learned from developing integrated ecosystem assessments to inform marine ecosystem-based management in the USA. ICES Journal of Marine Science 71:1,205–1,215, https://doi.org/10.1093/icesjms/fst141.

Samhouri, J.F., and P.S. Levin. 2012. Linking land- and sea-based activities to risk in coastal ecosystems. Biological Conservation 145:118–129, https://doi.org/10.1016/j.biocon.2011.10.021.

Scheffer, M., J., Bascompte, W.A. Brock, V. Brovkin, S.R. Carpenter, V. Dakos, H. Held, E.H. van Nes, M. Rietkerk, and G. Sugihara. 2009. Early-warning signals for critical transitions. Nature 461:53–59, https://doi.org/10.1038/nature08227.

Scheffer, M., S.R. Carpenter, T.M. Lenton, J. Bascompte, W. Brock, V. Dakos, J. van de Koppel, I.A. van de Leemput, S.A. Levin, E.H. van Nes, and others. 2012. Anticipating critical transitions. Science 338:344–348, https://doi.org/10.1126/science.1225244.

Shin, Y.-J., A. Bundy, L.J. Shannon, J.L. Blanchard, R. Chuenpagdee, M. Coll, B. Knight, C. Lynam, G. Piet, A.J. Richardson, and the IndiSeas Working Group. 2012. Global in scope and regionally rich: An IndiSeas workshop helps shape the future of marine ecosystem indicators. Reviews in Fish Biology and Fisheries 22:835–845, https://doi.org/10.1007/s11160-012-9252-z.

Smeets, E., and R. Weterings. 1999. Environmental Indicators: Typology and Overview. European Environment Agency, Copenhagen, Report No. 25, 19 pp.

Suter, G.W. 1999. Developing conceptual models for complex ecological risk assessments. Human and Ecological Risk Assessment 5:397–413, https://doi.org/10.1080/10807039991289491.

Teck, S.J., B.S. Halpern, C.V. Kappel, F. Micheli, K.A. Selkoe, C.M. Crain, R. Martone, C. Shearer, J. Arvai, B. Fischhoff, and others. 2010. Using expert judgment to estimate marine ecosystem vulnerability in the California Current. Ecological Applications 20:1,402–1,416, https://doi.org/10.1890/09-1173.1.

Teixeira, H., Á. Borja, S.B. Weisberg, J.A. Ranasinghe, D.B. Cadien, D.M. Dauer, J.-C. Dauvin, S. Degraer, R.J. Diaz, A. Grémare, and others. 2010. Assessing coastal benthic macrofauna community condition using best professional judgement: Developing consensus across North America and Europe. Marine Pollution Bulletin 60:589–600, https://doi.org/10.1016/j.marpolbul.2009.11.005.

Tett, P., R.J. Gowen, S.J. Painting, M. Elliott, R. Forster, D.K. Mills, E. Bresnan, E. Capuzzo, T.F. Fernandes, J. Foden, and others. 2013. Framework for understanding marine ecosystem health. Marine Ecology Progress Series 494:1–27, http://repository.essex.ac.uk/id/eprint/8549.

Thrush, S.F., J.E. Hewitt, P.K. Dayton, G. Coco, A.M. Lohrer, A. Norkko, J. Norkko, and M. Chiantore. 2009. Forecasting the limits of resilience: Integrating empirical research with theory. Proceedings of the Royal Society B 276:3,209–3,217, https://doi.org/10.1098/rspb.2009.0661.

Thrush, S.F., J.E. Hewitt, C.W. Hickey, and S. Kelly. 2008. Multiple stressor effects identified from species abundance distributions: Interactions between urban contaminants and species habitat relationships. Journal of Experimental Marine Biology and Ecology 366:160–168, https://doi.org/10.1016/j.jembe.2008.07.020.

Vallentyne, J.R. 1999. Extending causality in the Great Lakes basin ecosystem. Aquatic Ecosystem Health Management 2:229–237, https://doi.org/10.1080/14634989908656958.

Ward, T.J. 2014. The condition of Australia’s marine environment is good but in decline: An integrated evidence-based national assessment by expert elicitation. Ocean and Coastal Management 100:86–100, https://doi.org/10.1016/j.ocecoaman.2014.07.012.

Ward, T., S. Cork, K. Dobbs, P. Harper, P. Harris, T. Hatton, R. Joy, P. Kanowski, R. Mackay, N. McKenzie, and B. Wienecke. 2014. Framing an independent, integrated and evidence-based evaluation of the state of Australia’s biophysical and human environments. Journal of Environmental Planning and Management, https://doi.org/10.1080/09640568.2014.891073.

Weisberg, S.B., B. Thompson, J.A. Ranasinghe, D.E. Montagne, D.B. Cadien, D.M. Dauer, D. Diener, J. Oliver, D.J. Reish, R.G. Velarde, and J.Q. Word. 2008. The level of agreement among experts applying best professional judgment to assess the condition of benthic infaunal communities. Ecological Indicators 8:389–394, https://doi.org/10.1016/j.ecolind.2007.04.001.

Zador, S., ed. 2013. Ecosystem Considerations 2013. Appendix C of the BSAI/GOA Stock Assessment and Fishery Evaluation Reports. North Pacific Fishery Management Council, Anchorage, AK, 235 pp.

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