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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Upgrading Marine Ecosystem Restoration Using Ecological‐Social Concepts</title><author><name sortKey="Abelson, Avigdor" sort="Abelson, Avigdor" uniqKey="Abelson A" first="Avigdor" last="Abelson">Avigdor Abelson</name></author><author><name sortKey="Halpern, Benjamin S" sort="Halpern, Benjamin S" uniqKey="Halpern B" first="Benjamin S." last="Halpern">Benjamin S. Halpern</name></author><author><name sortKey="Reed, Daniel C" sort="Reed, Daniel C" uniqKey="Reed D" first="Daniel C." last="Reed">Daniel C. Reed</name></author><author><name sortKey="Orth, Robert J" sort="Orth, Robert J" uniqKey="Orth R" first="Robert J." last="Orth">Robert J. Orth</name></author><author><name sortKey="Kendrick, Gary A" sort="Kendrick, Gary A" uniqKey="Kendrick G" first="Gary A." last="Kendrick">Gary A. Kendrick</name></author><author><name sortKey="Beck, Michael W" sort="Beck, Michael W" uniqKey="Beck M" first="Michael W." last="Beck">Michael W. Beck</name></author><author><name sortKey="Belmaker, Jonathan" sort="Belmaker, Jonathan" uniqKey="Belmaker J" first="Jonathan" last="Belmaker">Jonathan Belmaker</name></author><author><name sortKey="Krause, Gesche" sort="Krause, Gesche" uniqKey="Krause G" first="Gesche" last="Krause">Gesche Krause</name></author><author><name sortKey="Edgar, Graham J" sort="Edgar, Graham J" uniqKey="Edgar G" first="Graham J." last="Edgar">Graham J. Edgar</name></author><author><name sortKey="Airoldi, Laura" sort="Airoldi, Laura" uniqKey="Airoldi L" first="Laura" last="Airoldi">Laura Airoldi</name></author><author><name sortKey="Brokovich, Eran" sort="Brokovich, Eran" uniqKey="Brokovich E" first="Eran" last="Brokovich">Eran Brokovich</name></author><author><name sortKey="France, Robert" sort="France, Robert" uniqKey="France R" first="Robert" last="France">Robert France</name></author><author><name sortKey="Shashar, Nadav" sort="Shashar, Nadav" uniqKey="Shashar N" first="Nadav" last="Shashar">Nadav Shashar</name></author><author><name sortKey="De Blaeij, Arianne" sort="De Blaeij, Arianne" uniqKey="De Blaeij A" first="Arianne" last="De Blaeij">Arianne De Blaeij</name></author><author><name sortKey="Stambler, Noga" sort="Stambler, Noga" uniqKey="Stambler N" first="Noga" last="Stambler">Noga Stambler</name></author><author><name sortKey="Salameh, Pierre" sort="Salameh, Pierre" uniqKey="Salameh P" first="Pierre" last="Salameh">Pierre Salameh</name></author><author><name sortKey="Shechter, Mordechai" sort="Shechter, Mordechai" uniqKey="Shechter M" first="Mordechai" last="Shechter">Mordechai Shechter</name></author><author><name sortKey="Nelson, Peter A" sort="Nelson, Peter A" uniqKey="Nelson P" first="Peter A." last="Nelson">Peter A. Nelson</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26977115</idno><idno type="pmc">4786620</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4786620</idno><idno type="RBID">PMC:4786620</idno><idno type="doi">10.1093/biosci/biv171</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000522</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000522</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Upgrading Marine Ecosystem Restoration Using Ecological‐Social Concepts</title><author><name sortKey="Abelson, Avigdor" sort="Abelson, Avigdor" uniqKey="Abelson A" first="Avigdor" last="Abelson">Avigdor Abelson</name></author><author><name sortKey="Halpern, Benjamin S" sort="Halpern, Benjamin S" uniqKey="Halpern B" first="Benjamin S." last="Halpern">Benjamin S. Halpern</name></author><author><name sortKey="Reed, Daniel C" sort="Reed, Daniel C" uniqKey="Reed D" first="Daniel C." last="Reed">Daniel C. Reed</name></author><author><name sortKey="Orth, Robert J" sort="Orth, Robert J" uniqKey="Orth R" first="Robert J." last="Orth">Robert J. Orth</name></author><author><name sortKey="Kendrick, Gary A" sort="Kendrick, Gary A" uniqKey="Kendrick G" first="Gary A." last="Kendrick">Gary A. Kendrick</name></author><author><name sortKey="Beck, Michael W" sort="Beck, Michael W" uniqKey="Beck M" first="Michael W." last="Beck">Michael W. Beck</name></author><author><name sortKey="Belmaker, Jonathan" sort="Belmaker, Jonathan" uniqKey="Belmaker J" first="Jonathan" last="Belmaker">Jonathan Belmaker</name></author><author><name sortKey="Krause, Gesche" sort="Krause, Gesche" uniqKey="Krause G" first="Gesche" last="Krause">Gesche Krause</name></author><author><name sortKey="Edgar, Graham J" sort="Edgar, Graham J" uniqKey="Edgar G" first="Graham J." last="Edgar">Graham J. Edgar</name></author><author><name sortKey="Airoldi, Laura" sort="Airoldi, Laura" uniqKey="Airoldi L" first="Laura" last="Airoldi">Laura Airoldi</name></author><author><name sortKey="Brokovich, Eran" sort="Brokovich, Eran" uniqKey="Brokovich E" first="Eran" last="Brokovich">Eran Brokovich</name></author><author><name sortKey="France, Robert" sort="France, Robert" uniqKey="France R" first="Robert" last="France">Robert France</name></author><author><name sortKey="Shashar, Nadav" sort="Shashar, Nadav" uniqKey="Shashar N" first="Nadav" last="Shashar">Nadav Shashar</name></author><author><name sortKey="De Blaeij, Arianne" sort="De Blaeij, Arianne" uniqKey="De Blaeij A" first="Arianne" last="De Blaeij">Arianne De Blaeij</name></author><author><name sortKey="Stambler, Noga" sort="Stambler, Noga" uniqKey="Stambler N" first="Noga" last="Stambler">Noga Stambler</name></author><author><name sortKey="Salameh, Pierre" sort="Salameh, Pierre" uniqKey="Salameh P" first="Pierre" last="Salameh">Pierre Salameh</name></author><author><name sortKey="Shechter, Mordechai" sort="Shechter, Mordechai" uniqKey="Shechter M" first="Mordechai" last="Shechter">Mordechai Shechter</name></author><author><name sortKey="Nelson, Peter A" sort="Nelson, Peter A" uniqKey="Nelson P" first="Peter A." last="Nelson">Peter A. Nelson</name></author></analytic><series><title level="j">Bioscience</title><idno type="ISSN">0006-3568</idno><idno type="eISSN">1525-3244</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Conservation and environmental management are principal countermeasures to the degradation of marine ecosystems and their services. However, in many cases, current practices are insufficient to reverse ecosystem declines. We suggest that <italic>restoration ecology</italic>, the science underlying the concepts and tools needed to restore ecosystems, must be recognized as an integral element for marine conservation and environmental management. Marine restoration ecology is a young scientific discipline, often with gaps between its application and the supporting science. Bridging these gaps is essential to using restoration as an effective management tool and reversing the decline of marine ecosystems and their services. Ecological restoration should address objectives that include improved ecosystem services, and it therefore should encompass social–ecological elements rather than focusing solely on ecological parameters. We recommend using existing management frameworks to identify clear restoration targets, to apply quantitative tools for assessment, and to make the re-establishment of ecosystem services a criterion for success.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adger, Wn" uniqKey="Adger W">WN Adger</name></author><author><name sortKey="Hughes, Tp" uniqKey="Hughes T">TP Hughes</name></author><author><name sortKey="Folke, C" uniqKey="Folke C">C Folke</name></author><author><name sortKey="Carpenter, Sr" uniqKey="Carpenter S">SR Carpenter</name></author><author><name sortKey="Rockstrom, J" uniqKey="Rockstrom J">J Rockstrom</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Barbier, Eb" uniqKey="Barbier E">EB. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Bioscience</journal-id><journal-id journal-id-type="iso-abbrev">Bioscience</journal-id><journal-id journal-id-type="hwp">bioscience</journal-id><journal-id journal-id-type="publisher-id">bioscience</journal-id><journal-title-group><journal-title>Bioscience</journal-title></journal-title-group><issn pub-type="ppub">0006-3568</issn><issn pub-type="epub">1525-3244</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26977115</article-id><article-id pub-id-type="pmc">4786620</article-id><article-id pub-id-type="doi">10.1093/biosci/biv171</article-id><article-categories><subj-group subj-group-type="heading"><subject>Forum</subject></subj-group></article-categories><title-group><article-title>Upgrading Marine Ecosystem Restoration Using Ecological‐Social Concepts</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Abelson</surname><given-names>Avigdor</given-names></name></contrib><contrib contrib-type="author"><name><surname>Halpern</surname><given-names>Benjamin S.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Reed</surname><given-names>Daniel C.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Orth</surname><given-names>Robert J.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Kendrick</surname><given-names>Gary A.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Beck</surname><given-names>Michael W.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Belmaker</surname><given-names>Jonathan</given-names></name></contrib><contrib contrib-type="author"><name><surname>Krause</surname><given-names>Gesche</given-names></name></contrib><contrib contrib-type="author"><name><surname>Edgar</surname><given-names>Graham J.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Airoldi</surname><given-names>Laura</given-names></name></contrib><contrib contrib-type="author"><name><surname>Brokovich</surname><given-names>Eran</given-names></name></contrib><contrib contrib-type="author"><name><surname>France</surname><given-names>Robert</given-names></name></contrib><contrib contrib-type="author"><name><surname>Shashar</surname><given-names>Nadav</given-names></name></contrib><contrib contrib-type="author"><name><surname>de Blaeij</surname><given-names>Arianne</given-names></name></contrib><contrib contrib-type="author"><name><surname>Stambler</surname><given-names>Noga</given-names></name></contrib><contrib contrib-type="author"><name><surname>Salameh</surname><given-names>Pierre</given-names></name></contrib><contrib contrib-type="author"><name><surname>Shechter</surname><given-names>Mordechai</given-names></name></contrib><contrib contrib-type="author"><name><surname>Nelson</surname><given-names>Peter A.</given-names></name></contrib><aff id="aff1">Avigdor Abelson (<email>avigdor@tauex.tau.ac.il</email>) is with the Department of Zoology at Tel Aviv University, in Israel. Benjamin S. Halpern is with the Bren School of Environmental Science and Management at the University of California, Santa Barbara. Daniel C. Reed is with the Marine Science Institute at the University of California, Santa Barbara. Robert J. Orth is with the School of Marine Science at the Virginia Institute of Marine Science at the College of William and Mary, in Gloucester Point, Virginia. Gary A. Kendrick is with the School of Plant Biology at the University of Western Australia, in Crawley. Michael W. Beck is with the Global Marine Team of The Nature Conservancy at the Institute of Marine Sciences at the University of California, Santa Cruz. Jonathan Belmaker is with the Department of Zoology at Tel Aviv University. Gesche Krause is with the Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research (AWI), Earth System Knowledge Platform (ESKP), in Bremerhaven, Germany. Graham J. Edgar is with the Institute for Marine and Antarctic Studies at the University of Tasmania, in Australia. Laura Airoldi is with the Centro Interdipartimentale di Ricerca per le Scienze Ambientali and the Dipartimento di Scienze Biologiche, Geologiche ed Ambientali at the Università di Bologna, in Ravenna, Italy. Eran Brokovich is with the Israel Society of Ecology and Environmental Sciences, Israel. Robert France is with the Department of Environmental Sciences at Dalhousie University, in Truro, Nova Scotia, Canada. Nadav Shashar and Noga Stambler are with the Eilat Campus at Ben-Gurion University, in Eilat, Israel; NS is also with the Israel Society of Ecology and Environmental Sciences. Arianne de Blaeij is with the LEI at Wageningen University and Research Centre, in The Hague, The Netherlands. Pierre Salameh is with the Department of Fisheries at the Ministry of Agriculture, in Kiryat Haim, Israel. Mordechai Shechter is with the Natural Resource and Environmental Research Center at the University of Haifa, in Israel. Peter A. Nelson is a senior fish ecologist at H. T. Harvey and Associates, in Los Gatos, California.</aff></contrib-group><pub-date pub-type="epub"><day>16</day><month>12</month><year>2015</year></pub-date><pub-date pub-type="ppub"><day>01</day><month>2</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>16</day><month>12</month><year>2015</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>66</volume><issue>2</issue><fpage>156</fpage><lpage>163</lpage><permissions><copyright-statement>© The Author(s) 2016. Published by Oxford University Press on behalf of the American Institute of Biological Sciences.</copyright-statement><copyright-year>2016</copyright-year><license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/">http://creativecommons.org/licenses/by-nc/4.0/</ext-link>), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact <email>journals.permissions@oup.com</email>.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:href="biv171.pdf"></self-uri><abstract><p>Conservation and environmental management are principal countermeasures to the degradation of marine ecosystems and their services. However, in many cases, current practices are insufficient to reverse ecosystem declines. We suggest that <italic>restoration ecology</italic>, the science underlying the concepts and tools needed to restore ecosystems, must be recognized as an integral element for marine conservation and environmental management. Marine restoration ecology is a young scientific discipline, often with gaps between its application and the supporting science. Bridging these gaps is essential to using restoration as an effective management tool and reversing the decline of marine ecosystems and their services. Ecological restoration should address objectives that include improved ecosystem services, and it therefore should encompass social–ecological elements rather than focusing solely on ecological parameters. We recommend using existing management frameworks to identify clear restoration targets, to apply quantitative tools for assessment, and to make the re-establishment of ecosystem services a criterion for success.</p></abstract><kwd-group><kwd>social–ecological restoration</kwd><kwd>conservation</kwd><kwd>marine ecosystems</kwd><kwd>Ocean Health Index (OHI)</kwd><kwd>marine spatial planning (MSP)</kwd></kwd-group><funding-group><award-group><funding-source id="gs1">Australian Research Council</funding-source><award-id>LP130100155</award-id></award-group></funding-group><counts><page-count count="8"></page-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>February 01, 2016</meta-value></custom-meta></custom-meta-group></article-meta></front><body><p><bold>Marine ecosystems play a crucial role in supporting</bold> human well-being, from our food supply and coastal protection to the regulation of the Earth's climate (figure <xref ref-type="fig" rid="fig1">1</xref>; e.g., Barbier <xref rid="bib2" ref-type="bibr">2012</xref>, Halpern et al. <xref rid="bib23" ref-type="bibr">2012</xref>, HLPE <xref rid="bib25" ref-type="bibr">2014</xref>). Nevertheless, contemporary marine ecosystems are changing, degrading, and disappearing (figure <xref ref-type="fig" rid="fig1">1</xref>; e.g., Waycott et al. <xref rid="bib50" ref-type="bibr">2009</xref>, Beck et al. <xref rid="bib3" ref-type="bibr">2011</xref>, Burke et al. <xref rid="bib9" ref-type="bibr">2011</xref>), a consequence of intensive exploitation together with other anthropogenic local and global effects (e.g., Burke et al. <xref rid="bib9" ref-type="bibr">2011</xref>, IPCC <xref rid="bib27" ref-type="bibr">2013</xref>). Such rapid ecological degradation results in drastic declines in the value of marine ecosystem services and increasing consequential costs to humanity (Barbier <xref rid="bib2" ref-type="bibr">2012</xref>).</p><fig id="fig1" orientation="portrait" position="float"><label>Figure 1.</label><caption><p>Examples of healthy (rich ecosystem services; e.g., food supply, nursery grounds, coastal protection) versus degraded (poor ecosystem services) marine ecosystem sites. (1) Tropical coral reefs: (a) a high-structural-complexity reef, dominated by reef-building corals (Kota Kinabalu, Malaysia), (b) a degraded reef (Ulithi, Yap, Federated States of Micronesia); (2) Mangrove forests: (a) a fully developed forest (Mangal; Solomon Islands), (b) a degraded mangrove site (Rookery Bay, Florida); (3) Seagrass meadows: (a) a <italic>Posidonia australis</italic> meadow (King George Sound, Australia), (b) a stressed <italic>Zostera muelleri</italic> meadow (Tasmania, Australia); (4) Kelp forests: (a) a highly productive giant kelp forest (California), (b) a deforested kelp reef with low productivity and diversity (California); (5) Canopy-forming algal forests: (a) a <italic>Cystoseira balearica</italic> forest (Scandola, Corsica), (b) urchin barrens (Porto Cesareo, Italy). Photographs: 1a C. Storlazzi; 1b A. Abelson; 2a E. Brokovich, 2b C.J. Sapp; 3a G. Kendrick, 3b G. Edgar; 4a,b R. McPeak; 5a E. Ballesteros, 5b P Guidetti.</p></caption><graphic xlink:href="biv171fig1"></graphic></fig><p>Current conservation and natural-resource management are the main countermeasures to this degradation of marine ecosystems (e.g., Gaines et al. <xref rid="bib20" ref-type="bibr">2010</xref>), and they operate primarily by regulating human behavior. These measures include rules crafted to reduce pollution (direct and nonpoint source); laws to protect threatened species (e.g., the US Marine Mammal Protection Act); rules to regulate resource extraction, such as offshore oil wells or seafloor mining; and fisheries regulations. The last include seasons, marine protected areas (MPAs) and other spatial closures, gear restrictions, catch limitations, and bycatch-mitigation measures. MPAs are designed to reduce human impacts—especially those caused by overfishing and habitat destruction—and to increase resilience to natural disturbances and indirect anthropogenic impacts (e.g., De'ath et al. <xref rid="bib15" ref-type="bibr">2012</xref>). However, in many cases, conservation and management as practiced are insufficient to maintain ecosystem health, much less reverse declines and restore ecosystem functions and services (e.g., Lotze et al. <xref rid="bib32" ref-type="bibr">2011</xref>, De'ath et al. <xref rid="bib15" ref-type="bibr">2012</xref>, Parravicini et al. <xref rid="bib37" ref-type="bibr">2013</xref>). For instance, De'ath and colleagues (<xref rid="bib15" ref-type="bibr">2012</xref>) documented a dramatic decline (over 50%) in the cover of live coral (from 28.0% to 13.8%) on Australia's Great Barrier Reef in less than 30 years (between 1985 and 2012). This huge decline at the largest and one of the best-protected coral reef systems in the world is a prominent case that raises questions about the general adequacy of management and protection efforts (Knowlton <xref rid="bib30" ref-type="bibr">2012</xref>), as well as the use of MPAs as the primary tool for conservation and the optimal conditions for natural recovery.</p><p><italic>Natural recovery</italic>, the process by which an ecosystem returns to a prior state following the cessation of some impact or alteration, is often a slow process that can take decades or even centuries (Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref>, Lotze et al. <xref rid="bib32" ref-type="bibr">2011</xref>). For example, the recovery of fished stocks relies on the natural system to recover at its own rate, and in some cases (e.g., North Atlantic cod), recovery has not occurred. In severe cases, a return to the “historic natural” state is not likely to occur in a reasonable time scale (e.g., Lotze et al. <xref rid="bib32" ref-type="bibr">2011</xref>). However, if we are able to identify the specific recovery inhibitors (e.g., phase-shift attractors) and these can be overcome by certain interventions, then this lengthy process may be dramatically shortened. Such identification and intervention are the essence of ecological restoration (e.g., Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref>, Suding <xref rid="bib45" ref-type="bibr">2011</xref>), in which <italic>ecological restoration</italic> is defined as the process of assisting the recovery of damaged, degraded, or destroyed ecosystems (e.g., Hobbs <xref rid="bib26" ref-type="bibr">2004</xref>).</p><p>Given that conservation and sustainable management likely require more than MPAs or fisheries regulations alone to be effective, we suggest that the scientific discipline of <italic>restoration ecology</italic>, defined as the science underlying the concepts and tools needed to restore ecosystems (SER <xref rid="bib44" ref-type="bibr">2004</xref>), needs to become an integral element for marine conservation, natural resource management, and sustainable development (MEA <xref rid="bib34" ref-type="bibr">2005</xref>, Suding <xref rid="bib45" ref-type="bibr">2011</xref>). Restoration ecology is a relatively young scientific discipline (e.g., Suding <xref rid="bib45" ref-type="bibr">2011</xref>), especially so in the marine environment, and wide gaps still exist among current implementation methods, approaches and standards, and the supporting science (e.g., Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>, Suding <xref rid="bib45" ref-type="bibr">2011</xref>, Duarte et al. <xref rid="bib17" ref-type="bibr">2014</xref>). In the marine context, this misalignment is exacerbated by (a) real or apparent inequalities between project cost and economic benefits (e.g., Cesar <xref rid="bib10" ref-type="bibr">2000</xref>) and the consequent inability to scale-up projects (e.g., Adger et al. <xref rid="bib1" ref-type="bibr">2005</xref>, Mumby and Steneck <xref rid="bib35" ref-type="bibr">2008</xref>); (b) treating symptoms rather than the causes (e.g., Mumby and Steneck <xref rid="bib35" ref-type="bibr">2008</xref>); and (c) confusing the semantics of <italic>restoration</italic> with inconsistent, conflicting, and sometimes overlapping terms (Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>, Duarte et al. <xref rid="bib17" ref-type="bibr">2014</xref>).</p><p>Vague or undefined restoration evaluation criteria present further obstacles to linking marine science with the practice of ecological restoration (e.g., Ruiz-Jaen and Aide <xref rid="bib41" ref-type="bibr">2005</xref>, Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>). Restoration evaluations typically are carried out by measuring state variables and ecological processes, which are based on scientific methods indicating ecosystem performance (Palmer and Filoso <xref rid="bib36" ref-type="bibr">2009</xref>). Such measurements are often complicated, and the evaluation of many restoration projects often falls short of reliable (Palmer and Filoso <xref rid="bib36" ref-type="bibr">2009</xref>). Moreover, using ecological metrics (e.g., species diversity) has proven to be inefficient for restoration assessment in many cases (Palmer and Filoso <xref rid="bib36" ref-type="bibr">2009</xref>). These shortcomings should be tackled if we are to realize the potential for using ecological restoration as an effective management tool and reversing the decline of numerous degraded marine ecosystem sites and their deteriorating services.</p><sec id="sec1"><title>Marine ecosystem restoration: Basic ecological goals</title><p>Ecological restoration encompasses multiple forms of intervention (e.g., restoration, rehabilitation, and reclamation—or replacement; points A, C, C’, and C” in figure <xref ref-type="fig" rid="fig2">2</xref>; for further definitions, such as of <italic>remediation, mitigation</italic>, and <italic>compensation</italic>, and recommended terminology, see Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>). These various forms differ in the way they affect the biota and/or physical conditions at a site in order to restore the structure and function of the original state (figure <xref ref-type="fig" rid="fig2">2</xref>; e.g., Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref>). The ideal aim of many ecological-restoration projects is to return the system to its past <italic>natural</italic> state (i.e., a state comparable to one unaffected by modern anthropogenic disturbance; point A in figure <xref ref-type="fig" rid="fig2">2</xref>; e.g., Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref>). Alternatively, the goal of restoration may be to bring the target habitat to a healthier state (i.e., a “self-maintaining, vigorous, resilient state to externally imposed pressures, and able to sustain services to humans…”; points C,C’,C” in figure <xref ref-type="fig" rid="fig2">2</xref>; Tett et al. <xref rid="bib48" ref-type="bibr">2013</xref>). Under other circumstances, restoration may focus on repairing the structure and function of degraded systems to some extent (figure <xref ref-type="fig" rid="fig2">2</xref>; see Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref> and Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref> for different definitions) or providing some function where missing (e.g., ports or other marine urban environments; Dafforn et al. <xref rid="bib12" ref-type="bibr">2015</xref>). A key question, then, is, “What can be done in those common cases where neither natural processes nor changes in resource management will return the ecosystem to its original state in a reasonable time frame?” (figure <xref ref-type="fig" rid="fig2">2</xref>). Examples of slow-recovering, or stable, degraded states may include: (a) the physical destruction of habitat-engineering species (e.g., a flattened reef area after years of blast fishing or severe storms), with natural recovery expected to take many years or decades (e.g., reef-building corals, mangroves, and seagrasses; Lotze et al. <xref rid="bib32" ref-type="bibr">2011</xref>); (b) extreme biotic changes (e.g., invasive pest species, overfished stocks, or replacement by new ecological engineering taxa), which can shift the system to a different state (i.e., phase shift; e.g., coral to macroalgae; Graham et al. <xref rid="bib22" ref-type="bibr">2015</xref>); or (c) extreme abiotic changes of either water quality (e.g., from oligotrophic to eutrophic) or substratum type (hard substrate, soft bottom, or change of sediment grain size) due to off-site activities, such as those occurring upstream or in adjacent watersheds.</p><fig id="fig2" orientation="portrait" position="float"><label>Figure 2.</label><caption><p>A schematic illustration of the effects of restoration interventions (e.g., restoration, rehabilitation, and reclamation) on ecosystem structure (e.g., species diversity and structural complexity) and ecosystem function (e.g., nutrient content and cycling as well as productivity), illustrating changes that occur as a degraded ecosystem (State B) recovers toward its original state (A). Practices which lead to partial recovery are termed <italic>rehabilitation</italic> (C), in which practices that improve either or both the ecosystem structure or function—but not toward the original state (A)—are termed <italic>reclamation</italic> (C’ and C”; after Dobson et al. <xref rid="bib16" ref-type="bibr">1997</xref>).</p></caption><graphic xlink:href="biv171fig2"></graphic></fig><p>Given these dramatic adverse changes, ecological restoration, if appropriate, should be applied to address any of three potential overall goals: (1) to accelerate recovery in the case of slow natural recovery processes, (2) to enable recovery when systems are stuck in alternative, less desirable states, or (3) to change the structure and/or function in cases of extreme decline of ecosystem services to form a healthy ecosystem, even if it differs from what we understand to have existed prior to human interference, and to enable the renewal of services in the form of a “target-designed novel ecosystem.” All three objectives include the expectation of improved ecosystem functionality and the attendant ecosystem services. If improved ecosystem services are defined as a key goal, then the restoration efforts should focus on social–ecological elements rather than solely on ecological-restoration ones (figure <xref ref-type="fig" rid="fig3">3</xref>).</p><fig id="fig3" orientation="portrait" position="float"><label>Figure 3.</label><caption><p>A schematic illustration of the effects of restoration interventions on ecosystem structure, ecosystem function, and ecosystem services, illustrating the hypothetical scenarios that may occur as degraded ecosystems either recover toward their original state or shift toward other improved directions (C–F). Arrays A’ to C’, correspond to figure <xref ref-type="fig" rid="fig2">2</xref>; B,B’ to the degraded ecosystem; D to improved function, structure, and services (e.g., the removal of stressors, which enables the partial or complete recovery of the ecosystems); E to the declined function and slight improvement of structure and services (e.g., the transplantation of a single habitat-engineering species); F to improved function and structure but no significant change in services (e.g., the restoration of a reef-table community with species that cannot improve coastal protection); G to no improvement of the structure and function of a given ecosystem site but improved locally needed services (e.g., enhanced food supply related to the creation of alternative habitat sites, such as artificial reefs).</p></caption><graphic xlink:href="biv171fig3"></graphic></fig></sec><sec id="sec2"><title>The concept of social–ecological restoration</title><p>Marine ecosystems are tightly linked to coastal human communities (social–ecological systems, <italic>sensu</italic> Berkes and Folke <xref rid="bib6" ref-type="bibr">1998</xref>, Kittinger et al. <xref rid="bib29" ref-type="bibr">2012</xref>), which reciprocally affect each other. By the term <italic>marine ecosystems</italic>, we refer here to a wide range of benthic marine ecosystems, from supralittoral and intertidal environments to subtidal environments. The overexploitation of marine ecosystems and natural resources can degrade life-supporting systems, such as coral reefs and mangrove forests, which, in turn, dramatically influence the quality of life and well-being of associated communities. Poverty in fishery-supported communities in developing countries, for example, is correlated with the decline of coastal ecosystems and their services (Béné <xref rid="bib4" ref-type="bibr">2003</xref>, <xref rid="bib5" ref-type="bibr">2009</xref>, Leisher et al. <xref rid="bib31" ref-type="bibr">2013</xref>). The strong interactions between human societies and marine ecosystems that define a social–ecological system should be considered in developing operative restoration plans, integrating effective tools and focused goals where degradation has led to declines in ecosystem services (e.g., the three examples of slow-recovering degraded states that we described above).</p><p>There is a growing literature on the socioeconomic aspects of the resilience, recovery, and ecosystem services of marine systems (e.g., Adger et al. <xref rid="bib1" ref-type="bibr">2005</xref>, Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>, Duarte et al. <xref rid="bib17" ref-type="bibr">2014</xref>). Within this literature, attention has focused on the social aspects of fishery management and establishing marine reserves (e.g., Hilborn <xref rid="bib24" ref-type="bibr">2007</xref>, Pollnac et al. <xref rid="bib39" ref-type="bibr">2010</xref>, Unsworth and Cullen <xref rid="bib49" ref-type="bibr">2010</xref>), whereas relatively few studies have dealt with the social aspects of marine ecological restoration (e.g., Elliott et al. <xref rid="bib18" ref-type="bibr">2007</xref>). Nevertheless, a disregard for the socioeconomic components in conservation projects can lead to failures (Bode et al. <xref rid="bib7" ref-type="bibr">2008</xref>, Polasky <xref rid="bib38" ref-type="bibr">2008</xref>), such as “paper parks.” These situations typically result when MPA planners fail to address stakeholder conflicts or disregard their values in the planning process; in these instances, local communities often ignore reserve boundaries, leading to a “failed” reserve (e.g., Bode et al. <xref rid="bib7" ref-type="bibr">2008</xref>). Similar outcomes can also occur when ecological-restoration projects lack socioeconomic dimensions. That is, restoration efforts that only focus on improving the structure and function of ecosystems while disregarding the needs of relevant stakeholders who are often the most direct recipients of ecosystem services will rarely succeed.</p><p>We recommend the use of ecosystem services (figure <xref ref-type="fig" rid="fig3">3</xref>; presented as a third axis in the model of restoration effects on ecosystem structure and function) and socioeconomic aspects as part of an integrated approach for planning, executing, and evaluating or monitoring restoration projects. The <italic>ecosystem-services</italic> concept describes and emphasizes the diverse benefits and uses of ecosystems to human society (see figure <xref ref-type="fig" rid="fig4">4</xref> for examples; MEA <xref rid="bib34" ref-type="bibr">2005</xref>). The application of this concept, which is gaining interest among scientists and policymakers, can facilitate collaboration between them and relevant practitioners and reduce conflicts among stakeholders (Tallis et al. <xref rid="bib47" ref-type="bibr">2012</xref>, Kelble et al. <xref rid="bib28" ref-type="bibr">2013</xref>). An example of the increased interest in including ecosystem services in decisionmaking processes is The Economics of Ecosystem Services and Biodiversity (TEEB) initiative, a global initiative focused on drawing attention to the economic benefits of biodiversity, including the growing cost of biodiversity loss and ecosystem degradation. The TEEB approach consists of recognizing value, demonstrating value, and capturing value (Sukhdev et al. <xref rid="bib46" ref-type="bibr">2014</xref>). Objections to the approach have been raised but have been well addressed (see Schröter et al. <xref rid="bib42" ref-type="bibr">2014</xref>). Another example, specific to marine ecosystems, that represents a shift from an exclusive focus on adverse anthropogenic impacts on ecosystems to a holistic management approach and includes ecosystem services is presented by Kelble and colleagues (<xref rid="bib28" ref-type="bibr">2013</xref>). In their conceptual model, they combine the widely applied conceptual model of driver, pressure, state, impact, and response (DPSIR) with an ecosystem-based management model that also incorporates positive changes in the ecosystem and its services (i.e., driver, pressure, state, ecosystem service, and response; EBM-DPSER; Kelble et al. <xref rid="bib28" ref-type="bibr">2013</xref>).</p><fig id="fig4" orientation="portrait" position="float"><label>Figure 4.</label><caption><p>Case studies of marine ecosystem restoration projects designed to restore or mitigate for lost ecosystem services, notably coastal protection, seabed stabilization, food supply, nursery habitats, carbon sequestration (“blue carbon”), and tourism attractions. (a) A replaced kelp forest, established on an artificial reef (i.e., deployed rocks) on a sandy seabed, in an alternative site to mitigate for the loss of a kelp forest damaged by a power plant, the San Onofre Nuclear Generating Station (California; a project by UCSB). (b) Restored salt marshes, which are part of the coastal defense strategy to protect the city of Venice and the Venetian Lagoon from flooding (Italy; the MOSE project by Consorzio Venezia Nuova). (c) A constructed oyster reef in the Gulf of Mexico as part of the living shoreline efforts (Alabama; a project by The Nature Conservancy). (d) A seagrass meadow of <italic>Posidonia australis</italic> restored three decades after having been heavily affected by eutrophication (Cockburn Sound, Perth, Western Australia; a project by Murdoch University). Photographs: (a) Richard Herrmann, (b) Laura Airoldi, (c) Jeff DeQuattro, and (d) Jennifer Verduin.</p></caption><graphic xlink:href="biv171fig4"></graphic></fig><p>Ecosystem services can be linked to ecosystem structure and function (Tett et al. <xref rid="bib48" ref-type="bibr">2013</xref>) but are also interconnected to human behavior and resource-exploitation levels, both of which affect the two former parameters. It is important, however, to distinguish between ecosystem services and ecosystem functions (figure <xref ref-type="fig" rid="fig3">3</xref>; Schwerdtner Manez et al. <xref rid="bib43" ref-type="bibr">2014</xref>): <italic>Ecosystem functions</italic> are the chemical, physical, and biological interactions associated with ecosystems, whereas <italic>ecosystem services</italic> depend on these functions but are different—they are the aspects of the ecosystem valued by people (Boyd and Banzhaf <xref rid="bib8" ref-type="bibr">2005</xref>) and do not necessarily present the same trends as the ecosystem structure and function (figure <xref ref-type="fig" rid="fig3">3</xref>).</p><p>The translation of ecosystem structure and function into ecosystem services requires an interdisciplinary approach (Daily et al. <xref rid="bib14" ref-type="bibr">2009</xref>). The structure and function of ecosystems expressed by the provision of ecosystem services can be described by ecological production functions (Daily et al. <xref rid="bib13" ref-type="bibr">2000</xref>). A better-informed decisionmaking process for restoration management can be made by making explicit all of the costs and benefits that affected people obtain from restored versus nonrestored marine ecosystems. This approach may be implemented using <italic>ecological production functions</italic> (Daily et al. <xref rid="bib14" ref-type="bibr">2009</xref>), which includes (a) the translation of the structure and function of ecosystems into the possible provision level of the services to humans; (b) the assessment of the real provision of these services, which depends on the human demand for these services and on identifying the stakeholders who are expected to benefit from the ecosystem restoration; and (c) the implementation of economic valuation methods to make different costs and benefits comparable in monetary terms.</p></sec><sec id="sec3"><title>Implementing and assessing social–ecological restoration</title><p>Restoring single species or particular ecosystem functions can in theory be straightforward but may succeed at the cost of other ecosystem elements. Understanding such trade-offs and helping guide restoration toward outcomes that meet multiple objectives require focusing on healthy ecosystems, but it can be difficult to quantitatively define a healthy ecosystem. If <italic>healthy ecosystems</italic> are those able to supply a full range of ecosystem services (e.g., Palmer and Filoso <xref rid="bib36" ref-type="bibr">2009</xref>, Tett et al. <xref rid="bib48" ref-type="bibr">2013</xref>; see also Schröter et al. <xref rid="bib42" ref-type="bibr">2014</xref>), then the social–ecological concept can provide a framework for setting realistic restoration goals and effective and reliable assessment parameters. Alternatively, if there is an easy-to-assess and high-value service that a given ecosystem provides, restoration interventions are likely to be funded and implemented, regardless of the expected health state—or the full range of ecosystem services—of the restored ecosystem (see figure <xref ref-type="fig" rid="fig4">4</xref> for examples).</p><p>The current focus on integrated coastal zone management (ICZM; European Commission <xref rid="bib19" ref-type="bibr">2007</xref>), ecosystem-based management (EBM; McLeod and Leslie <xref rid="bib33" ref-type="bibr">2009</xref>), and marine spatial planning (MSP; Gilliland and Laffoley <xref rid="bib21" ref-type="bibr">2008</xref>; also termed as coastal and marine spatial planning, CMSP) offers existing management frameworks within which to embed social–ecological restoration and helps to refine restoration targets and provide quantitative tools for assessment. The MSP concept can serve as a framing platform that directs restoration intervention toward specific focused goals; thus, the social–ecological restoration outcomes are expected to improve ecosystem services, which in turn will improve the MSP achievements by alleviating conflicts and enhancing the services supplied to society. Specifically, we believe that social–ecological restoration can help to achieve the goals of MSP in parallel with the ecosystem-services framework approach in two ways: First, this combined approach provides the tools to improve the ecosystem-services value by enhancing supply or by lowering the impact of exploitation via mitigation and therefore may enable enhanced direct and/or indirect use. Second, it can help by creating alternative incentives to conserve and restore ecosystem services and improve their sustainable supply. To be applicable, the MSP concept needs a comprehensive framework that considers a broad range of uses and accurately evaluates the suite of benefits (ecosystem services) humans receive from the oceans. However, at present, marine ecosystem services are often categorized under broad definitions and are roughly estimated or measured in different ways (Tallis et al. <xref rid="bib47" ref-type="bibr">2012</xref>, Schwerdtner Manez et al. <xref rid="bib43" ref-type="bibr">2014</xref>). A novel approach suggested by Tallis and colleagues (<xref rid="bib47" ref-type="bibr">2012</xref>) addressed many of the shortcomings noted above by using a three-step framework that, in addition to creating a refined classification of ecosystem services, emphasizes the importance of measuring ecosystem services at three distinct points along the ecosystem-services production chain: supply, service, and value. We suggest taking this approach further by incorporating social–ecological restoration as an additional tool in a reciprocal framework.</p><p>Assessing the success of social–ecological restoration in turn requires metrics of overall ocean health. The recent development of the Ocean Health Index (OHI; Halpern 2012) provides one such metric. The OHI is a systematic approach for measuring the overall condition of marine ecosystems and treats nature and people as integrated parts of a healthy system (Halpern et al. <xref rid="bib23" ref-type="bibr">2012</xref>). It can provide a powerful tool to direct resource management and improve policy, which also may include restoration interventions, if needed (Halpern et al. <xref rid="bib23" ref-type="bibr">2012</xref>). With repeated assessments over time, the OHI can be used to assess whether or how restoration actions affect each dimension of ocean health (e.g., ecosystem service) separately and altogether. In combination with other tools that model ecosystem-service provision under different management scenarios (such as InVEST; Daily et al. <xref rid="bib14" ref-type="bibr">2009</xref>) or evaluate likely change in ecosystems (such as Bayesian network based risk assessments), the OHI can also be used to evaluate how restoration activities may alter ocean health in the future.</p></sec><sec sec-type="conclusions" id="sec4"><title>Conclusions</title><p>Marine ecosystems are degrading at accelerated rates that jeopardize essential ecosystem services for human society. Unfortunately, our present management approaches and tools are inadequate to address the problem, and an urgent need exists to bridge the gaps among science, policy, and on-the-ground practice.</p><p>Ecological restoration cannot provide a substitute for the conservation of ecosystems, but where ecosystems are already heavily degraded, it may be a necessary and even a more effective management strategy. Natural recovery is preferred (ecologically and economically) over active restoration interventions. If, after the removal of significant stressors, natural recovery is expected to occur in a reasonable time scale, this is likely to emerge as the management priority. However, in cases in which the major stressor(s) cannot be removed or significantly reduced, when changes are beyond recovery because of the different trajectories of degradation and recovery (e.g., Lotze et al. <xref rid="bib32" ref-type="bibr">2011</xref>, Suding <xref rid="bib45" ref-type="bibr">2011</xref>), or when economic or social reasons motivate accelerating the recovery (even if the system would recover on its own), restoration interventions should be considered and implemented as essential elements of ecosystem management.</p><p>The strong link between human societies and marine ecosystems is a key element in applied ecological restoration and therefore should be integrated in restoration plans, especially in developing countries, where local stressors often play a stronger role than global stressors (e.g., Burke et al. <xref rid="bib9" ref-type="bibr">2011</xref>). In this regard, we propose testing the application of management frameworks (e.g., the OHI and MSP) as potentially effective tools for focusing restoration goals and providing more effective and reliable assessment. Incorporating the social–ecological restoration element is expected to compensate for the relatively low supply of ecosystem services, which is drastically below its potential (or former supply) because of misuse and overexploitation.</p><p>Overall, the development of effective, scalable restoration tools and approaches will inevitably be complicated by its broad multidisciplinary nature. Therefore, whatever the future direction, if ecological restoration is to result in reliable applied science, then strong collaboration will be required among ecological, economic, and social experts, as well as with private and public stakeholders, to encompass a diverse array of fields into a transdisciplinary co-designed approach.</p></sec></body><back><ack><p>This study was conducted as a part of the Marine Ecological Restoration Working Group (MER-WG) workshop held in Eilat, Israel, by the Red Sea. Thanks are due to Israel's Ministry of Environmental Protection and the Israel Society of Ecology and Environmental Sciences, whose support enabled the workshop and the US National Science Foundation (OCE-1232779) for assistance with publication costs. The MER workshop was held at the InterUniversity Institute (IUI) for Marine Sciences, in Eilat. We wish to thank the Dolphin Reef, in Eilat, for their help and support; Dr. Sinaia Netanyahu for her support; and the directors and staff of the IUI for their help and hospitality. This article is contribution no. 3501 of the Virginia Institute of Marine Science at the College of William and Mary. Gary Kendrick's travel to the workshop was funded through an Australian Research Council Linkage grant (no. LP130100155). Thanks are due to Ron McPeak, Cynthia Sapp (courtesy of Coastal Resources Group, Inc., in Venice, Florida), Enric Ballesteros, Paolo Guidetti, Richard Herrmann, Jeff DeQuattro, and Jennifer Verduin for their contributed photos. 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