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Articles Marine Ecosystem-based Management in Practice: Scientific and Governance Chaiienges MARY RUCKELSHAUS. TERRIE KLINGER. NANCY KNOWLTON. AND DOUGLAS R DEMASTER Ecosystem-based management (EBM) in the ocean is a relatively new approach, and existing applications are evolving from more traditional tnanagement of portions of ecosystems. Because comprehensive examples of EBM in the marine enviroiune?n do not yet exist, we ftrst summarize EBM principles that eitiergefrom the fisheries and marine social and ecological literature. We then opply those principles to four cases in which large parts of marine ecosystems are being managed, and iisk how inchuUng additional components of an EBM approach might improve the prospects for those ecosystems. The case studies provide examples of how additional elements of EBM approaches, if applied, could improve ecosystem function, in particular, two promising next steps for applying EBM are to identif}' management objectives for the ecosystem, including natural and human goals, and to ensure that the governance structure matches with the scale over which ecosystem elements are measured and managed. Keywords: frsheries, marine food webs, marine ecosystem-based management, I arine ecosystems are complex adaptive systems linkcti .ILTOSS tnultipic scales by llovv ot water and species movements (Levin and Lubchenco 2008). Despite their adaptive character and often rediindLint linkages, marine ecosystems are vulnerable to rapid changes in diversity and function (Pulumbi et al. 2008). Observable, widespread declines in the status of species, habitats, and ecosystem hinction in the marine environment have led to calls for ecosystembased management (EBM) as a solution for what ails the oceans (POC 2003, USCOP 2004). The argument that EBN4 could maintain ecosystem structure—thus allowing the ecosystem to maintain redundancies and resilience to environmental change—is appealing, yet not well tested. Why is there growing consensus that EBM is a promising approach for managing oceans? In short, marine ecosystems are in trouble, indicating that many previous attempts to manage individual threats in the absence of a system-wide approach have nol worked. Dramatic declines in some marine species caused by overfishing provide striking examples of failed management practices and ineffective governance in the face of imperfect scientific knowledge (Lotze et ai. 2006, Hilborn 2007). These high profile failures in single-species fisheries management led, in the mid-1990s, to efforts by the US Congress to mandate improvements in governance and a broader, more ecological approach. For example. Congress required that www.biosciencemag.org marine ecosystems, ocean zoning Fishery Management Plans identify habitat essential for the productivity of a species or stock (i.e., "essential fish habitat"). Essential fish habitat and other habitat-based approaches have the potential to offer proteclion for more than just a focal species, but their ancillary benefits to nontarget species are not well understood. In the late 1990s, academic scientists, natural resource agencies, and nongovernmental organizations began to promote the use of networks of marine protected areas (MPAs) as a management tool to help address the problem of uncoordinated, piecemeal approaches to protecting marine species and habitats (US White House 2000, Lubchenco et al. 2003). The objectives of MPA networks include the enhancement offisheriesyields and protection of marine species and communities. Within their boundaries, effective MPA networks incorporate linkages among habitats that meet the Mary Ruckelshaus (e-mail: mary.rucketshaus&noati.gov) Is with the NOAA (National Oceanic and Atmospheric Administration) Northwvst Fisheries Science Center in Seattle, Washington. Terrie Klinger is with the School of Marine Affairs at the University of Washington in Seattle. Nancy Knowlton is with the Center for Marine Biodiversity and Conservation at Scripps Institution of Oceanography in La lolla, California. Douglas P. DeMaster is wiih the NOAA Fisheries-Alaska Fisheries Science Center in Seattle. ® 2008 American Institute of Biological Sciences. January 2008 / Vol. 58 No. I • BioScience 53 Articles biological requirements of multiple species throughout their life-history stages (e.g., Sala et al. 2002); such networks may increase the resilience of systems to large-scale threats. Consequently, MPA networks can contribute as one tool within an ecosystem-based approach to ocean management, but they are not appropriate management tools for all species (e.g., highly migratory species) or all potential fiictors contributing to species declines (e.g., nonindigenous species, pollution, social phenomena; Hilborn et al. 2004). FiniiUy, MPAs may not be effective in restoring the abundance of target species in the face of global threats such as climate warming and disease (Jones etal. 2004). Two national panels recently reviewed the status of US oceans and concluded that marijie resources should be managed with a comprehensive, ecosystem-based strategy (POC 2003, USCOP 2004). The panels suggested that such a strategy should balance the interests of diverse stakeholder groups, consider the status of both target and nontarget species, incorporate networks of MPAs to protect habitats and their associated biota, and adopt an overarching system of ocean zoning to coordinate regulation of human activities in particular areas at particular times. At the core of most descriptions of EBM approaches is the fundamental importance of considering factors that drive human behavior and the choices we make regarding our use of and interactions with marine resources (USCOP 2004, Rosenberg and McLeod 2005). The EBM concept has received a good deal of attention in theory (NRC 1996,2006), and has been adopted in principle by some entities charged with managing ocean resources (e.g., NMFS 1999). However, examples of comprehensive approaches to marine EBM are rare. The dearth of cases most likely reflects incomplete scientific information and the difficulties inherent in implementing large-scale management strategies within the complex natural and socioeconomic systems characteristic of ocean governance. If EBM applications in the oceans are rare, estimates of success, or feedback on what approaches are likely to succeed in achieving ecosystem objectives, are rarer still. Although implementation ofthe fliU complement of EBM principles in the ocean is in its infancy, there are regional cases that essentially are "learning by doing" through management of portions of ecosystems towards a subset of ecosystem objectives. This growing number of management applications can help us see the way forward. In this article, we illustrate how a few guiding principles borrowed trom marine ecological,fisheries,and socioeconomic theory can be combined with case studies to develop a fuller application of EBM in marine environments. Guiding principles for putting marine EBM into practice: Case examples Implementing an EBM approach in the ocean requires us to think broadly Broadening the scope of any EBM plan for the oceans will require considering food-web interactions, drivers of ecosystem function, and how human activities interact with species and ecosystem services. On the basis of existing guidance from national and international fisheries manage54 BioScience • January 2008 / Vol. 58 No. I ment organizations (NMFS 1999, FAO 2003), a combination of ecological and socioeconomic theory, and lessons from existing test cases in marine environments, we summarize six basic principles that characterize EBM approaches in the oceans (box 1; POC 2003, USCOP 2004). Our objective here is to illustrate how some of these general principles are being used in partially developed EBM approaches in four specific marine and coastal areas around the world. The examples we offer illustrate how ecological principles have been combined with considerations of human use patterns to design improved management approaches that constitute the beginnings of a comprehensive EBM strategy for marine species and habitats. In each setting, we specify additional EBM principles that might be included to achieve broader ecosystem objectives. The waters of the Southern Ocean surrounding Antarctica Ecosystem-based tlshery management has been practiced in the waters surrounding Antarctica since the early 1980s, but management in the region currently lacks comprehensive ecosystem objectives, indicators, and management strategies to incorporate the full ecosystem consequences of the fisheries into a broader context (box 2). The Southern Ocean waters are highly productive, andfisheriesfor marine mammals, fish, and invertebrates have been in operation there for about two centuries. Since 1982, management of Antarctic marine resources has been regulated by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), whose membership consists of representatives of Antarctic Treaty nations, and whose mandate is to conserve the Antarctic marine ecosystem. The CCAMLR has pioneered an ecosystem approach to fisheries management. The goal of this approach is to avoid significant adverse impacts both on target species and on nontarget ecosystem components that are dependent on fished species or affected by fisheries in other ways, for example, through trophic interactions or bycatch (Kock 2000, Constable 2001). The primary species groups included in the Antarctic marine ecosystem arc krill and Other zooplankton, squid,finfish,v^de-ranging seabirds such as petrels and albatrosses, penguins, and marine mammals such as seals and toothed and baleen whales (figure 1). All of these species groups either have been directly commercially harvested or have suffered incidental mortality due to fishing activities (Constable 2004). The CCAMLR's mandate is to coordinate the management of all marine species in the Southern Ocean ecosystem, except for seals south of 6O''S and whales, which are covered under different maiiagement agreements (CCAMLR 2006). The krill fishery illustrates the CCAMLR's approach to ecosystem-based management. Kril! [Euphansia sitpcrba) is an important forage species for Antarctic predators, and also has become an important commercial species. In response to concern over high harvest rates, the CCAMLR developed and used models to determine sustainable rates of krill removal. These rates were then modified to account for the www.biosciencemag.org Articles Box 1 . Six basic principles for using an ecosystem-based management framework to manage marine resources. 1. Define the spariai boundaries of the marine ecosystem to be managed. The spatial extent of the ecosystem determines which species, other ecosystem attributes, and human activities iire the focus ol management. So-called large marine ecosystems already have been delineated on the basis of large-scale biological, gcomorphological, and hydrological features (see the figure below; Sherman 1995). The US Commission on Ocean Policy further recommends including watersheds (hat affect nearshore ecosystems within their boundaries (USCO1-' 20041. Because sociopolitical feedbacks and variation in ecosystem responses to environmental conditions may occur at smaller spatial scales than those over which large-scale ecological processes operate (Hutton and Leader-Williams 2003, Adger et al. 2005), nesting several ecosystem management efforts within larger ecosystems may be advisable. 2. Develop a clear statement of the objectives of ecosystem-based management (EBM). What biological and social values are desired from an ecosystem? For example, one aim of EBM could be to maximize overall ecosystem yield and benefits to society of total fishery harvests (Hilborn 2007). Alternatively, the objective of EBM could be to reach target levels ctf ecosystem services such as nutrient cycling or toxics filtering and ecosystem properties such as resilience in ecosystem dynamics, biodiversity, redundancy, and modularity (e.g., Rosenberg and McLeod 2005, Levin and Lubchenco 2008, Palumbi et al. 2008). Working through a deliberative political process to get broad agreement on the objectives helps tremendously in subsequent discassions about how to achieve ecosystem goals. 3. Include humans in characterizations of marine ecosystem attributes and indicators of their response to cbange. There is growing consensus among biologists .intl pt)licyniakcrs thai iiicluJing human u.ses of and interaclions with natural resources in KBM approaches improves the likelihood of achieving desired ecosystem outcomes (POC 2003, USCOP 2004, Hennessey and Sutinen 2005, Hiiborn 2007), It is important to be clear in articulating what natural- and human-system attributes of the ecosystem best indicate the status of the desired objectives .so that progress can be tracked over time and adjustnienis in strategics can be made as needed (e.g., Adger et al. 2005, Livingston et al. 2005). Large Marine Ecosystems of the World I) Cnt BerngSH ])Guir or Alaska iliromu Cumnl jir Df Califnmn )GuliiirM»iLE ) Soutnna us Centmcfltai S M ' ) Nortfwnt US CwMrwwtal Slwtf CiBn snc(t 9} hifHtauMiine-\.atmaor Shel' 101 (nsulsr I«cinc-Howsllan I1) Pacific Cantral'American Ccaslal www.biosciencemag. org 13) o I ) } HumBoWt Currant M l PMsgonlart Shall 15) South Biaill Shell 16) Eisi Brazil Shell 17) North Bniil SMt IS) West Greenland Shell 19)E««GrKnland5t»tf 20) BarvXt Sa 21) Nonwglsn Set }2> North Sci 27) IB) 29) 30) 31) Canary Current GubnMCurrsm aenguela Current Atjul^ai Current Somali Coastal Current 34) Btv a 3S} Gulf or Thailand 36) south CMru S«a 37) Sulu'Celebes Sea }B) tnaonnitn See %9) Ntvtti Australian SlwH 10) HantfBSI AunralLDn Shcir •li) EBttCerilral«uHr»IHr>5httl 42) Southeast Auttnllsn Shell 4}) Scutnwest AuUmllan Shelf 44) Weacentml A u n n l l l n Sneir S7) Laptev sea SB) Kara Sea *e) Sei 50) 51) 5J) 53) H) SS) Sea of Japan Oyashio Cummi Sea Of OkhotsK Vtut Berina Sea OiuKcMI Sea Baaufon Sea 59) loWWKl Slwll 60) 61) SI) 63) ftrg« Plateau *nt«rMlc* BIKH S«a Hudnn Bay fanuary 2008 / Vol. 58 No. I • BioScience 55 Articles Box 1 . {continued) 4. Use a variety of strategies to hedge against uncertainty in the ecosystem response to EBM approaches. Uminlicipalcd effect.s ol HBM on ecuMystems can come from inherent viiriability and complexity in food-wch dynamics, iheir interaction with complex socioeconomic systems, and the uiicertairity in the effects of alternative management approaches themselves. Regardless of the state of models or analysis used to characterize a system, adopting a management approach that becomes relatively more prescriptive over time as information (and thus certainty in outcomes) increases is one way to explicitly hiiild in learning to strategy development (e.g., Kaufman et al. 2004). Another prudent approach that can be implemented without extensive knowledge of a system is including a diversity of regulation, reward, and other incentive systems for human behaviors that are coiisi.stent with EBM objectives (Hutton and Leader-Williams 2003. Hilborn 2007). Where information allows, exploring and modifying altcrnalive approaches throui-h scenario modeling and experimentation, monitoring, and adaptive management also can improve contingency planning (Butterworth and Punl 1999). 5. Use spatial organizing frameworks such as zoning for coordinating multiple management sectors and approaches in EBM. Marine EBM will require multiple approaches to managing competing uses and authorities in the ocean, such asfisheries,recreatitin, research, conservation, and shipping. Such activities can be coordinated spatially and temporally through oirean znning or other spatially specific management approaches (NMFS 1999, POC 2003, USCOP 2004, Young et al. 2007). 6. Link the governance structure with the scale of the ecosystem elements to be managed under an EBM approach. Management decisions that are matched to the spatial scale of the ecosystem, to the programs Tur monitoring all desired ecosystem attributes, and to the relevant management authorities are likely to be more successful in achieving ecosystem objectives (Sissenwinc and Mace 2003, Rosenberg and McLeod 2005, USGAO 2005). Coordination and decision feedbacks among the goveming authorities are a crucial part of successful EBM. Other seabirds Figure 1. Simplified food-web diagram ofthe Southem Ocean (redrawn from CCAMLR's Management of the Antarctic,flVfli/flWearwww.ccamlr.org/pu/E/e_pubs/am/man-ant/toc.htm). 56 BioScience • January 2008 / Vol. 58 No. I www.bioscienccmag.org Articles importance of krill to predators, with the result that the recommended rates of removal are 25% lower than if predators were not considered (CCAMLR 2006). A second example of the ecosystem-based fishery approach is evident in the CCAMLR's management of fisheries bycatch. Limits on the incidental mortality ot nontarget species have been established, and once these limits are met, the target fishery can be closed, even if the quota for the target species has not been harvested. The CCAMLR's approach to HBM is iterative, taking into account new information as it becomes available. However, the character of this environment makes data collection and fisheries observation expensive and logistically challenging. If ecosystem metrics were adopted and monitored, information that is missing \ov specific species would not necessarily mean that they would tie removed from management focus. In this way, food-web and ecosystem metrics could themselves become the targets of management (in addition to single-species metrics), and consequently help drive management decisions and feedhacks. High-latitude environments such as the Southern Ocean may be especially susceptible to the impacts of multiple stressors such as those associated with climate change and with multiple commercial fisheries (e.g., Atkinson et al. 2004). Q>nsequently, the effectiveness of the ecosystem approach currently is limited by insufficient data to understand the biological effects of fishery regulations on food-web elements, potential lack of compliance with fishery regulations, and unknown effects of interactions of fishery management approaches with environmental change. For example, there is no clear mechanism for linking the CCAMLR's management recommendations regarding catch limits with those developed to manage the seal and whale fisheries. If management objectives, indicators, and strategies for diverse sectors were better coordinated, potential trade-offs would likely become more apparent. Because of the remote and large geographic area covered by the CCAMLR, a mix of regulatory and incentive-based approaches is likely to increase the chances that ecosystem goals will be achievable. Finally, the strength of the CCAMLR is in the organization and scope of scientific research underpinning EBM for the Southern Ocean. What is missing is a rigorous link between the scientific recommendations emerging from this process and policies that explicitly incorporate risk management in setting acceptable catch limits for the species harvested in the Southern Ocean. Tighter linkages between governance decisions and scientific information will increase the likeliliood of achieving overall ecosystem objectives. The Bering Sea-Aleutian Islands ecosystem Thefisherieswithin the Bering Sea-Aleutian Islands (BSAl) ecosystem are managed under a sophisticated multispecies framework that is based oti extensive monitoring by both fishers and managers. Similar to the management approach under the CCAMLR, the approach in the BSAI ecosystem can be characterized as an ecosystem-based fishery management www.biosciencemag.org approach that is evolving to incorporate broader ecosystem management elements more fully (box 2). Groundfish fisheries in the BSAl ecosystem are among the largestfisheriesin the world. They serve as an illustration for the way in which conservative single-species management of multiple species can contribute to an ecosystem approach to fisheries management. About 80 stocks of groundfish are recognized and managed in the BSAI ecosystem (NPFMC 2006); chief among these are stocks of walleye pollock. Pacific cod, and Atka mackerel (box 3). Despite intensive commercialfishing,none of the groundfish stocks is currently overfished according to the technical definition under the regulations (Lauth 2007). Removal levels and biomass of the primary commercial target species, walleye pollock, have been stable for more than two decades, and the average trophic level of the catch (an indicator of sustainablefishingpractices) has been stable for at least 15 years (Boldt 2006), which repre.sents approximately one generation for most species involved. In the BSAl groundfish fisheries, single-species management is Implemented by establishing annual or seasonal fishing quotas that are lower than the estimated maximum sustainable yield, which is considered an upper limit on fishing effort rather than a target. Quotas become more conservative as uncertainty about the status of the stock increases. Removals are further restricted by limitations on the total catch of all groundfish species combined. This combined quota is lower than the sum of the individual quotas, thereby providing an extra measure of precaution in tnanagement of this system. Additional limits are established lor the incidental catch of nontarget and protected species; once these limits are reached, thefisheryis closed, even if catch quotas of target species have not been reached. It is common in the BSAI groundfish fisheries for caps on the mortality of protected species to limit fishing on target species in a given area and season (NPFMC 2006). The simultaneous application of quotas at the level of itidividual stock, combined total catch, incidental take of nontarget species, and incidental take of protected species substantially reduces the likelihood of long-term impairment of the ecosystem byfishing.Setting such quotas requires an extensive data collection and management system. Data collection includes fishery-independent survey data (i.e., both bottom trawl and acoustic surveys for groundfish and surface trawls for forage fish) that supplement the fisherydependent data provided by the fishers and observers on commercialfisheryvessels (e.g., catch per unit effort, biological samples, bycatch monitoring, etc.). The annual cost of the fishery-independent data currently is on the order of $20 million to $30 million a year, an investment that has been acceptable to the federal government and the t~ishing industry, given the approximately $1 billion atinual value of the fishery (NPFMC 2006). Other fishery management methods are applied in the BSAI groundfishfisheriesto account for some predator-prey interactions and habitat protection (NMFS 2003, NPFMC 2006). Large areas have been closed tofishing,depending on January 2008 / Vol. 58 No. 1 • BioScience 57 Articles Box 2. Summary of current and potential ecosystenvbased management strategies for selected marine and coastal management areas. Antarctic/Southern Ocean Current strategies: Spatial boundaries are defined by international agreement through the Commission for the Conservation of Antarctic Marine Living Resources. Clear statements of objectives arc defined for fisheries, hut not for marine mammals and for only home birds. Human activities (commercial fisheries) arc explicitly considered, A zoning framework is applied (as a sectoral framework). The governance structure allows for the ecosystem-based management (EBM) approach, but monitoring and enforcement are difficult. Additional components for a comprehensive EBM approach: Develop indicators of ecosystem status and function (current management relics on the status and trends in some individual species). Diversity approaches and tools to hedge against uncertainty in food-web dynamics, future climate, and so on. Develop spatial strategies for each sector at smaller, ecologically relevant scales using a mix ofregulatory and incentive-based approaches. Link the governance structure fully to scientific processes and adaptive management. Bering Sea/Aleutian Islands Current strategies: Spatial boundaries are defined as large marine ecosystems on the basis on hydrographic, bathymetric, and biogeographic criteria. Fishery-based management objectives are based on allowable catch for targeted and nontargeted species caught as bycatch. Indicators for fished part of food web and some habitats are well monitored. Quotas for nontargel species reduce risk for the overall food web, some food-web experiments are being conducted, and uncertainty is explicitly included in stock assessments tor pollock, a primary fished species. Spatially explicit fishery regulations are ased. Governance is relatively simple because few management sectors are relevant (i.e., federal and state governments, the fishing community). Additional components for a comprehensive EBM approach: Identify ecologically and politically relevant subregioiis of the ecosystem loi- more targeted management. Adopt broader ecosystem objectives, taking into account socially valued habitats and species in higher and lower trophic levels. Include indicators for larger marine mammals, dim ate-mediated processes for better predictions of ecosystem responses to management. Incorporate future scenarios of climate change into fishery and habitat management strategies to increase the certainty of ecosystem response. Broaden governance to include other managed parts ofthe ecosystem (e.g., marine mammals, watershed influences). Great Barrier Reef Marine Park Current strategies: The boundary of the managed area is defined by the extent of the Great Barrier Reef (GBR) and adjacent waters. The objeaives adopted by a broad group of users explicitly include ecological sustainability, through protection of natural resources and human use and enjoyment ofthe Great Barrier Reef. There is monitoring of biophysical and some socioeconomic attributes ofthe GBR Marine Park and no single report card for cecf "health." A 25-year strategic plan outlines eight broad strategy areas; education of the public is key. Clear zoning maps specify the uses of the GBR Marine Park (e.g., commercial uses, tourism, recreation, traditional uses, research) and the degree of protection ("general use" or "preservation," e.g.). The GBR Marine Park Authority has an explicitly stated relationship with C:ommonwi:alth and Queensland governmental organizations, roles are spelled luit in governance documents, and Australia's 1998 oceans policy provides a framework for EBM in marine waters. Additional components for a comprehensive EBM approach: Advance work on performance indicators and identify clear paths for monitoring feedback into strategies. Emphasize social and economic aspects of research and adaptive management, in addition to the biophysical aspect. Develop a plan for dealing with external factors affecting the quality of resources within the GBR Marine Park, such as water quality, climate change, coastal development, and fisheries. Education about the 2004 zoning plan, and enforcement of it, are critical. Improve coordination between commonwealth and state laws in managing the GBR Marine Park. California coast Current strategies: Spatial boundaries are defined by state statute. The marine protected area and general coastal ocean management objectives are stated. Human activities (e.g., commercial fisheries) arc explicitly considered. A zoning framework is applied (within the context of marine protected area networks). Additional components for a comprehensive EBM approach: Adopt specific objectives for multiple natural and human ecosystem components. Identify a set of natural and human system indicators for tracking progress. Identify and get commitments for the role of different management sectors in contributing to ecosystem objectives. Link the governance structure to management and scientific processes. 5« BioScience • January 2008 / Vol. 58 No. 1 www.hiosciencemag.org Articles gear type and season, for the protection of habitat and important prey species. For example, areas around Steller sea lion rookeries are closed to some types of fishing when pups are present, in ordei" to preserve the prey items required for pup survival and growth. Experiments to determine how fishing levels affect the prey field for Steller sea lions are testing these impacts explicitly (Wilson et al. 2003). In 2006, the Regional Fishery Management Council responsible for developing recommendations to the federal government on acceptable catch levels created an ecosystem committee for the purpose of developing a fishery ecosystem plan for the Aleutian Islands region. This ecosystem plan will he an overarching guide for the implementation of EBM of fisheries in this area, which is a subregion of the BSAI ecosystem. This work is considered a pilot effort and its effectiveness will be evaluated as it is implemented. Whether other subregions of the BSAI ecosystem should be managed more precisely will depend in part on the distinctness of ecosystem responses in different parts of the system. For example, Ciannelii and colleagues (2004) used food-web energetic models and information on species'dispersal distances to define the spatial scales over which there are predator and prey feedbacks for some of the species in the Pribilof Islands portit)n (tf the BSAI ecosystem. Although parts of the BSAI ecosystem are subject to an ecosystem-based fishery approach, unknown effects of other factors within the ecosystem reduce the certainty of predicting future states. Some drivers in the system are poorly studied, such as fbod-web interactions and relationships between habitat quality and productivity of target and nontarget species. For example, the implications of potential food-web interactions among whales, pinnipeds, sea otters, urchins, and kelp forests (Springer et al. 2003, DeMaster et al. 2006) for fishery management are not well understood. In addition, the impacts on the ecosystem of rising water temperatures, loss of sea ice, and changes in pH and carbonate saturation are just beginning to be examined. Afive-year,$30-million research program, which will begin in 2008, is designed to provide an initial understanding of some of these key processes and interactions associated with increasing concentrations of greenhouse gases. An improved understanding of all elements of the ecosystem within a management strategy evaluation framework (e.g., Butterworth and Punt 1999) will better allow commercial and subsistence hunters and fishers in the region to prepare for Hkety changes in the Bering Sea over the next 20 to 50 years. Including management objectives for a broader scope of species or habitat types within the ecosystem will require the difficult work of engaging representatives from more sectors (e.g., Alaska native subsistence whaling interests). The relatively low density of the human population in the BSAI ecosystem makes such governance chaiienges relatively minor, compared with systems such as California's coast, where manv more stakeholders are involved. w^vw.biosdencemag.org Box 3. Types of species in the fishery management plan for the Bering Sea-Aleutian Island ecosystem. Prohibited species Prohibited species are those species and species groups that when caught must be returned to the sea with a minimum i)f injurv', except when their retention is authorized by other iipplicahk' law. Torcign llshcries must maintain catcli records for each of these species. All bycatch of marine mammals must be reported to ihc appropriate agency. Examples of prohibited species iiicludo Pacific halibut, Pacific herring, salmonids, king crab, iiEul ianni.T crab. Target species Target species arc commercially important and generally targeted upon Iw the groundfish fishery. SiifflcioTit data exist to specify total allowalile catch (TAt;) and to manage each species or species group separately. Catch records must be kopl for each of these species, larget species, or species groups, may he conibined or split by regulatory amendment. Examples of target species defined in the regulations include atka mackerel, arrowtooth flounder, llatliciid sole, Greenland lurbot. Pacific cod. Pacific Ocean perch, rock sole, sablefish, squid, walleye pollock, and yellowfin sole. Other species Other species have little economic value and arc not usually targeted, but they may be significant components ol' the ecosystem or have economic potential. A single TAC applies to this category as a whole. Catch records must he kept for each of these species. Other species include sculpin, eulachon, capelin, shark, skates, smelt, and octopus. Nonspecified species Nonspecified species are those species and species groups of no current economic value taken as incidcntLil catch in the target fisheries. Virtually no data exist that would allow population assessments. No record of catch is necessary. No TAC is established for this category; the allowable catch is the amount that is taken incidentally during fishing lor target and other species, whether retained or discarded. Nonspecified species include numerous fish and invertebrates such as grenadiers, eelpouts, sea urchins, and mussels. The Great Barrier Reef Marine Park, Australia TheCreat Barrier Reef (CiBR) ecosystem boasts a system-wide spatial management approach that is arguably the world's most sophisticated and extensively itnplemented example of marine zoning. Stretching more than 2300 kilometers along the northeastern coast of Australia and comprising 70 bioregions, the GBR is the largest and most famous reef system January 20081 Vol. 58 No. I • BioScience 59 Articles 200 I 400 I GSR Marine Park -10° S Coral Sea -15° S -20° S -25° S No-take areas ^0 Original (pre-2004) Current however, other threats were recognized, and comprehensive management of this reef system has now evolved to the point where multiple uses and protection of marine biodiversity are addressed directly. The GBRMPA tiianagement philosophy explicitly emphasizes tnanagement at the ecosystem level, conservation and reasonable use, public participation and community involvement, and monitoring and performance evaluation. Protection recently took an enormous step forward with the establishment of a new zoning plan on 1 luly 2004. As a consequence, the proportion of no-take zones increased from less than 5% to more than 33% ofthe total area of the park (figure 2). These no-take zones protect representative examples of each of the broad habitat types in the GBR and represent the world's largest such network in operation today. Although increasing the protection of biodiversity was a top priority, a further aim was to minimize impacts on the existing users of the GBR Marine Park, including commercial and recreational fishers. Both these aims were achieved by a comprehensive program of both scientific input and community involvement; the participatory planning was the largest such exercise for any environmental issue in Australia's histor>'. The rationales for the decisions made are summarized in a series of biophysical operational principles and in a set of social, economic, cultural, and management feasibility operational principles (Fernandeset ai. 2005). Managing for resilience is explicitly mentioned in GBRMPA documents. There is also a clear awareness that no-take areas in isolation cannot achieve all conservation aims, and management of land use is therefore Figure 2. Green zones (no-take areas) in the Great Barrier Reef before and considered a critical component of successHil reef after enactment ofthe 2004 zoning plan. management. This is facilitated by legislation that in the world and the largest World Heritage Area. Coral reefs allows regulation of activities outside the GBR that could in general are both the most diverse of all marine ecosystems have adverse impacts (Day 2002) and by prioritizing marine and among the most threatened (Pandolfi et al. 2003). Threats areas that lie adjacent to protected land (Fernandes et al. include not only tbe loss of intensively harvested species (in2005); the Reef Water Quality Protection Plan of 2003 Is an cluding elimination through fishing of spawning aggregation example of this approach. Global temperature rise and acidsites) but also the loss of the coral reef framework itself ification cannot, of course, be managed directly on a local scale, because of destructive fishing practices, coral disease, coral but some evidence exists that reducing local impacts imbleaching, algal overgrowth, and now ocean acidification. proves reef resilience to global stressors (Hughes ct al. 2007). Thus, although the ecosystem outcomes remain to be docuAlthough the GBR oft^en is assumed to be in relatively mented, the GBRMPA is arguably the best example we have good condition, recent analyses indicate that it too has sufof EBM in place today. fered substantial degradation (Pandolfi et a!. 2003, Beilwood et al. 2004). Fortunately, the GBR has the benefit of being A thorough review of the management ofthe GBR Marine almost entirely within the jurisdiction ofthe Great Barrier Reef Park was completed in 2006 (DEH 2006), and the recomMarine Park Authority (GBRMPA; www.gbrmpa.gov.au/) of mendations include a sophisticated list of the next issues to Australia. The GBRMPA was established in 1975, and concems address. Relatively speaking, the management ofthe GBR area about oil drilling drove its early development. Over the years. is tnature enough that detailed implementation of mnny 145° E 60 BioScience • January 2008 / Vol. 58 No. 1 150" E www.bioscienccmag.org Articles HBM principles iilready is under way. The review highlighted the need for greater attention to social and economic issues in research, reporting, and governance, and pointed out that relatively more attention has been focused on understanding and managing the biophysical aspects of the ecosystem. For example, there has been no assessment of cumulative regional, social, and economic impacts of the 2004 zoning plan on the viability of businesses. Management of the park's resources also would benefit from careful consideration of external factors affecting the status of the ecosystem—such as impacts iVotn climate change, land-based inputs of sediments and nutrients from development, and the way in which fishery management on highly migratory species affects the ecosystem's functioning. Finally, better coordination among many state and commonwealth laws (e.g., there are six laws regulating fisheries alone) will help to protect the environmental and cultural values that are part of the GBRMPA's ecosystem objectives. Ecosystem-based management approaches in coastal California California is a leader in promoting marine EBM approaches through legislation. California's Marine Life Management Act (MLMA) became law in early 1999, and it represents an ecosystem-based approach to managing all marine wildlife in the state's waters (CDFG 2007). The goals of the MLMA include conservation of nonconsumptive values of marine resources, sustainability offisheriesand reduction in bycatch, habitat conservation and restoration, and consideration of socioeconomic benefits tofishingcommunities from changes in management of marine resources. Thefisherymanagement plans included under the law's umbrella must be linked in a master plan, which defines the ecosystem-based management principles, prioritizes fisheries for plan development, and incorporates interactions among management plans for individualfisheries.The 29 species included in the prioritized list are diverse laxonomically, including surlperches, sharks and rays, sea basses, halibut, sea urchins, lobster, sea cucumbers, subtidal snails, intertida! invertebrates, and two species of kelp. One of the key fishery management plans for California is the nearshorefisherymanagement plan, which must contain fishery management objectives for 19 species of flnfish while also meeting the ecosystem and nonconsumptive use provisions of the MLMA. A unique feature of the nearshore fishery management plan is its inclusion of an adaptive management framework for setting biological objectives that explicitly adjusts for the quality of information over time (Kaufman et al. 2004). A so-called control rule in the plan guides the establishment of total catch limits for each species, and the rule is designed to evolve over time as data availability increases on the ecosystem effects of harvest. The design of the control rule encourages data collection and analysis as the EBM approaches to setting harvest levels are implemented, and acknowledges that such approaches are likely to be experimental in the early stages. As more information is www. biosciencemag.org gathered over time, the precautionary approach to setting harvest limits can be moderated and replaced by more informed catch limits that incorporate ktiowledge of ecosystem relationships and interactions among species. The MLMA also requires that a plan for a network of marine protected areas be developed as a means to achieve the objectives of the act. The Marine Life Protection Act Initiative is designed to use scietitific, policy, and public input to identify networks of MPAs along the California coast. After a thorough two-year science-stakeholder-policy process, the first of the regional networks—along the central coast—was approved in April 2007 by the California Fish and Game Commission (CDFG 2007). The science policy process will begin anew for adopting an MPA network along the northcentral California coastal region. Previous to the MLMA enactment, a network of marine reserves in the Channel Islands in southern California waters was developing, and after a rigorous science-policy process to identify scenarios of protected areas, the network currently contains 453 square kilometers of state-managed reserves within the existing federal Channel Islands National Marine Sanctuary (Airame et al. 2003; www.dfg.ca.gov/mrd/channel_islands/index.html). More recently, the California state legislature passed the California Ocean Protection Act, which creates a state Ocean Protection Council (OPC) composed of the state agencies that have responsibility for ocean issues. Tlie California Ocean Protection Act also establishes a $10 million Ocean Protection Trust Ftjnd, which is designed to reduce threats to marine ecosystems through incentives for sustainable fisheries, improved management, and monitoring. As part of implementing the new act, the OPC created afive-yearstrategic plan that identifies goals for the California marine ecosystem and outlines measurable outcomes and key actions for achieving these goals (COPC 2006). The goals laid out in the plan discuss explicitly that an EBM approach is needed to maintain ocean and coastal ecosystems, including coordinating governing bodies; learning about the systetn through monitoring and research; maintaining water quality, physical processes, habitat structure, and wildlife; and conducting education and outreach. A more comprehensive EBM approach in California's coastal region, at the scale of the entire California coast, could be achieved through application of many of the EBM principles that already have been implemented at local scales for more focused issues (e.g., Channel Islands and Central Q)ast MPA network prtKesses). In particular, using public participatory processes to adopt specific objectives for multiple natural and human ecosystem components for coastal California would help greatly in coordinating ongoing and future work across many sectors. Such work could guide actions affecting the ecosystem beyond establishing MPA networks or setting fishery catch limits, such as land- and water-use regulations, shipping practices, and oil and gas development. Once the ecosystem objectives are broadly agreed upon, different management sectors can identify acfanuary 2008 / Vol. 58 No. I • BioScience 61 Articles tions (and expected ecosystem responses) to which they will contribute under an accountability system. Conclusions The case examples we highlight in this article illustrate the current, relatively young state of marine EBM in practice. Evaluating the success of something as complex as EBM will take diligent monitoring and evaluation of strategies and desired ecosystem components—such data are just beginning to emerge. In the meantime, strategies in each case are evolving as managers slowly expand the components ofthe ecosystem included within their evaluations and the EBM principles they include in management approaches. The examples we highlight differ in the particular aspects of EBM that have been applied, yet each suggests several promising next steps that could advance EBM approaches and improve ecosystem prospects. Fishery-based ecosystem management approaches in the Antarctic and BSAI ecosystems provide good examples of how explicit adoption of objectives and monitoring of indicators can drive management decisions through governance bodies charged with meeting those objectives. The multispecies fisheries objectives in those two regions are tnostly being met through evolving management approaches, but components oftho.se ecosystems that are peripheral to the managed portions are not getting the same level of attention as target species. More work to expand ecosystem objectives and management sectors beyond fishing interests could bolster fisheries and support broader ecosystem functions, such as persistence of migratory marine mammals, sea birds, and habitats, in both of these regions. Both of these ecosystembasedfisherymanagement examples also would benefit fi'om broadening their strategies to include a cornbination of regulatory and socioeconomic incentives as a way to meet more comprehensive ecosystem objectives. The GBRMPA is the current gold standard for EBM in the oceans, and its success thus far in applying EBM principles is in large part becau.se of its equal attention to both the human and natural systems parts of ecosystem managetnent. Tracing the evolution of management of the GBR fi'om one largely driven by concerns about oil extraction to one guided by full ecosystem objectives and management of multiple threats is instructive for the younger regional EBM efforts. Managers in the GBRMPA clearly recognize the potentially significant ecosystem benefits that arise from involving stakeholders in identifying and adopting strategies to achieve ecosystem goals. The ecosystem work through the GBRMPA benefitsfi-omclearly identified entry points for all elements (natural, social, political) ofthe decision framework. How such an approach ultimately will succeed in achieving the biodiversity and socioeconomic objectives to which they aspire will become clearer over time. Finally, the sort of adaptive approach adopted in Galifornia, which will require many yeans for ecosystem-dynamic properties to emerge, will very likely be fi'uitful in most approaches to EBM. EBM is in the early stages of imple62 BioScience • Inuunry 2008 / Vol. 58 No. 1 mentation and evaluation. Debate about how best to implement EBM in the ocean will be informed by tests designed to guide the establishment and monitoring of scientifically based thresholds, to determine the impact of decisions triggered when such thresholds are reached, and to elucidate decision implementation and feedback mechanisms within specific governance structures. Such first steps will improve our ability to identify opportunities for new and coordinated actions that have the greatest likelihood of improving ecosystem function. These steps recognize that EBM per se is not our objective, and instead place the emphasis where it belongs—on improving ecosystem resilience and function. Acknowledgments We thank Heather Leslie, Mike Ford, Jeff Hard, Phil Levin, Rick Methot, Enric Sala, and Steve Palumbi and his lab group for comments on an earlier version of this manuscript. Gomments from three anonymous reviewers greatly improved the practical nature ofthe messages in this article. Kimberiy Toai and Jeremy Davies improved thefigures.Discussions with Andy Rosenberg and Will Stelle at the "Managing for Resilience: An Integrated Approach to Goastal Marine Science and Gonservation" symposium at the University of Washington's Friday Harbor Laboratories helped us better understand the challenges and opportunities associated with implementing EBM in the oceans. We also thank the director and staff of Friday Harbor Laboratories, the David and Lucile Packard Foundation, and the Andrew W. Mellon Foundation for supporting the symposium, its diverse participants, and .stimulating discussion ofthe ideas contained in this manuscript. References crted Adycr W'N, Hughes TP, Folke C, Carpenter SR, Rockstrom |, 2005. Social-ecological resilience to coa.staldisL]sttTs.Sdeni:c 309:1036-1039. Airame S, Dugan |E, Lafferly KD. Leslie H, McArdle DA, Warner RR. 2003, Applying ecological criteria to marine reserve design: A cast study from the California Channel Island.s. 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