Special Section

Climate Change, Marine Environments, and the U.S. Endangered Species Act ERIN E. SENEY,∗ † ‡‡ MELANIE J. ROWLAND,‡†† RUTH ANN LOWERY,§ ROGER B. GRIFFIS,∗ AND MICHELLE M. MCCLURE∗∗ ∗

National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Office of Science and Technology, 1315 East-West Highway, Silver Spring, MD 20910, U.S.A. †Erin Seney Consulting, LLC, Woodbridge, VA 22192, U.S.A. ‡National Oceanic and Atmospheric Administration, Office of the General Counsel, Northwest Section, Seattle, WA, U.S.A. (retired) §National Oceanic and Atmospheric Administration, Office of General Counsel, Fisheries and Protected Resources Section, 1315 East-West Highway, Silver Spring, MD 20910, U.S.A. ∗∗ National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Northwest Fisheries Science Center, 2725 Montlake Boulevard, East, Seattle, WA 98112, U.S.A. ††Melanie J. Rowland Consulting, Twisp, WA 98856, U.S.A.

Abstract: Climate change is expected to be a top driver of global biodiversity loss in the 21st century. It poses new challenges to conserving and managing imperiled species, particularly in marine and estuarine ecosystems. The use of climate-related science in statutorily driven species management, such as under the U.S. Endangered Species Act (ESA), is in its early stages. This article provides an overview of ESA processes, with emphasis on the mandate to the National Marine Fisheries Service (NMFS) to manage listed marine, estuarine, and anadromous species. Although the ESA is specific to the United States, its requirements are broadly relevant to conservation planning. Under the ESA, species, subspecies, and “distinct population segments” may be listed as either endangered or threatened, and taking of most listed species (harassing, harming, pursuing, wounding, killing, or capturing) is prohibited unless specifically authorized via a case-by-case permit process. Government agencies, in addition to avoiding take, must ensure that actions they fund, authorize, or conduct are not likely to jeopardize a listed species’ continued existence or adversely affect designated critical habitat. Decisions for which climate change is likely to be a key factor include: determining whether a species should be listed under the ESA, designating critical habitat areas, developing species recovery plans, and predicting whether effects of proposed human activities will be compatible with ESA-listed species’ survival and recovery. Scientific analyses that underlie these critical conservation decisions include risk assessment, longterm recovery planning, defining environmental baselines, predicting distribution, and defining appropriate temporal and spatial scales. Although specific guidance is still evolving, it is clear that the unprecedented changes in global ecosystems brought about by climate change necessitate new information and approaches to conservation of imperiled species. Keywords: anadromous species, critical habitat, environmental assessment, imperiled species, interagency consultation, ocean acidification, recovery plan, uncertainty El Cambio Clim´atico, los Ecosistemas Marinos y el Acta Estadunidense de Especies en Peligro

Resumen: Se espera que el cambio clim´atico sea un principal conductor de la p´erdida de biodiversidad global en el siglo 21. Esto proporciona nuevos retos para la conservaci´ on y el manejo de especies en peligro, particularmente en ecosistemas marinos y estuarinos. El uso de ciencias relacionadas con el cambio clim´ atico en el manejo de especies estatutarios, como bajo el Acta Estadunidense de Especies en Peligro (ESA), se encuentra en sus fases iniciales. Este art´ıculo proporciona un an´ alisis de los procesos de ESA, con ´enfasis en los mandatos al Servicio Nacional de Pesqueras Marinas (NMFS) para enlistar especies marinas, estuarinas y

‡‡Address for correspondence: National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Office of Science and Technology, 1315 East-West Highway, Silver Spring, MD 20910, U.S.A. email [email protected] Paper submitted July 31, 2012; revised manuscript accepted April 11, 2013.

1138 Conservation Biology, Volume 27, No. 6, 1138–1146  C 2013 Society for Conservation Biology DOI: 10.1111/cobi.12167

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an´ adromas. Aunque la ESA es espec´ıfica de los Estados Unidos, sus requerimientos en general son relevantes para la planificaci´ on de la conservaci´ on. Bajo la ESA, las especies, subespecies y “segmentos distintivos de la poblaci´ on” pueden enlistarse como en peligro o amenazadas, y la colecta de la mayoria de los especies enlistadas (molestar, da˜ nar, perseguir, herir, matar o capturar) est´ a prohibida a menos que sea autorizada espec´ıficamente por un proceso de permiso caso-por-caso. Las agencias gubernamentales, adem´ as de evitar la colecta, deben asegurar que las acciones que patrocinan, autorizan o llevan a cabo no pongan en peligro la existencia continua de una especie enlistada ni afecten negativamente h´ abitat cr´ıticos designados. Las decisiones para las cuales el cambio clim´ atico probablemente sea considerado un factor clave incluyen: determinar si una especie deber´ıa estar enlistada bajo la ESA, designar a abitat cr´ıtico, desarrollar ´ reas de h´ planes de recuperaci´ on de especies, y predecir si los efectos de actividades humanas propuestas pueden ser compatibles con la supervivencia y recuperaci´ on de especies enlistadas en ESA. Los an´ alisis cient´ıficos que subyacen estas decisiones cr´ıticas para la conservaci´ on incluyen estudios de riesgo, planeaci´ on de recuperaci´ on a largo plazo, definir las bases ambientales y definir escalas temporales y espaciales apropiadas. Aunque la orientaci´ on espec´ıfica todav´ıa est´ a evolucionando, est´ a claro que los cambios sin precedentes en los ecosistemas globales causados por el cambio clim´ atico necesitan informaci´ on nueva y nuevas aproximaciones para la conservaci´ on de especies en peligro.

Palabras Clave: acidificaci´on oce´anica, consulta interagencias, especies an´adromas, especies en peligro, estudios ambientales, h´abitat cr´ıtico, incertidumbre, plan de recuperaci´ on

Introduction Climate change is expected to be a top driver of global biodiversity change and loss in the 21st century (Leadley et al. 2010; Pereira et al. 2010). It will likely affect the physiology, phenology, habitat, and population responses of imperiled species and the structure and function of ecosystems (Parmesan 2006; Dawson et al. 2011; Doney et al. 2012). Climate change presents new challenges to conserving and managing natural resources, particularly because experiences on which to base or validate ecological models of current and future effects are lacking (Williams & Jackson 2007; Doney et al. 2009; Lawler 2009). These challenges are particularly acute in marine and estuarine systems, which have received far less scientific attention than terrestrial environments (Richardson & Poloczanska 2008). Recommendations regarding best practices for integrating climate change into management of marine and anadromous species are needed. We present a general overview of climate change’s potential effects on species and ecosystems and a brief review of the relevant requirements of the U.S. Endangered Species Act (ESA) (United States Code [U.S.C.] Title 16, Sections 1531–1544). Although much of the information is broadly applicable to conservation under climate change, the overview emphasizes marine and estuarine systems, with much of the discussion rooted in the ESA’s mandate to the U.S. National Oceanic and Atmospheric Administration’s (NOAA) National Marine Fisheries Service (NMFS) to manage ESA-listed marine, estuarine, and anadromous species. Specific examples of integration of climate change into ESA decisions and related conservation processes—and the challenges therein—are found in other papers in this special section.

Climate Observations and Projections Effects of climate change are being documented worldwide. Global mean surface air temperature (SAT) increased approximately 0.75 ◦ C during the last century; the global rate of increase has been approximately 0.2 ◦ C/decade since 1971 (Blunden & Arndt 2012). Similarly, the average temperature of the oceans’ upper layers increased by 0.6 ◦ C between the early 1900s and 2010, and the oceans’ uptake of approximately one-third of the world’s anthropogenic CO2 has led to decreases in surface water pH (acidification) and carbonate concentrations (Hoegh-Guldberg & Bruno 2010). Modern-day atmospheric concentrations of CO2 , the largest known contributor to climate change, are now higher than any experienced in the last 800,000 years (Blunden & Arndt 2012), and dramatic decreases in global emissions are unlikely in the near term (Meehl et al. 2007). Projections that assume no emission reductions predict SAT increases of 1.1–6.4 ◦ C, thermal expansion (sea-level rise) of 0.18–0.59 m, and ocean pH declines of 0.14– 0.35 units during the 21st century (Meehl et al. 2007). Recent data suggest that Intergovernmental Panel on Climate Change scenarios that incorporate higher, fossil fuel-intensive projections are plausible, given increasing global energy demands and limited, uneven efforts to curb emissions (Betts et al. 2011; International Energy Agency 2013). Although uncertainty exists with respect to the form, magnitude, timing, and distribution of future effects of climate change, particularly at regional and local scales (Meehl et al. 2007; Loarie et al. 2009; Hoegh-Guldberg & Bruno 2010), global trajectory is well established for the 21st century. Further information on

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recent and projected changes in global and regional temperatures, sea level, sea ice, pH, precipitation patterns, and frequency of extreme events are detailed elsewhere (e.g., Karl et al. 2009; Betts et al. 2011; Blunden & Arndt 2012).

Effects of Climate Change on Species and Ecosystems By the end of this century, large portions of the Earth’s surface are projected to have climates and ecological conditions outside historical norms, and some presentday climates may disappear (Williams & Jackson 2007). Primary effects of climate change on individual species include habitat loss or alteration, distribution changes, geographic isolation or extirpation of populations unable to adapt or migrate, new interspecific interactions, and shifts in phenology (e.g., Lawler 2009; Urban et al. 2011; Hellmann et al. 2012) (Fig. 1). Additionally, ocean acidification and consequent reductions in carbonate ion concentrations will directly affect shell-forming marine organisms. Although some marine species may benefit from increased dissolved CO2 in the oceans, many are likely to exhibit reduced calcification and growth rates (Doney et al. 2009). Secondary effects of climate change and ocean acidification may include disruption of predator–prey interactions. Some species will experience reduced food supply and increased stress, disease susceptibility, and predation, whereas other species may encounter reduced barriers to settlement (e.g., Parmesan 2006; HoeghGuldberg & Bruno 2010; Doney et al 2012). Climate change may also exacerbate nonclimate stressors such as pollution or overharvesting and thus affect species’ adaptive capacity (Fig. 1). Similarly, human adaptation to climate change (e.g., relocation of communities and changes in fishing, agriculture, and land-use patterns) may have additional effects including habitat conversion, ecological degradation, and introduction of non-native species (e.g., Ruhl 2008; Kaplan et al. 2010; Glick et al. 2011). Many climate-related ecological effects, including range shifts and potentially some extinctions, have already been documented (e.g., Parmesan 2006; Wassmann et al. 2011; Hare et al. 2012). Changing environments make the development and integration of new approaches to conservation planning and risk assessment vital to near-term and future natural resource management (e.g., Pereira et al. 2010; Hellmann et al. 2012; National Fish, Wildlife, and Plants Climate Partnership [NFWPCP] 2012), particularly because uncertainties also exist as to species’ responses and adaptive capacities in the face of these changes (e.g., Williams & Jackson 2007; Doney et al. 2009; Dawson et al. 2011).

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Climate Change and the ESA

Overview and Legal Background of the ESA The ESA was enacted in 1973 to prevent species’ extinction and promote their recovery (i.e., improvement in the species’ status to the point of delisting). The law affords protection to listed vertebrate, invertebrate, and plant species. Under the ESA and herein, species include subspecies and “distinct population segments” (DPSs) of vertebrates. A DPS is a population that is both “discrete” and biologically and ecologically “significant” to its taxon (USFWS & NMFS 1996). The ESA emphasizes the importance of habitats and ecosystems and provides “a means whereby the ecosystems upon which endangered species and threatened species depend may be conserved” and “a program for the conservation of such . . . species.” Although it has been amended several times, the ESA’s structure and key provisions have been retained throughout its existence (Bean 2009). The USFWS, an agency in the Department of the Interior, and NMFS, part of NOAA in the Department of Commerce, share responsibility for implementing the ESA’s central provisions. In general, USFWS is responsible for terrestrial and freshwater species, whereas NMFS is responsible for marine and anadromous species. As of July 2013, ESA-listed species comprised 361 mammals, 317 birds, 126 reptiles, 35 amphibians, 166 fishes, 241 invertebrates, and 856 plants (USFWS 2013). Of listed species, 1481 occur in the United States and its territories, and 621 occur only in other countries (i.e., foreign species). Petitions to list marine and anadromous species under the ESA have become more frequent in recent years, and NMFS has recently listed species affected by climate change such as Pacific eulachon (Thaleichthys pacificus) and spotted seal (Phoca largha). Forty-four marine and anadromous fish, 29 marine mammal, 16 marine turtle, 4 marine invertebrate, and 1 marine plant species are managed by NMFS under the ESA. An additional 11 ESAlisted marine mammal species, including the sea-ice dependent polar bear (Ursus maritimus), are managed by USFWS. Species, including subspecies and DPSs, may be listed under the ESA as either endangered or threatened if they meet the definitions throughout all or a “significant portion” of their range. No species is protected under the ESA until it has been formally added to the list of threatened or endangered species as a result of being formally determined to meet one of these categories’ standards, regardless of its rarity or vulnerability (Bean 2009), although some limited protections from federal activities apply once a species is proposed for listing. The ESA prohibits, with some exceptions, the take (e.g., harassing, harming, pursuing, wounding, killing, or capturing) of any listed endangered animal species (U.S.C. Title 16, Section 1538) by all entities subject to U.S. jurisdiction: individuals, businesses, and government entities, including citizens and fisheries operating outside the U.S.

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Figure 1. Simplified schematic of the numerous interactions among a species, the species’ ecosystem, and climate effects (although not depicted here, interactions also occur among all ecosystem components). exclusive economic zone. Endangered plants receive more limited protection, including protection from removal or malicious damage on federal (U.S. Government) land. The take prohibition does not automatically apply to threatened species (U.S.C. Title 16, Section 1533), but the USFWS has adopted a rule applying it to all the threatened species under its jurisdiction, whereas NMFS has applied some form of take prohibition to most threatened species. Federal agencies, in addition to avoiding take, must ensure that actions they fund, authorize, or conduct are not likely to jeopardize a listed species’ continued existence or result in the destruction or adverse modification of designated critical habitat (U.S.C. Title 16, Section 1536). Agencies are required to use the best available scientific (e.g., biological, ecological, and climatic) and commercial information in key ESA decisions, even in light of uncertainty and variability in models and projections. Additionally, agencies must adhere to the standards for rational decision making of the Administrative Procedure Act (U.S.C. Title 5, Sections 551 et seq.), which prohibits “arbitrary and capricious” decisions and requires that the administrative record for a decision demonstrates that all relevant factors were considered and that the decision is supported by facts.

Climate Change and ESA Decisions The ESA was adopted before a broad scientific understanding of climate change existed (Rowland 2011; Bernazzani et al. 2012). It does, however, explicitly rec-

ognize the importance of environmental factors that are themselves influenced by climate change and sets forth an overarching goal to conserve listed species and their habitats. In light of the growing scientific understanding of its effects on physical and biological systems (e.g., Parmesan 2006; Meehl et al. 2007; Doney et al. 2012), climate change is a critical issue that requires developing new scientific and management approaches for imperiled species. Both recent scientific work (e.g., Hunter et al. 2010) and court decisions (e.g., Pacific Coast Federation of Fishermen’s Associations v. Gutierrez regarding Chinook salmon [Oncorhynchus tshawytscha] and Central Valley steelhead [O. mykiss], and Natural Resources Defense Council v. Kempthorne regarding delta smelt [Hypomesus transpacificus]) have established the importance of considering climate change in ESA decisions, and many government agencies and other organizations are exploring approaches to natural resource conservation in a changing climate (e.g., Glick et al. 2011; U.S. Forest Service 2011; NFWPCP 2012). Depending on the specific facts of each situation, climate change may be a large factor in 5 key types of ESA decisions: listing determinations (e.g., Brainard et al. 2013); designation of critical habitat for listed species (e.g., USFWS 2010); recovery planning (Povilitis & Suckling 2010); interagency consultations to assess ESA-related effects of actions that federal agencies propose to authorize, fund, or conduct (e.g., Busch et al. 2013; Jorgensen et al. 2013; Walters et al. 2013); and issuance of permits to allow takes of individuals for scientific or populationenhancement purposes or that are incidental to lawful activities (e.g., Bernazzani et al. 2012). Conservation Biology Volume 27, No. 6, 2013

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Listing Determinations The ESA defines an endangered species as a species, subspecies, or DPS that “is in danger of extinction throughout all or a significant portion of its range” and a threatened species as a species, subspecies, or DPS that “is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range” (U.S.C. Title 16, Section 1532). The ESA provides a framework for these determinations that includes review of specific factors that may be affecting the species as well as considering ongoing conservation efforts. The analytic process used in ESA listing determinations is somewhat analogous to other conservation and listing measures, such as those used by the International Union for Conservation of Nature (IUCN Red List of Threatened and Endangered Species) and the Canadian government (Species at Risk Act [SARA]), Unfortunately, most conservation measures contain ambiguous terms, such as the ESA’s foreseeable future and significant portion of its range. The ambiguity of these terms complicates the application of scientific analysis to, for example, identification of an appropriate time frame for risk analyses (Brainard et al. 2013) and understanding of the importance of portions of the range to a species’ persistence (Wassmann et al. 2011; Hare et al. 2012; Boughton & Pike 2013). Listing decisions are reached only after a full review of the species’ status to determine whether the species is threatened or endangered as a result of one or more of 5 types of factors described in Section 4 of the ESA: habitat destruction, modification, or reduction (e.g., loss or degradation of habitat due to human activities); overutilization for commercial, recreational, scientific, or educational purposes (e.g., overfishing); predation or disease (e.g., establishment of an introduced predator or pathogen); inadequate regulations or management (e.g., failure to adequately regulate any of the aforementioned factors); and any “other natural or manmade factors” (e.g., reduced survival under conditions outside physiological limits). Effects of climate change and ocean acidification are relevant to listing decisions if they present one or more new threats that affect species persistence (e.g., impairment of calcareous shell formation) or if they exacerbate or interact with existing and likely future threats (e.g., increased susceptibility to pathogens due to warmer temperatures). For any factor that significantly affects a species’ status, the agency considers whether any existing or planned regulations or mitigation measures are likely to adequately address its impacts and thereby reduce or obviate the need for ESA protection. Climate-change effects were important factors in several recent marine listing decisions (Ruhl 2008; Rowland 2011). Warming-induced coral bleaching and more frequent hurricane damage were important factors in the NMFS decision to list elkhorn (Acropora palmata) and

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staghorn corals (A. cervicornis) as threatened (NMFS 2006), whereas climate-related changes in ocean conditions were identified by NMFS as the largest threat to the threatened southern DPS of Pacific eulachon and its habitats (NMFS 2010a). A decreased amount of sea ice was a key factor in the decisions to list the polar bear (USFWS 2008; Hunter et al. 2010) and southern DPS of the spotted seal (NMFS 2010b) as threatened. More recently, the effects of ocean basin-level climatic factors were considered in the status determinations for new loggerhead sea turtle (Caretta caretta) DPSs (Van Houtan & Halley 2011), and climate change and ocean acidification effects were examined for 82 coral species being considered for listing (Brainard et al. 2013). An agency-initiated review examining the status of cusk (Brosme brosme) considered the effects of climate on availability of habitat for this deep-water fish (Hare et al. 2012).

Designation of Critical Habitat The ESA’s critical habitat component was added in 1978. It requires the listing agency to determine what particular habitat areas are critical to a listed species’ conservation and to consider economic and national security effects of specifying a particular area as a species’ critical habitat. Designated areas are protected against appreciable adverse effects through the interagency consultation provision of ESA Section 7. Thus, the determination may be economically important to many entities because a project requiring federal permitting or receiving federal funds may be precluded if the permitting or funding agency cannot assure that the proposed action is not likely to damage or destroy designated critical habitat (see Assessing and Mitigating Effects of Proposed Federal Actions below). Critical habitat designations are not required in areas outside U.S. jurisdiction, and as such, are not made for non-U.S. species. Of the 73 listed domestic species managed by NMFS, final critical habitat designations have been made for 46, and critical habitat has been proposed for an additional 3 species (NMFS 2013). A listed species’ critical habitat comprises specific areas within the geographical area occupied by the species at the time of listing “on which are found those physical or biological features (I) essential to the conservation of the species and (II) which may require special management considerations or protection.” It also includes specific areas outside the geographical area occupied by the species that “are essential for the conservation of the species” (U.S.C. Title 16, Section 1532). The latter may be especially important for species affected by climate change, given the likelihood of future range shifts, and identifying areas of high value to the species now and into the future is important to all thoughtful conservation planning. Key issues for designating critical habitat include determining which areas not occupied by the

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species at the time of listing are likely to be essential for a species’ conservation under climate change and how broadly to define the necessary physical and biological features of habitat for occupied habitat, both of which are likely to require changes in scientific approaches.

Recovery Planning The protection of a species under an individual nation’s law or an international agreement is of limited consequence to management without specific guidelines and criteria to provide a framework for the species’ conservation and survival. Once a domestic species is listed under the ESA, the listing agency must develop and implement a recovery plan that includes specific actions to achieve recovery and, to the extent feasible, measurable criteria for determining when it no longer needs ESA protection. Forty of NMFS’ 73 domestic ESA species have final recovery plans, whereas 5 have draft plans, and 16 have plans under development (L. Plants, personal communication). Although the ESA requires that NMFS and USFWS “develop and implement” recovery plans, these agencies do not have the authority to require other federal agencies or nonfederal entities to comply with the plans. Moreover, courts have allowed NMFS and USFWS wide discretion as to how they implement these plans. In practice, the most significant role of recovery plans is in the interagency consultation process (described below). A plan provides overall context for evaluating likely effects of a particular action on the species’ recovery, and the agencies have been working to improve consistency between consultation decisions and recovery plans. Climate change has increasingly been incorporated into new or revised recovery plans over the past decade, but it has not yet been integrated into plans for many climate-threatened species. Over 87% of the 1209 recovery plans developed in the U.S. through 2008 did not address climate change, but 59% of new recovery plans finalized during 2005–2008 did (Povilitis & Suckling 2010). Examples of new and revised recovery plans that incorporate climate change—to some extent—include plans for Puget Sound Chinook salmon (Shared Strategy Development Committee 2007), southern resident killer whales (Orcinus orca) (NMFS 2008a), Stellar sea lions (Eumetopias jubatus) (NMFS 2008b), and Kemp’s ridley sea turtle (Lepidochelys kempii) (NMFS et al. 2011). These plans’ different approaches to climate change include discussing potential effects of climate on species and likelihood of future species-relevant changes in physical and biological conditions, and some provide recommendations to further examine climate-change responses and develop adaptive-management techniques (NMFS 2008a; Povilitis & Suckling 2010; NMFS et al. 2011; Rowland 2011). No plans provide specific conservation strategies under likely climate scenarios. Ideally, recovery plans

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should explain how a species’ status and recovery potential may be affected by climate change (e.g., habitat loss or ecosystem modification) and explore what efforts may be undertaken to reduce other (not related to climate) threats to the species to increase its resilience to climate change. Given the broad effects of climate change and ocean acidification (e.g., Doney et al. 2009; Pereira et al. 2010), such considerations are important in conserving most imperiled species worldwide.

Assessing and Mitigating Effects of Proposed Federal Actions Nearly all conservation planners must assess the effect of specific activities or changes on a species or ecosystem. Stated simply, U.S. agencies that conduct, permit, or fund activities that affect one or more listed species must ensure that the proposed activities are not likely to jeopardize the continued existence of a listed species or destroy or adversely modify designated critical habitat. The agency conducting, permitting, or funding the project consults with NMFS or USFWS (the expert agencies) as to the likely effects of the action. Examples of projects subject to “interagency consultation” are riverbank armoring (Jorgensen et al. 2013), tidal energy development (Busch et al. 2013), and freshwater diversion (Walters et al. 2013). If the action is likely to have adverse effects on a listed species, the consultation concludes with the expert agency’s determination of whether those effects are consistent with ESA requirements and a biological opinion (i.e., a written explanation of the determination). If NMFS or USFWS determines an action is likely to appreciably reduce a species’ likelihood of survival and recovery or result in the destruction or adverse modification of critical habitat, the agency may suggest an alternative, ESA-compliant way to proceed with the project (Ruhl 2008; Rowland 2011). Particular challenges to scientists undertaking interagency consultations involve projecting the environmental baseline (i.e., conditions that are projected to exist in the future, without the proposed action) as it will exist under climate change to determine likely effects of the action on the species’ future status. The likely effects of the proposed action are then added to the species’ projected status under the environmental baseline. Additional challenges include defining the temporal scale of the consultation (multiple articles in this section); defining the action area, or spatial extent of the action (Jorgensen et al. 2013); conducting multispecies assessments (Busch et al. 2013); obtaining downscaled climate projections at appropriate spatial and temporal scales; and assessing the effects of climate change together with those of the proposed action and other actions likely to occur in the same area (Walters et al. 2013). Concerns regarding the

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Table 1. Overview of Endangered Species Act and climate case studies examined by the National Marine Fisheries Service from 2010 through 2012. Location Arctic Circle Puget Sound, Washington Lower Willamette River, Oregon Lemhi River sub-basin, Idaho Pajaro River flood plain, California Northeast U.S. continental shelf Caribbean and Indo-Pacific coral reefs North Pacific and northwest Atlantic Oceans

Species or population segment Bearded seal (Erignathus barbatus) Multiple fish and marine mammal species Upper Willamette River Chinook salmon (Oncorhynchus tshawytscha) Snake River spring and summer Chinook salmon (O. tshawytscha) South-central California Coast steelhead trout (O. mykiss) Cusk (Brosme brosme) Caribbean and Pacific corals Loggerhead sea turtle (Caretta caretta)

Species’ ESA status

Primary reference

E. b. nauticus: threatened

Sea ice habitat

Dahle et al., unpublished

Threatened and endangered

Interagency consultation (proposed tidal power project) Interagency consultation (proposed river bank stabilization)

Busch et al. 2013

Threatened

Jorgensen et al. 2013

Threatened

Interagency consultation (proposed freshwater diversions)

Walters et al. 2013

Threatened

Flood control options

Boughton & Pike 2013

ESA candidate species and NOAA species of Concern 66 of 82 reviewed species proposed for ESA listing North Pacific: endangered; northwest Atlantic: threatened

Species status review (agency initiated)

Hare et al. 2012, also see McClure et al. 2013

Species status review (result of petition finding) Long-term population trends

Brainard et al. 2013

definition of appropriate temporal and geographical scale of analysis apply similarly in other contexts of ESA and other conservation decision making.

Issuance of Incidental Take Permits Managing threatened and endangered species requires decisions about whether specific human activities warrant a detrimental effect on the species. The USFWS or NMFS may issue a permit to a nonfederal entity whose activity is not covered through an interagency consultation to authorize take of a listed species in connection with certain activities. Permits may cover either intentional take “for scientific purposes or to enhance the propagation or survival” of a listed species or take that will be incidental to otherwise lawful activities (U.S.C. Title 16, Section 1539). Examples of activities for which incidental take permits (ITPs) have been issued include commercial and recreational fisheries, water diversion, forest management, and land development. An ITP applicant must prepare a habitat conservation plan (HCP) that reduces the adverse effects of the activity on listed species as much as practicable. The plan may propose measures beneficial to the species to offset unavoidable adverse effects. The standard for issuing a permit is similar to that for reviewing a proposed federal action under ESA Section 7. A permit will be issued if

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Focus

Van Houtan & Halley 2011, also see McClure et al. 2013

the permitting agency (NMFS or USFWS) determines that conducting the activity under the terms of the HCP is not likely to appreciably reduce the species’ likelihood of survival and recovery. As with interagency consultations, the permitting agency will consider the likely effects of climate change on future environmental conditions when determining whether the action covered by the ITP is likely to create an unacceptable degree of risk to the species’ survival and recovery. Likewise, climate change, ocean acidification, and their effects should be addressed and integrated, as appropriate, into an HCP to ensure that it provides for mitigation of both short- and long-term effects and provides sufficient flexibility to adjust conservation measures as new information becomes available (Rowland 2011). Although integration of climate-change information into HCPs has increased in recent years, most still lack explicit linkages between probable effects and management responses (Bernazzani et al. 2012).

Overview of the Articles A changing climate poses new challenges to the conservation of marine and anadromous species due to the strong links between climatic and aquatic processes, the dynamism of aquatic systems, the extensive migrations of many aquatic animals, and uncertainty regarding the pace and magnitude of climate-related changes

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(Hoegh-Guldberg & Bruno 2010; Doney et al. 2012; Boughton & Pike 2013). Moreover, understanding, tracking, and projecting effects of climate change on marine ecosystems is especially complex, generally requiring analysis in 4 nested areas to assess effects on species at higher trophic levels: climate conditions that affect species; ocean physical and chemical conditions; primary and secondary productivity; and the wide variety of lifehistory characteristics indicative of higher trophic levels (Stock et al. 2011). To better understand the challenges climate change presents in conserving threatened and endangered marine and anadromous species, NMFS conducted 8 case studies to explore approaches for including climate change in ESA decision making. The case studies (Table 1) encompassed a range of taxa (invertebrates, teleost fishes, marine mammals, and turtles), ESA decision types, spatial scales, and climate effects. They served not only to address specific ESA-related issues, but also to increase understanding of the challenges of incorporating climate change into conservation planning and improved ability to implement the ESA in a changing world. This special section includes papers generated by 5 of these case studies and examines cross-cutting issues such as selecting and using climate models in conservation planning (Snover et al. 2013) and decision-support applications (Gregory et al. 2013). The ESA is one of the strongest conservation tools in the United States, and its strength derives in large part from reliance on robust science to inform decision making. In the 40 years since its adoption, a strong body of scientific analysis and legal precedent has been established. Although agency and judicial guidance is still evolving, it is clear that the unprecedented changes in global ecosystems—those already occurring and those anticipated—necessitate new approaches to the scientific analyses that underlie critical conservation decisions, including identifying at-risk species, defining environmental baselines, predicting distribution and habitat shifts, and defining appropriate temporal and spatial scales.

Acknowledgments We thank all members of the NMFS Endangered Species Climate Working Group for their contributions to the group’s case studies, workshops, and other projects and for feedback on this paper, including C. Toole who provided the authors useful insights during numerous discussions. We also thank those who provided comments on earlier versions: N. Green, J. Hare, J. Jorgensen, E. Shott, and two anonymous reviewers. J. Howard and K. Watson assisted with figure development. Support for group activities was provided by the NMFS Office of Science and Technology and in-kind support from the

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respective offices of group members. The views and opinions expressed or implied in this article are those of the authors and do not necessarily reflect the position of the National Marine Fisheries Service or the National Oceanic and Atmospheric Administration.

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