Special Section
Incorporating Climate and Ocean Change into Extinction Risk Assessments for 82 Coral Species RUSSELL E. BRAINARD,∗ MARISKA WEIJERMAN,† C. MARK EAKIN,‡ PAUL MCELHANY,§ MARGARET W. MILLER,∗∗ MATT PATTERSON,†† GREGORY A. PINIAK,‡‡ MATTHEW J. DUNLAP,† AND CHARLES BIRKELAND§§ ∗
Pacific Islands Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 1125B Ala Moana Boulevard, Honolulu, HI 96814, U.S.A. email [email protected]. †Joint Institute for Marine and Atmospheric Research, University of Hawaii at Manoa, Honolulu, HI 96822, U.S.A. ‡NOAA Coral Reef Watch, Center for Satellite Applications and Research, National Environmental Satellite, Data and Information Service, National Oceanic and Atmospheric Administration, 5830 University Research Court, College Park, MD 20737, U.S.A. §Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, WA 98112, U.S.A. ∗∗ Southeast Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 75 Virginia Beach Drive, Miami, FL 33149–1099, U.S.A. ††South Florida Inventory & Monitoring Network, National Park Service, 18001 Old Cutler Road Suite 419, Miami, FL 33157, U.S.A. ‡‡National Centers for Coastal Ocean Science, National Ocean Service, National Oceanic and Atmospheric Administration, 1305 East-West Highway, Silver Spring, MD 20910, U.S.A. §§Department of Biology, University of Hawaii at Manoa, 2500 Campus Road, Honolulu, HI 96822, U.S.A.
Abstract: Many marine invertebrate species facing potential extinction have uncertain taxonomies and poorly known demographic and ecological traits. Uncertainties are compounded when potential extinction drivers are climate and ocean changes whose effects on even widespread and abundant species are only partially understood. The U.S. Endangered Species Act mandates conservation management decisions founded on the extinction risk to species based on the best available science at the time of consideration—requiring prompt action rather than awaiting better information. We developed an expert-opinion threat-based approach that entails a structured voting system to assess extinction risk from climate and ocean changes and other threats to 82 coral species for which population status and threat response information was limited. Such methods are urgently needed because constrained budgets and manpower will continue to hinder the availability of desired data for many potentially vulnerable marine species. Significant species-specific information gaps and uncertainties precluded quantitative assessments of habitat loss or population declines and necessitated increased reliance on demographic characteristics and threat vulnerabilities at genus or family levels. Adapting some methods (e.g., a structured voting system) used during other assessments and developing some new approaches (e.g., integrated assessment of threats and demographic characteristics), we rated the importance of threats contributing to coral extinction risk and assessed those threats against population status and trend information to evaluate each species’ extinction risk over the 21st century. This qualitative assessment resulted in a ranking with an uncertainty range for each species according to their estimated likelihood of extinction. We offer guidance on approaches for future biological extinction risk assessments, especially in cases of data-limited species likely to be affected by global-scale threats. Keywords: Climate and ocean change, coral, data-limited species, extinction risk, ESA, risk assessment Incorporaci´ on del Cambio Clim´atico y Oce´anico en Estudios de Riesgo de Extinci´ on para 82 Especies de Coral
Resumen: Muchas especies de invertebrados marinos que enfrentan extinci´on potencial tienen taxonom´ıas inciertas y caracter´ısticas demogr´ aficas y ecol´ ogicas poco conocidas. Las incertidumbres est´ an compuestas cuando los conductores potenciales de extinci´ on son los cambios clim´ aticos y oce´ anicos, cuyos efectos, incluso sobre especies abundantes y con distribuci´ on extensa, son parcialmente entendidos. El Acta Estadunidense
∗ email
[email protected] Paper submitted July 26, 2012; revised manuscript accepted June 29, 2013.
1169 Conservation Biology, Volume 27, No. 6, 1169–1178 C 2013 Society for Conservation Biology DOI: 10.1111/cobi.12171
1170
Climate Change and Coral Extinction Risk
de Especies en Peligro dicta decisiones de manejo de conservaci´ on basadas en el riesgo de extinci´ on para las especies basado en la mejor ciencia disponible en el momento de consideraci´ on, lo que requiere una pronta acci´ on en lugar de esperar mejor informaci´ on. Desarrollamos un acercamiento basado en amenazas y opiniones de expertos que involucra un sistema de votaci´ on estructurado para estudiar el riesgo de extinci´ on a partir de los cambios clim´ aticos y oce´ anicos y otras amenazas para 82 especies de coral, para las cuales la informaci´ on sobre el estado de la poblaci´ on y la respuesta a la amenaza era limitada. Tales m´etodos son una necesidad urgente porque los presupuestos restringidos y la voluntad de la mano de obra continuar´ an dificultando la disponibilidad de la informaci´ on deseada para muchas especies marinas potencialmente vulnerables. Vac´ıos de informaci´ on, significativos y espec´ıficos de especie e incertidumbres impidieron estudios cuantitativos de la p´erdida de h´ abitat o disminuciones poblacionales y requirieron dependencia incrementada de los caracteres demogr´ aficos y las debilidades de amenaza en los niveles de g´enero o familia. Al adaptar algunos m´etodos (p. ej.: un sistema estructurado de votaci´ on) usados durante otros estudios y desarrollando algunos acercamientos nuevos (p. ej.: estudios integrados de amenazas y caracter´ısticas demogr´ aficas), calificamos la importancia de las amenazas que contribuyen al riesgo de extinci´ on de los corales y estudiamos esas amenazas contra el estado de la poblaci´ on y la tendencia de la informaci´ on para evaluar el riesgo de extinci´ on de cada especie en el siglo 21. Este estudio cualitativo result´ o en una clasificaci´ on con un rango de incertidumbre para cada especie de acuerdo a su probabilidad estimada de extinci´ on. Ofrecemos orientaci´ on en los acercamientos para estudios futuros de riesgo de extinci´ on biol´ ogica, especialmente en casos de especies con informaci´ on limitada y con probabilidad de ser afectadas por amenazas a escala global.
Palabras Clave: Cambios clim´aticos y oce´anicos, coral, especies con informaci´on limitada, ESA, evaluaci´on de riesgos, riesgo de extinci´ on
Introduction Many species extinction risk analyses require an accounting of both local and global threats (i.e., climate and ocean change), but it is challenging to develop methods to make scientifically sound and reliable extinctionrisk assessments of species for which little is known. Traditional analyses rely on demographic patterns, but the use of trait-specific, threat-based ecological-risk assessments has been increasing. For even well-studied species, comprehensive information on emerging threats such as climate and ocean changes is often not available. Recent expansions of International Union for Conservation of Nature (IUCN) Red List assessments for sea turtles (Wallace et al. 2011) and pinnipeds (Kovacs et al. 2012) specifically considered potential climate effects. The sea turtle assessment divided species into regional management units (RMUs) but omitted climate change from the overall threat assessment when they found 38 of the 58 RMUs were data deficient with respect to climate-change effects. The pinniped assessment included an extensive summary of climate effects, but in evaluating individual species and subspecies it simply listed climate effects as a primary or impending secondary threat without detailing the species-specific effects. Climate effects were a primary threat for 12 species and an impending secondary threat for 28 more. Eight species did not have climate effects as an explicit concern. In a more comprehensive approach, Chin et al. (2010) devised an integrated risk assessment for climate change that blends 3 components of species vulnerability traits— exposure, sensitivity, and adaptive capacity—with traditional fishery assessments to evaluate sharks and rays on the Great Barrier Reef. Little information was available on
Conservation Biology Volume 27, No. 6, 2013
effects to individual species, so all species within habitats were considered together to determine relative vulnerability to a suite of direct (temperature, acidification, and freshwater input) and indirect climate effects for each habitat. Thirty of the 133 species evaluated were assessed to be highly or moderately vulnerable to climate effects. The authors identified potential actions to reduce risk, but the assessment method itself was not linked to any particular conservation or extinction framework. These examples advanced the assessments of their respective species, but generally efforts to incorporate considerations of climate and ocean change into extinction-risk evaluations are in early developmental stages relative to traditional demographic techniques. In October 2009, the Center for Biological Diversity petitioned the National Marine Fisheries Service (NMFS) to list 83 coral species under the U.S. Endangered Species Act (ESA), citing climate and ocean change-related effects as primary contributing factors in extinction risk. The NMFS determined further assessment was warranted for 82 of the petitioned species and convened a biological review team (BRT) of 7 subject-matter experts (all of whom are authors on this paper) charged with assessing the status of and extinction risk to each species. The ESA requires a comprehensive threat evaluation, so we developed a methodology that was transferable across a suite of threats, both local and global. However, given the large number of species petitioned, significant data gaps were likely. Also, the complex evolutionary history, hybridization, and inconsistencies between classical morphologically based taxonomy and newer genetic approaches (e.g., Veron 1995; Forsman et al. 2010; Pinz´ on & LaJeunesse 2011) even made defining coral species problematic. Because corals are colonial organisms that
Brainard et al.
incur partial mortality and most coral reef surveys identify corals to the genus level, defining individual abundance and population trends was similarly difficult. Our objective here is to present the methods developed for reviewing the status of and extinction risk for the 82 candidate coral species in the climate-based ESA petition and to provide lessons learned for incorporating considerations of climate and ocean change that might be applicable to extinction-risk assessments for other data-limited species.
1171
range of CO2 emission scenarios and collection of global climate models provided projections with adequate confidence to the year 2100 for us to reasonably use this time frame for evaluation of critical-risk thresholds for the candidate coral species. Much of the scientific information available on the potential effects of ocean acidification on corals has likewise been based on IPCC CO2 emission scenarios and model projections.
Components of Extinction Risk General Approach We reviewed species risks at 2 levels—considering key threats to corals in general and evaluating available information on population status and susceptibility to threats that was either available for or applicable to each species. We then used a structured expert-opinion voting system to evaluate the overall risk of extinction for each of the 82 species across its entire range. Absolute extinction is reached when there are zero individuals of a particular species alive. Prior to that, a species may become functionally extinct when extinction is inevitable, although some individuals may still be alive. For more practical conservation management decision making under ESA, we defined the term critical-risk threshold to indicate a condition in which the species is of such low abundance, so spatially fragmented, or at such reduced genetic or genotypic diversity that extinction is extremely likely (conceptually similar to extinction thresholds for habitat fragmentation; Ovaskainen & Hanski 2003). Critical-risk threshold was not defined as a single abundance number, density, spatial distribution, or trend value, but rather as a qualitative description encompassing such characteristics where quantitative information is lacking. In assessing the critical-risk threshold, we considered depensatory processes, environmental stochasticity, catastrophic events, and known local and global anthropogenic stressors, including climate and ocean change, to allow for evaluation despite insufficient data to compute quantitative thresholds for the species. Assessment Time Horizon Lacking a formal ESA definition for foreseeable future, agency policy recommends linking risk evaluation to the time frame over which it is possible to scientifically predict threat effects (U.S. Department of Interior 2009). The analyses and synthesis of information developed for the Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report (AR4) (IPCC 2007) were the most thoroughly documented and reviewed assessments of future climate and ocean change ever issued and represented the best scientific information on potential future changes in Earth’s climate system available at the time the species’ status was reviewed (Brainard et al. 2011). The
The general trends of coral decline and the importance of various global change and local threats are reasonably well documented for corals, but information was sorely lacking on the specifics of how these threats would affect most of the individual candidate species. Therefore, the focus was placed on exposure to threats and susceptibility of the species to them. Here, we evaluated extinction risk for each species by considering 2 separate, but related, types of information: global and local threats, including their intensity and trends (Crawford & Rumsey 2009) and traits, dynamics, and responses of the species to these threats and distribution of the species themselves. In most cases, there was no quantitative species-level information regarding abundance and trends or threat susceptibility. There was also a lack of geographically refined predictions regarding exposure, especially to global threats. Identifying Important Threats We considered status and trends of human population and consumption of natural resources to be the root drivers of the important environmental threats, which fall into 2 main categories: global climate- and oceanchange threats (atmospheric CO2 , ocean warming, ocean acidification, sea-level rise, changing ocean circulation, changing storm characteristics, atmospheric dust, and changes in insolation) and local threats (land-based pollution, disease, predation, fishing and trophic cascades, destructive fishing practices, ornamental trade, natural physical damage, human-induced physical damage, and invasive species). Furthermore, we explicitly considered interactions between threats during the assessment of risks. Evaluating the severity and likelihood of effects based on documented responses to natural changes and experiments from the threats outlined above across the global range of reef corals, we concluded that the 3 most important threats in terms of extinction risk of coral species between now and the year 2100 are ocean warming, disease, and ocean acidification (Table 1). Local threats with widespread effect, such as sedimentation, eutrophication, and fishing, were considered medium extinction risks. Many other threats (e.g., physical damage, invasive
Conservation Biology Volume 27, No. 6, 2013
Climate Change and Coral Extinction Risk
1172 Table 1. Summary of proximate threats considered in assessing extinction risks to the 82 coral species petitioned for listing under the U.S. Endangered Species Act, ordered on the basis of the Coral Biological Review Team’s estimate of the threat’s importance for extinction risk. Scale
Proximate threat
Global Local Global Local
ocean warming disease ocean acidification reef fishing—trophic effects sedimentation nutrients sea-level rise toxins changing ocean circulation changing storm tracks and intensities predation reef fishing—habitat effects, destructive fishing practices ornamental trade natural physical damage human-induced physical damage aquatic invasive species salinity African/Asian dust changes in insolation
Local Local Global Local Global Global Local Local Local Local Local Local Local Local Global
Importance high high medium-high medium low-medium low-medium low-medium low low low low low low low negligible-low negligible-low negligible negligible probably negligible
species, collection, and trade) can cause extirpation at local scales but pose significant extinction risk only for species with restricted geographic ranges or species that have already undergone precipitous population declines. To date, there is little evidence that corals can adapt or acclimate to the projected magnitude and rate of change in environmental conditions (Baskett et al. 2009a, 2009b; Rodolfo-Metalpa et al. 2011), let alone to multiple stressors simultaneously and interactively. Specific mechanisms of climate- and ocean-change threats were examined individually (Table 1) (see Brainard et al. 2011 for a detailed assessment). The 2 greatest global threats to extinction to all or most coral species over the next century were ocean warming and acidification, which will continue to increase as atmospheric CO2 continues to rise. Globally, thermal stress has and will continue to affect corals throughout all or most of their ranges (Hoegh-Guldberg et al. 2007). An association of mass coral bleaching events with rising temperatures began on a large scale in the early 1980s (Glynn 1991; Fitt et al. 2001). The return frequency of mass bleaching events has already begun to exceed the ability of many reefs and coral species to recover (Baker et al. 2008; Eakin et al. 2010), and thermal stress may have already caused the first modern coral extinction (Glynn et al. 2001). Although, it is theoretically possible that future technologi-
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cal or policy changes could reduce these climate threats, management cannot rely on assumptions about future policy changes or technological advances. Moreover, the threat posed by even the most optimistic scenarios of 21st century CO2 emissions used in the IPCC AR4 (IPCC 2007)—or simply the threat posed by committed climate change (Hare & Meinshausen 2006)—represents a plausible extinction risk to many coral species. Fortunately, some combination of field and lab studies on bleaching effects was available for many species being evaluated or their congeners. The magnitude of the threat of ocean acidification to coral reefs has been accepted only within the last decade. The atmospheric CO2 concentration recently surpassed 400 ppm and continues to accelerate, already exceeding the worst-case emission trajectories used in the AR4 (IPCC 2007; Allison et al. 2009). Rising atmospheric CO2 will continue to induce ocean acidification, but there remain many unknowns in understanding of how ocean acidification will affect the diversity and interdependence of marine species. Based on current knowledge and projections for the future, we ranked ocean acidification as a medium-high extinction risk to corals. The severity of this threat to the growth and, particularly, recruitment of corals will make it more difficult for many of them to recover from other effects (reviewed in Brainard et al. 2011). Some corals are already experiencing reproductive impairment and recruitment failure (Hughes & Tanner 2000; Albright et al. 2010; Polato et al. 2010). Unfortunately, ocean acidification effects have been quantified for only a handful of coral species, so we had to assume effects of congeneric or confamilial species would apply to the species being evaluated. It is clear that multiple stressors affect organisms simultaneously and interactively, although it is not certain whether the effects will be additive, multiplicative, or negative. There are numerous examples of climaterelated interactive effects on corals. Growing evidence from both the Caribbean and Indo-Pacific suggests corals experiencing physiological stress from poor-water quality (Carilli et al. 2009; Wooldridge 2009) or ocean acidification (Anthony et al. 2008; Crawley et al. 2010) are more sensitive to high temperatures. Increased seawater temperature also may act synergistically with coral diseases to reduce coral health and survival (Bruno et al. 2007). Although, we first considered the overall importance of separate threats, each species also was assessed on the available information regarding its responses to the identified threats acting interactively and collectively. Species Demography, Ecology, and Traits Ideally, ESA biological reviews should include information on each species’ physiological response and threat susceptibility (van Woesik et al. 2012; Foden et al. 2013), as well as a demographic assessment—but there was a
Brainard et al.
general lack of most of these data for the coral species we considered. The vulnerabilities of different corals to stressors are fundamentally related to natural-history traits that are often common to genera or even families. Although, we were cautious regarding presumed ecological similarities among the species within a genus, some reliable intrageneric traits were used as indicators of likely species-level vulnerabilities. For example, members of the genus Acropora have high-growth rates and porous skeletons. However, their thin superficial tissues provide low-energy reserves, and they consistently display high sensitivity to a range of stressors (e.g., increased temperatures, sedimentation, disease, and predation). Hence, Acropora species are usually among the first corals to show substantial losses under stressful conditions, putting that genus at relatively high risk to some of the climate-related and disease threats. That said, it is recognized that such traits may also provide opportunities for potentially rapid recovery. Lacking much of the desired information on speciesspecific susceptibility, the modern known geographic and habitat distributions of each species were used as proxies for species’ threat exposures and responses. In the case of invertebrates, the ESA requires that evaluation and protection be applied across a species’ entire range. Many corals have vast ranges spanning much of the global tropics. Population trends were available for only a few (
Incorporating Climate and Ocean Change into Extinction Risk Assessments for 82 Coral Species RUSSELL E. BRAINARD,∗ MARISKA WEIJERMAN,† C. MARK EAKIN,‡ PAUL MCELHANY,§ MARGARET W. MILLER,∗∗ MATT PATTERSON,†† GREGORY A. PINIAK,‡‡ MATTHEW J. DUNLAP,† AND CHARLES BIRKELAND§§ ∗
Pacific Islands Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 1125B Ala Moana Boulevard, Honolulu, HI 96814, U.S.A. email [email protected]. †Joint Institute for Marine and Atmospheric Research, University of Hawaii at Manoa, Honolulu, HI 96822, U.S.A. ‡NOAA Coral Reef Watch, Center for Satellite Applications and Research, National Environmental Satellite, Data and Information Service, National Oceanic and Atmospheric Administration, 5830 University Research Court, College Park, MD 20737, U.S.A. §Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, WA 98112, U.S.A. ∗∗ Southeast Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 75 Virginia Beach Drive, Miami, FL 33149–1099, U.S.A. ††South Florida Inventory & Monitoring Network, National Park Service, 18001 Old Cutler Road Suite 419, Miami, FL 33157, U.S.A. ‡‡National Centers for Coastal Ocean Science, National Ocean Service, National Oceanic and Atmospheric Administration, 1305 East-West Highway, Silver Spring, MD 20910, U.S.A. §§Department of Biology, University of Hawaii at Manoa, 2500 Campus Road, Honolulu, HI 96822, U.S.A.
Abstract: Many marine invertebrate species facing potential extinction have uncertain taxonomies and poorly known demographic and ecological traits. Uncertainties are compounded when potential extinction drivers are climate and ocean changes whose effects on even widespread and abundant species are only partially understood. The U.S. Endangered Species Act mandates conservation management decisions founded on the extinction risk to species based on the best available science at the time of consideration—requiring prompt action rather than awaiting better information. We developed an expert-opinion threat-based approach that entails a structured voting system to assess extinction risk from climate and ocean changes and other threats to 82 coral species for which population status and threat response information was limited. Such methods are urgently needed because constrained budgets and manpower will continue to hinder the availability of desired data for many potentially vulnerable marine species. Significant species-specific information gaps and uncertainties precluded quantitative assessments of habitat loss or population declines and necessitated increased reliance on demographic characteristics and threat vulnerabilities at genus or family levels. Adapting some methods (e.g., a structured voting system) used during other assessments and developing some new approaches (e.g., integrated assessment of threats and demographic characteristics), we rated the importance of threats contributing to coral extinction risk and assessed those threats against population status and trend information to evaluate each species’ extinction risk over the 21st century. This qualitative assessment resulted in a ranking with an uncertainty range for each species according to their estimated likelihood of extinction. We offer guidance on approaches for future biological extinction risk assessments, especially in cases of data-limited species likely to be affected by global-scale threats. Keywords: Climate and ocean change, coral, data-limited species, extinction risk, ESA, risk assessment Incorporaci´ on del Cambio Clim´atico y Oce´anico en Estudios de Riesgo de Extinci´ on para 82 Especies de Coral
Resumen: Muchas especies de invertebrados marinos que enfrentan extinci´on potencial tienen taxonom´ıas inciertas y caracter´ısticas demogr´ aficas y ecol´ ogicas poco conocidas. Las incertidumbres est´ an compuestas cuando los conductores potenciales de extinci´ on son los cambios clim´ aticos y oce´ anicos, cuyos efectos, incluso sobre especies abundantes y con distribuci´ on extensa, son parcialmente entendidos. El Acta Estadunidense
[email protected] Paper submitted July 26, 2012; revised manuscript accepted June 29, 2013.
1169 Conservation Biology, Volume 27, No. 6, 1169–1178 C 2013 Society for Conservation Biology DOI: 10.1111/cobi.12171
1170
Climate Change and Coral Extinction Risk
de Especies en Peligro dicta decisiones de manejo de conservaci´ on basadas en el riesgo de extinci´ on para las especies basado en la mejor ciencia disponible en el momento de consideraci´ on, lo que requiere una pronta acci´ on en lugar de esperar mejor informaci´ on. Desarrollamos un acercamiento basado en amenazas y opiniones de expertos que involucra un sistema de votaci´ on estructurado para estudiar el riesgo de extinci´ on a partir de los cambios clim´ aticos y oce´ anicos y otras amenazas para 82 especies de coral, para las cuales la informaci´ on sobre el estado de la poblaci´ on y la respuesta a la amenaza era limitada. Tales m´etodos son una necesidad urgente porque los presupuestos restringidos y la voluntad de la mano de obra continuar´ an dificultando la disponibilidad de la informaci´ on deseada para muchas especies marinas potencialmente vulnerables. Vac´ıos de informaci´ on, significativos y espec´ıficos de especie e incertidumbres impidieron estudios cuantitativos de la p´erdida de h´ abitat o disminuciones poblacionales y requirieron dependencia incrementada de los caracteres demogr´ aficos y las debilidades de amenaza en los niveles de g´enero o familia. Al adaptar algunos m´etodos (p. ej.: un sistema estructurado de votaci´ on) usados durante otros estudios y desarrollando algunos acercamientos nuevos (p. ej.: estudios integrados de amenazas y caracter´ısticas demogr´ aficas), calificamos la importancia de las amenazas que contribuyen al riesgo de extinci´ on de los corales y estudiamos esas amenazas contra el estado de la poblaci´ on y la tendencia de la informaci´ on para evaluar el riesgo de extinci´ on de cada especie en el siglo 21. Este estudio cualitativo result´ o en una clasificaci´ on con un rango de incertidumbre para cada especie de acuerdo a su probabilidad estimada de extinci´ on. Ofrecemos orientaci´ on en los acercamientos para estudios futuros de riesgo de extinci´ on biol´ ogica, especialmente en casos de especies con informaci´ on limitada y con probabilidad de ser afectadas por amenazas a escala global.
Palabras Clave: Cambios clim´aticos y oce´anicos, coral, especies con informaci´on limitada, ESA, evaluaci´on de riesgos, riesgo de extinci´ on
Introduction Many species extinction risk analyses require an accounting of both local and global threats (i.e., climate and ocean change), but it is challenging to develop methods to make scientifically sound and reliable extinctionrisk assessments of species for which little is known. Traditional analyses rely on demographic patterns, but the use of trait-specific, threat-based ecological-risk assessments has been increasing. For even well-studied species, comprehensive information on emerging threats such as climate and ocean changes is often not available. Recent expansions of International Union for Conservation of Nature (IUCN) Red List assessments for sea turtles (Wallace et al. 2011) and pinnipeds (Kovacs et al. 2012) specifically considered potential climate effects. The sea turtle assessment divided species into regional management units (RMUs) but omitted climate change from the overall threat assessment when they found 38 of the 58 RMUs were data deficient with respect to climate-change effects. The pinniped assessment included an extensive summary of climate effects, but in evaluating individual species and subspecies it simply listed climate effects as a primary or impending secondary threat without detailing the species-specific effects. Climate effects were a primary threat for 12 species and an impending secondary threat for 28 more. Eight species did not have climate effects as an explicit concern. In a more comprehensive approach, Chin et al. (2010) devised an integrated risk assessment for climate change that blends 3 components of species vulnerability traits— exposure, sensitivity, and adaptive capacity—with traditional fishery assessments to evaluate sharks and rays on the Great Barrier Reef. Little information was available on
Conservation Biology Volume 27, No. 6, 2013
effects to individual species, so all species within habitats were considered together to determine relative vulnerability to a suite of direct (temperature, acidification, and freshwater input) and indirect climate effects for each habitat. Thirty of the 133 species evaluated were assessed to be highly or moderately vulnerable to climate effects. The authors identified potential actions to reduce risk, but the assessment method itself was not linked to any particular conservation or extinction framework. These examples advanced the assessments of their respective species, but generally efforts to incorporate considerations of climate and ocean change into extinction-risk evaluations are in early developmental stages relative to traditional demographic techniques. In October 2009, the Center for Biological Diversity petitioned the National Marine Fisheries Service (NMFS) to list 83 coral species under the U.S. Endangered Species Act (ESA), citing climate and ocean change-related effects as primary contributing factors in extinction risk. The NMFS determined further assessment was warranted for 82 of the petitioned species and convened a biological review team (BRT) of 7 subject-matter experts (all of whom are authors on this paper) charged with assessing the status of and extinction risk to each species. The ESA requires a comprehensive threat evaluation, so we developed a methodology that was transferable across a suite of threats, both local and global. However, given the large number of species petitioned, significant data gaps were likely. Also, the complex evolutionary history, hybridization, and inconsistencies between classical morphologically based taxonomy and newer genetic approaches (e.g., Veron 1995; Forsman et al. 2010; Pinz´ on & LaJeunesse 2011) even made defining coral species problematic. Because corals are colonial organisms that
Brainard et al.
incur partial mortality and most coral reef surveys identify corals to the genus level, defining individual abundance and population trends was similarly difficult. Our objective here is to present the methods developed for reviewing the status of and extinction risk for the 82 candidate coral species in the climate-based ESA petition and to provide lessons learned for incorporating considerations of climate and ocean change that might be applicable to extinction-risk assessments for other data-limited species.
1171
range of CO2 emission scenarios and collection of global climate models provided projections with adequate confidence to the year 2100 for us to reasonably use this time frame for evaluation of critical-risk thresholds for the candidate coral species. Much of the scientific information available on the potential effects of ocean acidification on corals has likewise been based on IPCC CO2 emission scenarios and model projections.
Components of Extinction Risk General Approach We reviewed species risks at 2 levels—considering key threats to corals in general and evaluating available information on population status and susceptibility to threats that was either available for or applicable to each species. We then used a structured expert-opinion voting system to evaluate the overall risk of extinction for each of the 82 species across its entire range. Absolute extinction is reached when there are zero individuals of a particular species alive. Prior to that, a species may become functionally extinct when extinction is inevitable, although some individuals may still be alive. For more practical conservation management decision making under ESA, we defined the term critical-risk threshold to indicate a condition in which the species is of such low abundance, so spatially fragmented, or at such reduced genetic or genotypic diversity that extinction is extremely likely (conceptually similar to extinction thresholds for habitat fragmentation; Ovaskainen & Hanski 2003). Critical-risk threshold was not defined as a single abundance number, density, spatial distribution, or trend value, but rather as a qualitative description encompassing such characteristics where quantitative information is lacking. In assessing the critical-risk threshold, we considered depensatory processes, environmental stochasticity, catastrophic events, and known local and global anthropogenic stressors, including climate and ocean change, to allow for evaluation despite insufficient data to compute quantitative thresholds for the species. Assessment Time Horizon Lacking a formal ESA definition for foreseeable future, agency policy recommends linking risk evaluation to the time frame over which it is possible to scientifically predict threat effects (U.S. Department of Interior 2009). The analyses and synthesis of information developed for the Intergovernmental Panel on Climate Change (IPCC) Fourth Assessment Report (AR4) (IPCC 2007) were the most thoroughly documented and reviewed assessments of future climate and ocean change ever issued and represented the best scientific information on potential future changes in Earth’s climate system available at the time the species’ status was reviewed (Brainard et al. 2011). The
The general trends of coral decline and the importance of various global change and local threats are reasonably well documented for corals, but information was sorely lacking on the specifics of how these threats would affect most of the individual candidate species. Therefore, the focus was placed on exposure to threats and susceptibility of the species to them. Here, we evaluated extinction risk for each species by considering 2 separate, but related, types of information: global and local threats, including their intensity and trends (Crawford & Rumsey 2009) and traits, dynamics, and responses of the species to these threats and distribution of the species themselves. In most cases, there was no quantitative species-level information regarding abundance and trends or threat susceptibility. There was also a lack of geographically refined predictions regarding exposure, especially to global threats. Identifying Important Threats We considered status and trends of human population and consumption of natural resources to be the root drivers of the important environmental threats, which fall into 2 main categories: global climate- and oceanchange threats (atmospheric CO2 , ocean warming, ocean acidification, sea-level rise, changing ocean circulation, changing storm characteristics, atmospheric dust, and changes in insolation) and local threats (land-based pollution, disease, predation, fishing and trophic cascades, destructive fishing practices, ornamental trade, natural physical damage, human-induced physical damage, and invasive species). Furthermore, we explicitly considered interactions between threats during the assessment of risks. Evaluating the severity and likelihood of effects based on documented responses to natural changes and experiments from the threats outlined above across the global range of reef corals, we concluded that the 3 most important threats in terms of extinction risk of coral species between now and the year 2100 are ocean warming, disease, and ocean acidification (Table 1). Local threats with widespread effect, such as sedimentation, eutrophication, and fishing, were considered medium extinction risks. Many other threats (e.g., physical damage, invasive
Conservation Biology Volume 27, No. 6, 2013
Climate Change and Coral Extinction Risk
1172 Table 1. Summary of proximate threats considered in assessing extinction risks to the 82 coral species petitioned for listing under the U.S. Endangered Species Act, ordered on the basis of the Coral Biological Review Team’s estimate of the threat’s importance for extinction risk. Scale
Proximate threat
Global Local Global Local
ocean warming disease ocean acidification reef fishing—trophic effects sedimentation nutrients sea-level rise toxins changing ocean circulation changing storm tracks and intensities predation reef fishing—habitat effects, destructive fishing practices ornamental trade natural physical damage human-induced physical damage aquatic invasive species salinity African/Asian dust changes in insolation
Local Local Global Local Global Global Local Local Local Local Local Local Local Local Global
Importance high high medium-high medium low-medium low-medium low-medium low low low low low low low negligible-low negligible-low negligible negligible probably negligible
species, collection, and trade) can cause extirpation at local scales but pose significant extinction risk only for species with restricted geographic ranges or species that have already undergone precipitous population declines. To date, there is little evidence that corals can adapt or acclimate to the projected magnitude and rate of change in environmental conditions (Baskett et al. 2009a, 2009b; Rodolfo-Metalpa et al. 2011), let alone to multiple stressors simultaneously and interactively. Specific mechanisms of climate- and ocean-change threats were examined individually (Table 1) (see Brainard et al. 2011 for a detailed assessment). The 2 greatest global threats to extinction to all or most coral species over the next century were ocean warming and acidification, which will continue to increase as atmospheric CO2 continues to rise. Globally, thermal stress has and will continue to affect corals throughout all or most of their ranges (Hoegh-Guldberg et al. 2007). An association of mass coral bleaching events with rising temperatures began on a large scale in the early 1980s (Glynn 1991; Fitt et al. 2001). The return frequency of mass bleaching events has already begun to exceed the ability of many reefs and coral species to recover (Baker et al. 2008; Eakin et al. 2010), and thermal stress may have already caused the first modern coral extinction (Glynn et al. 2001). Although, it is theoretically possible that future technologi-
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cal or policy changes could reduce these climate threats, management cannot rely on assumptions about future policy changes or technological advances. Moreover, the threat posed by even the most optimistic scenarios of 21st century CO2 emissions used in the IPCC AR4 (IPCC 2007)—or simply the threat posed by committed climate change (Hare & Meinshausen 2006)—represents a plausible extinction risk to many coral species. Fortunately, some combination of field and lab studies on bleaching effects was available for many species being evaluated or their congeners. The magnitude of the threat of ocean acidification to coral reefs has been accepted only within the last decade. The atmospheric CO2 concentration recently surpassed 400 ppm and continues to accelerate, already exceeding the worst-case emission trajectories used in the AR4 (IPCC 2007; Allison et al. 2009). Rising atmospheric CO2 will continue to induce ocean acidification, but there remain many unknowns in understanding of how ocean acidification will affect the diversity and interdependence of marine species. Based on current knowledge and projections for the future, we ranked ocean acidification as a medium-high extinction risk to corals. The severity of this threat to the growth and, particularly, recruitment of corals will make it more difficult for many of them to recover from other effects (reviewed in Brainard et al. 2011). Some corals are already experiencing reproductive impairment and recruitment failure (Hughes & Tanner 2000; Albright et al. 2010; Polato et al. 2010). Unfortunately, ocean acidification effects have been quantified for only a handful of coral species, so we had to assume effects of congeneric or confamilial species would apply to the species being evaluated. It is clear that multiple stressors affect organisms simultaneously and interactively, although it is not certain whether the effects will be additive, multiplicative, or negative. There are numerous examples of climaterelated interactive effects on corals. Growing evidence from both the Caribbean and Indo-Pacific suggests corals experiencing physiological stress from poor-water quality (Carilli et al. 2009; Wooldridge 2009) or ocean acidification (Anthony et al. 2008; Crawley et al. 2010) are more sensitive to high temperatures. Increased seawater temperature also may act synergistically with coral diseases to reduce coral health and survival (Bruno et al. 2007). Although, we first considered the overall importance of separate threats, each species also was assessed on the available information regarding its responses to the identified threats acting interactively and collectively. Species Demography, Ecology, and Traits Ideally, ESA biological reviews should include information on each species’ physiological response and threat susceptibility (van Woesik et al. 2012; Foden et al. 2013), as well as a demographic assessment—but there was a
Brainard et al.
general lack of most of these data for the coral species we considered. The vulnerabilities of different corals to stressors are fundamentally related to natural-history traits that are often common to genera or even families. Although, we were cautious regarding presumed ecological similarities among the species within a genus, some reliable intrageneric traits were used as indicators of likely species-level vulnerabilities. For example, members of the genus Acropora have high-growth rates and porous skeletons. However, their thin superficial tissues provide low-energy reserves, and they consistently display high sensitivity to a range of stressors (e.g., increased temperatures, sedimentation, disease, and predation). Hence, Acropora species are usually among the first corals to show substantial losses under stressful conditions, putting that genus at relatively high risk to some of the climate-related and disease threats. That said, it is recognized that such traits may also provide opportunities for potentially rapid recovery. Lacking much of the desired information on speciesspecific susceptibility, the modern known geographic and habitat distributions of each species were used as proxies for species’ threat exposures and responses. In the case of invertebrates, the ESA requires that evaluation and protection be applied across a species’ entire range. Many corals have vast ranges spanning much of the global tropics. Population trends were available for only a few (
