Taxonomic and Geographic Patterns of Decline for Threatened and Endangered Species in the United States

Abstract: Species listed under the U.S. Endangered Species Act (i.e., listed species) have declined to the point that the probability of their extinction is high. The decline of these species, however, may manifest itself in different ways, including reductions in geographic range, number of populations, or overall abundance. Understanding the pattern of decline can help managers assess extinction probability and define recovery objectives. Although quantitative data on changes in geographic range, number of populations, and abundance usually do not exist for listed species, more often qualitative data can be obtained. We used qualitative data in recovery plans for federally listed species to determine whether each listed species declined in range size, number of populations, or abundance relative to historical levels. We calculated the proportion of listed species in each state (or equivalent) that declined in each of those ways. Nearly all listed species declined in abundance, and range size or number of populations declined in approximately 80% of species for which those data were available. Patterns of decline, however, differed taxonomically and geographically. Declines in range were more common among vertebrates than plants, whereas population extirpations were more common among plants. Invertebrates had high incidence of range and population declines. Narrowly distributed plants and invertebrates may be subject to acute threats that may result in population extirpations, whereas vertebrates may be affected by chronic threats that reduce the extent and size of populations. Additionally, in the eastern United States and U.S. coastal areas, where the level of land conversion is high, a greater percentage of species’ ranges declined and more populations were extirpated than in other areas. Species in the Southwest, especially plants, had fewer range and population declines than other areas. Such relations may help in the selection of species’ recovery criteria.     

The role of scientists in statutory interpretation of the U.S. Endangered Species Act

Like many federal statutes, the U.S. Endangered Species Act (ESA) contains vague or ambiguous language. The meaning imparted to the ESA's unclear language can profoundly impact the fates of endangered and threatened species. Hence, conservation scientists should contribute to the interpretation of the ESA when vague or ambiguous language contains scientific words or refers to scientific concepts. Scientists need to know at least these 2 facts about statutory interpretation: statutory interpretation is subjective and the potential influence of normative values results in different expectations for the parties involved. With the possible exception of judges, all conventional participants in statutory interpretation are serving their own interests, advocating for their preferred policies, or biased. Hence, scientists can play a unique role by informing the interpretative process with objective, policy‐neutral information. Conversely, scientists may act as advocates for their preferred interpretation of unclear statutory language. The different roles scientists might play in statutory interpretation raise the issues of advocacy and competency. Advocating for a preferred statutory interpretation is legitimate political behavior by scientists, but statutory interpretation can be strongly influenced by normative values. Therefore, scientists must be careful not to commit stealth policy advocacy. Most conservation scientists lack demonstrable competence in statutory interpretation and therefore should consult or collaborate with lawyers when interpreting statutes. Professional scientific societies are widely perceived by the public as unbiased sources of objective information. Therefore, professional scientific societies should remain policy neutral and present all interpretations of unclear statutory language; explain the semantics and science both supporting and contradicting each interpretation; and describe the potential consequences of implementing each interpretation. A review of scientists’ interpretations of the phrase “significant portion of its range” in the ESA is used to critique the role of scientists and professional societies in statutory interpretation.     

Quantification of Extinction Risk: IUCN's System for Classifying Threatened Species

Abstract: The International Union for Conservation of Nature (IUCN) Red List of Threatened Species was increasingly used during the 1980s to assess the conservation status of species for policy and planning purposes. This use stimulated the development of a new set of quantitative criteria for listing species in the categories of threat: critically endangered, endangered, and vulnerable. These criteria, which were intended to be applicable to all species except microorganisms, were part of a broader system for classifying threatened species and were fully implemented by IUCN in 2000. The system and the criteria have been widely used by conservation practitioners and scientists and now underpin one indicator being used to assess the Convention on Biological Diversity 2010 biodiversity target. We describe the process and the technical background to the IUCN Red List system. The criteria refer to fundamental biological processes underlying population decline and extinction. But given major differences between species, the threatening processes affecting them, and the paucity of knowledge relating to most species, the IUCN system had to be both broad and flexible to be applicable to the majority of described species. The system was designed to measure the symptoms of extinction risk, and uses 5 independent criteria relating to aspects of population loss and decline of range size. A species is assigned to a threat category if it meets the quantitative threshold for at least one criterion. The criteria and the accompanying rules and guidelines used by IUCN are intended to increase the consistency, transparency, and validity of its categorization system, but it necessitates some compromises that affect the applicability of the system and the species lists that result. In particular, choices were made over the assessment of uncertainty, poorly known species, depleted species, population decline, restricted ranges, and rarity; all of these affect the way red lists should be viewed and used. Processes related to priority setting and the development of national red lists need to take account of some assumptions in the formulation of the criteria.     

Floodplain Rehabilitation as a Hedge against Hydroclimatic Uncertainty in a Migration Corridor of Threatened Steelhead

A strategy for recovering endangered species during climate change is to restore ecosystem processes that moderate effects of climate shifts. In mid‐latitudes, storm patterns may shift their intensity, duration, and frequency. These shifts threaten flooding in human communities and reduce migration windows (conditions suitable for migration after a storm) for fish. Rehabilitation of historic floodplains can in principle reduce these threats via transient storage of storm water, but no one has quantified the benefit of floodplain rehabilitation for migrating fish, a widespread biota with conservation and economic value. We used simple models to quantify migration opportunity for a threatened migratory fish, steelhead (Oncorhynchus mykiss), in an episodic rain‐fed river system, the Pajaro River in central California. We combined flow models, bioenergetic models, and existing climate projections to estimate the sensitivity of migration windows to altered storm patterns under alternate scenarios of floodplain rehabilitation. Generally, migration opportunities were insensitive to warming, weakly sensitive to duration or intensity of storms, and proportionately sensitive to frequency of storms. The rehabilitation strategy expanded migration windows by 16–28% regardless of climate outcomes. Warmer conditions raised the energy cost of migrating, but not enough to matter biologically. Novel findings were that fewer storms appeared to pose a bigger threat to migrating steelhead than warmer or smaller storms and that floodplain rehabilitation lessened the risk from fewer or smaller storms across all plausible hydroclimatic outcomes. It follows that statistical downscaling methods may mischaracterize risk, depending on how they resolve overall precipitation shifts into changes of storm frequency as opposed to storm size. Moreover, anticipating effects of climate shifts that are irreducibly uncertain (here, rainfall) may be more important than anticipating effects of relatively predictable changes such as warming. This highlights a need to credibly identify strategies of ecosystem rehabilitation that are robust to uncertainty. Rehabilitación de Planicies Inundables como Cerco contra la Incertidumbre Hidroclimática en un Corredor Migratorio de Oncorhynchus mykiss, Especie Amenazada     

Public Willingness to Pay for Recovering and Downlisting Threatened and Endangered Marine Species

Abstract: Nonmarket valuation research has produced economic value estimates for a variety of threatened, endangered, and rare species around the world. Although over 40 value estimates exist, it is often difficult to compare values from different studies due to variations in study design, implementation, and modeling specifications. We conducted a stated‐preference choice experiment to estimate the value of recovering or downlisting 8 threatened and endangered marine species in the United States: loggerhead sea turtle (Caretta caretta), leatherback sea turtle (Dermochelys coriacea), North Atlantic right whale (Eubalaena glacialis), North Pacific right whale (Eubalaena japonica), upper Willamette River Chinook salmon (Oncorhynchus tshawytscha), Puget Sound Chinook salmon (Oncorhynchus tshawytscha), Hawaiian monk seals (Monachus schauinslandi), and smalltooth sawfish (Pristis pectinata). In May 2009, we surveyed a random sample of U.S. households. We collected data from 8476 households and estimated willingness to pay for recovering and downlisting the 8 species from these data. Respondents were willing to pay for recovering and downlisting threatened and endangered marine taxa. Willingness‐to‐pay values ranged from $40/household for recovering Puget Sound Chinook salmon to $73/household for recovering the North Pacific right whale. Statistical comparisons among willingness‐to‐pay values suggest that some taxa are more economically valuable than others, which suggests that the U.S. public's willingness to pay for recovery may vary by species.     

Incorporating Climate Science in Applications of the U.S. Endangered Species Act for Aquatic Species

Aquatic species are threatened by climate change but have received comparatively less attention than terrestrial species. We gleaned key strategies for scientists and managers seeking to address climate change in aquatic conservation planning from the literature and existing knowledge. We address 3 categories of conservation effort that rely on scientific analysis and have particular application under the U.S. Endangered Species Act (ESA): assessment of overall risk to a species; long‐term recovery planning; and evaluation of effects of specific actions or perturbations. Fewer data are available for aquatic species to support these analyses, and climate effects on aquatic systems are poorly characterized. Thus, we recommend scientists conducting analyses supporting ESA decisions develop a conceptual model that links climate, habitat, ecosystem, and species response to changing conditions and use this model to organize analyses and future research. We recommend that current climate conditions are not appropriate for projections used in ESA analyses and that long‐term projections of climate‐change effects provide temporal context as a species‐wide assessment provides spatial context. In these projections, climate change should not be discounted solely because the magnitude of projected change at a particular time is uncertain when directionality of climate change is clear. Identifying likely future habitat at the species scale will indicate key refuges and potential range shifts. However, the risks and benefits associated with errors in modeling future habitat are not equivalent. The ESA offers mechanisms for increasing the overall resilience and resistance of species to climate changes, including establishing recovery goals requiring increased genetic and phenotypic diversity, specifying critical habitat in areas not currently occupied but likely to become important, and using adaptive management. Incorporación de las Ciencias Climáticas en las Aplicaciones del Acta Estadunidense de Especies en Peligro para Especies Acuáticas     

Actual and Potential Use of Population Viability Analyses in Recovery of Plant Species Listed under the U.S. Endangered Species Act

Use of population viability analyses (PVAs) in endangered species recovery planning has been met with both support and criticism. Previous reviews promote use of PVA for setting scientifically based, measurable, and objective recovery criteria and recommend improvements to increase the framework's utility. However, others have questioned the value of PVA models for setting recovery criteria and assert that PVAs are more appropriate for understanding relative trade‐offs between alternative management actions. We reviewed 258 final recovery plans for 642 plants listed under the U.S. Endangered Species Act to determine the number of plans that used or recommended PVA in recovery planning. We also reviewed 223 publications that describe plant PVAs to assess how these models were designed and whether those designs reflected previous recommendations for improvement of PVAs. Twenty‐four percent of listed species had recovery plans that used or recommended PVA. In publications, the typical model was a matrix population model parameterized with ≤5 years of demographic data that did not consider stochasticity, genetics, density dependence, seed banks, vegetative reproduction, dormancy, threats, or management strategies. Population growth rates for different populations of the same species or for the same population at different points in time were often statistically different or varied by >10%. Therefore, PVAs parameterized with underlying vital rates that vary to this degree may not accurately predict recovery objectives across a species’ entire distribution or over longer time scales. We assert that PVA, although an important tool as part of an adaptive‐management program, can help to determine quantitative recovery criteria only if more long‐term data sets that capture spatiotemporal variability in vital rates become available. Lacking this, there is a strong need for viable and comprehensive methods for determining quantitative, science‐based recovery criteria for endangered species with minimal data availability. Uso Actual y Potencial del Análisis de Viabilidad Poblacional para la Recuperación de Especies de Plantas Enlistadas en el Acta de Especies En Peligro de E.U.A     

Quantitative tools for implementing the new definition of significant portion of the range in the U.S. Endangered Species Act

In 2014, the Fish and Wildlife Service (FWS) and National Marine Fisheries Service announced a new policy interpretation for the U.S. Endangered Species Act (ESA). According to the act, a species must be listed as threatened or endangered if it is determined to be threatened or endangered in a significant portion of its range (SPR). The 2014 policy seeks to provide consistency by establishing that a portion of the range should be considered significant if the associated individuals’ “removal would cause the entire species to become endangered or threatened.” We reviewed 20 quantitative techniques used to assess whether a portion of a species’ range is significant according to the new guidance. Our assessments are based on the 3R criteria—redundancy (i.e., buffering from catastrophe), resiliency (i.e., ability to withstand stochasticity), and representation (i.e., ability to evolve)—that the FWS uses to determine if a species merits listing. We identified data needs for each quantitative technique and considered which methods could be implemented given the data limitations typical of rare species. We also identified proxies for the 3Rs that may be used with limited data. To assess potential data availability, we evaluated 7 example species by accessing data in their species status assessments, which document all the information used during a listing decision. In all species, an SPR could be evaluated with at least one metric for each of the 3Rs robustly or with substantial assumptions. Resiliency assessments appeared most constrained by limited data, and many species lacked information on connectivity between subpopulations, genetic variation, and spatial variability in vital rates. These data gaps will likely make SPR assessments for species with complex life histories or that cross national boundaries difficult. Although we reviewed techniques for the ESA, other countries require identification of significant areas and could benefit from this research.     

Thresholds of species loss in Amazonian deforestation frontier landscapes

In the Brazilian Amazon, private land accounts for the majority of remaining native vegetation. Understanding how land‐use change affects the composition and distribution of biodiversity in farmlands is critical for improving conservation strategies in the face of rapid agricultural expansion. Working across an area exceeding 3 million ha in the southwestern state of Rondônia, we assessed how the extent and configuration of remnant forest in replicate 10,000‐ha landscapes has affected the occurrence of a suite of Amazonian mammals and birds. In each of 31 landscapes, we used field sampling and semistructured interviews with landowners to determine the presence of 28 large and medium sized mammals and birds, as well as a further 7 understory birds. We then combined results of field surveys and interviews with a probabilistic model of deforestation. We found strong evidence for a threshold response of sampled biodiversity to landscape level forest cover; landscapes with <30–40% forest cover hosted markedly fewer species. Results from field surveys and interviews yielded similar thresholds. These results imply that in partially deforested landscapes many species are susceptible to extirpation following relatively small additional reductions in forest area. In the model of deforestation by 2030 the number of 10,000‐ha landscapes under a conservative threshold of 43% forest cover almost doubled, such that only 22% of landscapes would likely to be able to sustain at least 75% of the 35 focal species we sampled. Brazilian law requires rural property owners in the Amazon to retain 80% forest cover, although this is rarely achieved. Prioritizing efforts to ensure that entire landscapes, rather than individual farms, retain at least 50% forest cover may help safeguard native biodiversity in private forest reserves in the Amazon. Umbrales de Pérdida de Especies en los Paisajes Fronterizos de Deforestación en el Amazonas Ochoa‐Quintero     

Using Ecological Function to Develop Recovery Criteria for Depleted Species: Sea Otters and Kelp Forests in the Aleutian Archipelago

Abstract: Recovery criteria for depleted species or populations normally are based on demographic measures, the goal being to maintain enough individuals over a sufficiently large area to assure a socially tolerable risk of future extinction. Such demographically based recovery criteria may be insufficient to restore the functional roles of strongly interacting species. We explored the idea of developing a recovery criterion for sea otters (Enhydra lutris) in the Aleutian archipelago on the basis of their keystone role in kelp forest ecosystems. We surveyed sea otters and rocky reef habitats at 34 island‐time combinations. The system nearly always existed in either a kelp‐dominated or deforested phase state, which was predictable from sea otter density. We used a resampling analysis of these data to show that the phase state at any particular island can be determined at 95% probability of correct classification with information from as few as six sites. When sea otter population status (and thus the phase state of the kelp forest) was allowed to vary randomly among islands, just 15 islands had to be sampled to estimate the true proportion that were kelp dominated (within 10%) with 90% confidence. We conclude that kelp forest phase state is a more appropriate, sensitive, and cost‐effective measure of sea otter recovery than the more traditional demographically based metrics, and we suggest that similar approaches have broad potential utility in establishing recovery criteria for depleted populations of other functionally important species.     

Estimating Effects of Tidal Power Projects and Climate Change on Threatened and Endangered Marine Species and Their Food Web

Marine hydrokinetic power projects will operate as marine environments change in response to increased atmospheric carbon dioxide concentrations. We considered how tidal power development and stressors resulting from climate change may affect Puget Sound species listed under the U.S. Endangered Species Act (ESA) and their food web. We used risk tables to assess the singular and combined effects of tidal power development and climate change. Tidal power development and climate change posed risks to ESA‐listed species, and risk increased with incorporation of the effects of these stressors on predators and prey of ESA‐listed species. In contrast, results of a model of strikes on ESA‐listed species from turbine blades suggested that few ESA‐listed species are likely to be killed by a commercial‐scale tidal turbine array. We applied scenarios to a food web model of Puget Sound to explore the effects of tidal power and climate change on ESA‐listed species using more quantitative analytical techniques. To simulate development of tidal power, we applied results of the blade strike model. To simulate environmental changes over the next 50 years, we applied scenarios of change in primary production, plankton community structure, dissolved oxygen, ocean acidification, and freshwater flooding events. No effects of tidal power development on ESA‐listed species were detected from the food web model output, but the effects of climate change on them and other members of the food web were large. Our analyses exemplify how natural resource managers might assess environmental effects of marine technologies in ways that explicitly incorporate climate change and consider multiple ESA‐listed species in the context of their ecological community. Estimación de los Efectos de Proyectos de Energía de las Mareas y el Cambio Climático sobre Especies Marinas Amenazadas y en Peligro y su Red Alimentaria     

Use of Community‐Composition Data to Predict the Fecundity and Abundance of Species

Abstract: Species distribution models are critical tools for the prediction of invasive species spread and conservation of biodiversity. The majority of species distribution models have been built with environmental data. Community ecology theory suggests that species co‐occurrence data could also be used to predict current and potential distributions of species. Species assemblages are the products of biotic and environmental constraints on the distribution of individual species and as a result may contain valuable information for niche modeling. We compared the predictive ability of distribution models of annual grassland plants derived from either environmental or community‐composition data. Composition‐based models were built with the presence or absence of species at a site as predictors of site quality, whereas environment‐based models were built with soil chemistry, moisture content, above‐ground biomass, and solar radiation as predictors. The reproductive output of experimentally seeded individuals of 4 species and the abundance of 100 species were used to evaluate the resulting models. Community‐composition data were the best predictors of both the site‐specific reproductive output of sown individuals and the site‐specific abundance of existing populations. Successful community‐based models were robust to omission of data on the occurrence of rare species, which suggests that even very basic survey data on the occurrence of common species may be adequate for generating such models. Our results highlight the need for increased public availability of ecological survey data to facilitate community‐based modeling at scales relevant to conservation.     

Intraspecific Chromosome Number Variation: a Neglected Threat to the Conservation of Rare Plants

Abstract: The effectiveness of rare plant conservation will increase when life history, demographic, and genetic data are considered simultaneously. Inbreeding depression is a widely recognized genetic concern in rare plant conservation, and the mixing of genetically diverse populations in restoration efforts is a common remedy. Nevertheless, if populations with unrecognized intraspecific chromosome variation are crossed, progeny fitness losses will range from partial to complete sterility, and reintroductions and population augmentation of rare plants may fail. To assess the current state of cytological knowledge of threatened and endangered plants in the continental United States, we searched available resources for chromosome counts. We also reviewed recovery plans to discern whether recovery criteria potentially place listed species at risk by requiring reintroductions or population augmentation in the absence of cytological information. Over half the plants lacked a chromosome count, and when a taxon did have a count it generally originated from a sampling intensity too limited to detect intraspecific chromosome variation. Despite limited past cytological sampling, we found 11 plants with documented intraspecific cytological variation, while 8 others were ambiguous for intraspecific chromosome variation. Nevertheless, only one recovery plan addressed the chromosome differences. Inadequate within‐species cytological characterization, incomplete sampling among listed taxa, and the prevalence of interspecific and intraspecific chromosome variation in listed genera, suggests that other rare plants are likely to have intraspecific chromosome variation. Nearly 90% of all recovery plans called for reintroductions or population augmentation as part of recovery criteria despite the dearth of cytological knowledge. We recommend screening rare plants for intraspecific chromosome variation before reintroductions or population augmentation projects are undertaken to safeguard against inadvertent mixtures of incompatible cytotypes.     

Potential Effects of Ongoing and Proposed Hydropower Development on Terrestrial Biological Diversity in the Indian Himalaya

Indian Himalayan basins are earmarked for widespread dam building, but aggregate effects of these dams on terrestrial ecosystems are unknown. We mapped distribution of 292 dams (under construction and proposed) and projected effects of these dams on terrestrial ecosystems under different scenarios of land‐cover loss. We analyzed land‐cover data of the Himalayan valleys, where dams are located. We estimated dam density on fifth‐ through seventh‐order rivers and compared these estimates with current global figures. We used a species–area relation model (SAR) to predict short‐ and long‐term species extinctions driven by deforestation. We used scatter plots and correlation studies to analyze distribution patterns of species and dams and to reveal potential overlap between species‐rich areas and dam sites. We investigated effects of disturbance on community structure of undisturbed forests. Nearly 90% of Indian Himalayan valleys would be affected by dam building and 27% of these dams would affect dense forests. Our model projected that 54,117 ha of forests would be submerged and 114,361 ha would be damaged by dam‐related activities. A dam density of 0.3247/1000 km² would be nearly 62 times greater than current average global figures; the average of 1 dam for every 32 km of river channel would be 1.5 times higher than figures reported for U.S. rivers. Our results show that most dams would be located in species‐rich areas of the Himalaya. The SAR model projected that by 2025, deforestation due to dam building would likely result in extinction of 22 angiosperm and 7 vertebrate taxa. Disturbance due to dam building would likely reduce tree species richness by 35%, tree density by 42%, and tree basal cover by 30% in dense forests. These results, combined with relatively weak national environmental impact assessment and implementation, point toward significant loss of species if all proposed dams in the Indian Himalaya are constructed. Efectos Potenciales del Desarrollo Hidroeléctrico Actual y Propuesto sobre la Diversidad Biológica Terrestre en el Himalaya Hindú     

Threatened Species and the Potential Loss of Phylogenetic Diversity: Conservation Scenarios Based on Estimated Extinction Probabilities and Phylogenetic Risk Analysis

Abstract: New species conservation strategies, including the EDGE of Existence (EDGE) program, have expanded threatened species assessments by integrating information about species' phylogenetic distinctiveness. Distinctiveness has been measured through simple scores that assign shared credit among species for evolutionary heritage represented by the deeper phylogenetic branches. A species with a high score combined with a high extinction probability receives high priority for conservation efforts. Simple hypothetical scenarios for phylogenetic trees and extinction probabilities demonstrate how such scoring approaches can provide inefficient priorities for conservation. An existing probabilistic framework derived from the phylogenetic diversity measure (PD) properly captures the idea of shared responsibility for the persistence of evolutionary history. It avoids static scores, takes into account the status of close relatives through their extinction probabilities, and allows for the necessary updating of priorities in light of changes in species threat status. A hypothetical phylogenetic tree illustrates how changes in extinction probabilities of one or more species translate into changes in expected PD. The probabilistic PD framework provided a range of strategies that moved beyond expected PD to better consider worst‐case PD losses. In another example, risk aversion gave higher priority to a conservation program that provided a smaller, but less risky, gain in expected PD. The EDGE program could continue to promote a list of top species conservation priorities through application of probabilistic PD and simple estimates of current extinction probability. The list might be a dynamic one, with all the priority scores updated as extinction probabilities change. Results of recent studies suggest that estimation of extinction probabilities derived from the red list criteria linked to changes in species range sizes may provide estimated probabilities for many different species. Probabilistic PD provides a framework for single‐species assessment that is well‐integrated with a broader measurement of impacts on PD owing to climate change and other factors.