Taxonomic Considerations in Listing Subspecies Under the U.S. Endangered Species Act

Abstract:  The U.S. Endangered Species Act (ESA) allows listing of subspecies and other groupings below the rank of species. This provides the U.S. Fish and Wildlife Service and the National Marine Fisheries Service with a means to target the most critical unit in need of conservation. Although roughly one-quarter of listed taxa are subspecies, these management agencies are hindered by uncertainties about taxonomic standards during listing or delisting activities. In a review of taxonomic publications and societies, we found few subspecies lists and none that stated standardized criteria for determining subspecific taxa. Lack of criteria is attributed to a centuries-old debate over species and subspecies concepts. Nevertheless, the critical need to resolve this debate for ESA listings led us to propose that minimal biological criteria to define disjunct subspecies (legally or taxonomically) should include the discreteness and significance criteria of distinct population segments (as defined under the ESA). Our subspecies criteria are in stark contrast to that proposed by supporters of the phylogenetic species concept and provide a clear distinction between species and subspecies. Efforts to eliminate or reduce ambiguity associated with subspecies-level classifications will assist with ESA listing decisions. Thus, we urge professional taxonomic societies to publish and periodically update peer-reviewed species and subspecies lists. This effort must be paralleled throughout the world for efficient taxonomic conservation to take place.     

Designatable Units for Status Assessment of Endangered Species

Abstract:  Species status assessment and the conservation of biological diversity may require defining units below the species level to portray probabilities of extinction accurately and to help set priorities for conservation efforts. What those units should be has been debated in the scientific literature largely in terms of evolutionarily significant units (ESUs), but this discourse has had little impact on government policy with regard to status assessment. As with species concepts, the variously proposed ESU concepts have not been resolvable into a single approach. The need for a practicable procedure to identify infraspecific entities for status assignment is the motivation behind employing designatable units (DUs). In aid of a policy to prevent elements of biodiversity from becoming extinct or extirpated, DUs are determined during the process of resolving a species' conservation status according to broadly applicable guidelines. The procedure asks whether putative DUs are distinguishable based on a reliably established taxonomy or a well-corroborated phylogeny, compelling evidence of genetic distinction, range disjunction, and/or biogeographic distinction as long as extinction probabilities also differ. The language of the DU approach avoids wording that implies value judgments concerning evolutionary importance or significance. Because species conservation status assessment is not science but, rather, the use of science to further policy, DUs contribute to a precautionary approach to listing whereby status may be assessed even though knowledge of systematic relationships below the species level may be lacking or unresolved. The pragmatic approach of using DUs has been adopted by the Committee on the Status of Endangered Wildlife in Canada for status assessment of species under the Canadian Species at Risk Act.     

Accounting for Uncertainty in Making Species Protection Decisions

Abstract:  Uncertainty gives rise to two decision errors in implementing the U.S. Endangered Species Act: listing species that are not in danger of extinction and delisting species that are in danger of extinction. I evaluated four methods (minimum standard, precautionary principle, minimax regret criterion, adaptive management) for deciding whether to list or delist a species when there is uncertainty about how those decisions are likely to influence survival of the species. A safe minimum standard criterion preserves some minimum amount or safe standard (population) of a species unless maintaining that amount generates unacceptable social cost. The precautionary principle favors not delisting a species when there is insufficient evidence on the efficacy of state management plans for protecting them. A minimax regret criterion selects the delisting decision that minimizes the maximum loss likely to occur under alternative ecosystem states. When the cost of making a correct decision is less than the cost of making an incorrect decision, the minimax regret criteria indicates that delisting is the optimal decision. Active adaptive management employs statistically valid experiments to test hypotheses about the likely impacts of delisting decisions. Safe minimum standard and minimax regret criterion are not compatible with the U.S. Endangered Species Act. The precautionary principle comes closest to describing how federal agencies make delisting decisions. Active adaptive management is scientifically superior to the other methods but is costly and time consuming and may not be compatible with the U.S. National Environmental Policy Act.     

Interacting Effects of Landownership, Land Use, and Endangered Species on Conservation of Southwestern U.S. Rangelands

Abstract:  The contemporary southwestern United States is characterized by fire-adapted ecosystems; large numbers of federally listed threatened and endangered species; a patchwork of federal, state, and private landownership; and a long history of livestock grazing as the predominant land use. I compared eight sites in southern Arizona and New Mexico to assess the interacting effects of these characteristics on conservation practices and outcomes. There was widespread interest and private-sector leadership in restoring fire to southwestern rangelands, and there is a shortage of predictive scientific knowledge about the effects of fire and livestock grazing on threatened and endangered species. It was easier to restore fire to lands that were either privately owned or not grazed, in part because of obstacles created by threatened and endangered species on grazed public lands. Collaborative management facilitated conservation practices and outcomes, and periodic removal of livestock may be necessary for conservation, but permanent livestock exclusion may be counterproductive because of interactions with land-use and landownership patterns.     

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.     

Hybridization,agency discretion,and implementation of the U.S. Endangered Species Act

The U.S. Endangered Species Act (ESA) requires that the “best available scientific and commercial data” be used to protect imperiled species from extinction and preserve biodiversity. However, it does not provide specific guidance on how to apply this mandate. Scientific data can be uncertain and controversial, particularly regarding species delineation and hybridization issues. The U.S. Fish and Wildlife Service (FWS) had an evolving hybrid policy to guide protection decisions for individuals of hybrid origin. Currently, this policy is in limbo because it resulted in several controversial conservation decisions in the past. Biologists from FWS must interpret and apply the best available science to their recommendations and likely use considerable discretion in making recommendations for what species to list, how to define those species, and how to recover them. We used semistructured interviews to collect data on FWS biologists’ use of discretion to make recommendations for listed species with hybridization issues. These biologists had a large amount of discretion to determine the best available science and how to interpret it but generally deferred to the scientific consensus on the taxonomic status of an organism. Respondents viewed hybridization primarily as a problem in the context of the ESA, although biologists who had experience with hybridization issues were more likely to describe it in more nuanced terms. Many interviewees expressed a desire to continue the current case‐by‐case approach for handling hybridization issues, but some wanted more guidance on procedures (i.e., a “flexible” hybrid policy). Field‐level information can provide critical insight into which policies are working (or not working) and why. The FWS biologists’ we interviewed had a high level of discretion, which greatly influenced ESA implementation, particularly in the context of hybridization.     

Geography and Recovery under the U.S. Endangered Species Act

Abstract: The U.S. Endangered Species Act (ESA) defines an endangered species as one “at risk of extinction throughout all or a significant portion of its range.” The prevailing interpretation of this phrase, which focuses exclusively on the overall viability of listed species without regard to their geographic distribution, has led to development of listing and recovery criteria with fundamental conceptual, legal, and practical shortcomings. The ESA's concept of endangerment is broader than the biological concept of extinction risk in that the “esthetic, ecological, educational, historical, recreational, and scientific” values provided by species are not necessarily furthered by a species mere existence, but rather by a species presence across much of its former range. The concept of “significant portion of range” thus implies an additional geographic component to recovery that may enhance viability, but also offers independent benefits that Congress intended the act to achieve. Although the ESA differs from other major endangered‐species protection laws because it acknowledges the distinct contribution of geography to recovery, it resembles the “representation, resiliency, and redundancy” conservation‐planning framework commonly referenced in recovery plans. To address representation, listing and recovery standards should consider not only what proportion of its former range a species inhabits, but the types of habitats a species occupies and the ecological role it plays there. Recovery planning for formerly widely distributed species (e.g., the gray wolf [Canis lupus]) exemplifies how the geographic component implicit in the ESA's definition of endangerment should be considered in determining recovery goals through identification of ecologically significant types or niche variation within the extent of listed species, subspecies, or “distinct population segments.” By linking listing and recovery standards to niche and ecosystem concepts, the concept of ecologically significant type offers a scientific framework that promotes more coherent dialogue concerning the societal decisions surrounding recovery of endangered species.     

Species Listing under Canada's Species at Risk Act

Abstract: In a preliminary analysis of listing decisions under Canada's Species at Risk Act (SARA), Mooers et al. (2007) demonstrated an apparent bias against marine and northern species. As a follow‐up, we expanded the set of potential explanatory variables, including information on jurisdictional and administrative elements of the listing process, and considered an additional 16 species recommended for listing by SARA's scientific advisory committee as of 15 August 2006. Logistic model selection based on Akaike differences suggested that species were less likely to be listed if they were harvested or had commercial or subsistence harvesting as an explicitly identified threat; had Department of Fisheries and Oceans (DFO) as a responsible authority (RA); were located in Canada's north generally, and especially in Nunavut; or were found mostly or entirely within Canada. Subsequent model validation with an independent set of 50 species for which a listing decision was handed down in December 2007 showed an overall misclassification rate of <0.10, indicating reasonable predictive power. In light of these results, we recommend that RAs under SARA adopt a two‐track listing approach to address problems of delays arising from extended consultations and the inconsistent use by the RAs of socioeconomic analysis; consider revising SARA so that socioeconomic analysis occurs during decisions about protecting species and their habitats rather than at the listing stage; and maintain an integrated database with information on species’ biology, threats, and agency actions to enable future evaluation of SARA's impact.     

Assessing the impact of the U.S. Endangered Species Act recovery planning guidelines on managing threats for listed species

The Endangered Species Act (ESA) of the United States was enacted in 1973 to prevent the extinction of species. Recovery plans, required by 1988 amendments to the ESA, play an important role in organizing these efforts to protect and recover species. To improve the use of science in the recovery planning process, the Society for Conservation Biology (SCB) commissioned an independent review of endangered species recovery planning in 1999. From these findings, the SCB made key recommendations for how management agencies could improve the recovery planning process, after which the U.S. Fish and Wildlife Service and the National Marine Fisheries Service redrafted their recovery planning guidelines. One important recommendation called for recovery plans to make threats a primary focus, including organizing and prioritizing recovery tasks for threat abatement. We sought to determine the extent to which results from the SCB study were incorporated into these new guidelines and whether the SCB recommendations regarding threats manifested in recovery plans written under the new guidelines. Recovery planning guidelines generally incorporated the SCB recommendations, including those for managing threats. However, although recent recovery plans have improved in their treatment of threats, many fail to adequately incorporate threat monitoring. This failure suggests that developing clear guidelines for monitoring should be an important priority in improving ESA recovery planning.     

Gray Whales and the Value of Monitoring Data in Implementing the U.S. Endangered Species Act

Abstract: Many scientists lament the absence of data for endangered species and argue that more funds should be spent acquiring basic information about population trends. Using 19 years of abundance estimates for the eastern North Pacific gray whale ( Eschrichtius robustus ), we sampled subsets of the original survey data to identify the number of years of data required to remove the population from the U.S. Endangered Species Act's (ESA) list of endangered and threatened wildlife. For any given duration of monitoring, we selected all possible combinations of consecutive counts. To incorporate variability in growth rates, we extracted a maximum likelihood estimator of growth rate and confidence interval about that growth rate on the assumption that the population changes can be approximated by a simple diffusion process with drift. We then applied a new approach to determine ESA status for each subset of survey data and found that a quantitative decision to delist is unambiguously supported by 11 years of data but is precariously uncertain with fewer than 10 years of data. The data needed to produce an unequivocal decision to delist gray whales cost the National Marine Fisheries Service an estimated U.S. $660,000, a surprisingly modest expense given the fact that delisting can greatly simplify regulatory constraints. This example highlights the value of population monitoring in administering the ESA and provides a compelling example of the utility of such information in identifying both imperiled and recovered species. The economic value of such data is that they provide the foundation for delisting, which could ultimately save much more money than the collection of the data would ever cost.     

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     

Testing Decision Rules for Categorizing Species’ Extinction Risk to Help Develop Quantitative Listing Criteria for the U.S. Endangered Species Act

Lack of guidance for interpreting the definitions of endangered and threatened in the U.S. Endangered Species Act (ESA) has resulted in case‐by‐case decision making leaving the process vulnerable to being considered arbitrary or capricious. Adopting quantitative decision rules would remedy this but requires the agency to specify the relative urgency concerning extinction events over time, cutoff risk values corresponding to different levels of protection, and the importance given to different types of listing errors. We tested the performance of 3 sets of decision rules that use alternative functions for weighting the relative urgency of future extinction events: a threshold rule set, which uses a decision rule of x% probability of extinction over y years; a concave rule set, where the relative importance of future extinction events declines exponentially over time; and a shoulder rule set that uses a sigmoid shape function, where relative importance declines slowly at first and then more rapidly. We obtained decision cutoffs by interviewing several biologists and then emulated the listing process with simulations that covered a range of extinction risks typical of ESA listing decisions. We evaluated performance of the decision rules under different data quantities and qualities on the basis of the relative importance of misclassification errors. Although there was little difference between the performance of alternative decision rules for correct listings, the distribution of misclassifications differed depending on the function used. Misclassifications for the threshold and concave listing criteria resulted in more overprotection errors, particularly as uncertainty increased, whereas errors for the shoulder listing criteria were more symmetrical. We developed and tested the framework for quantitative decision rules for listing species under the U.S. ESA. If policy values can be agreed on, use of this framework would improve the implementation of the ESA by increasing transparency and consistency. Evaluando Reglas de Decisión para Categorizar el Riesgo de Extinción de Especies con el Fin de Desarrollar de Criterios Cuantitativos de Alistamiento en el Acta de Especies en Peligro de los EE. UU.     

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     

Factors associated with preemptive conservation under the U.S. Endangered Species Act

In recent decades, there has been an increasing emphasis on proactive efforts to conserve species being considered for listing under the U.S. Endangered Species Act (ESA) before they are listed (i.e., preemptive conservation). These efforts, which depend on voluntary actions by public and private land managers across the species’ range, aim to conserve species while avoiding regulatory costs associated with ESA listing. We collected data for a set of social, economic, environmental, and institutional factors that we hypothesized would influence voluntary decisions to promote or inhibit preemptive conservation of species under consideration for ESA listing. We used logistic regression to estimate the association of these factors with preemptive conservation outcomes based on data for a set of species that entered the ESA listing process and were either officially listed (n = 314) or preemptively conserved (n = 73) from 1996 to 2018. Factors significantly associated with precluded listing due to preemptive conservation included high baseline conservation status, low proportion of private land across the species’ range, small total range size, exposure to specific types of threats, and species’ range extending over several states. These results highlight strategies that can help improve conservation outcomes, such as allocating resources for imperiled species earlier in the listing process, addressing specific threats, and expanding incentives and coordination mechanisms for conservation on private lands.     

The Normative Dimension and Legal Meaning of Endangered and Recovery in the U.S. Endangered Species Act

Abstract:  The ethical, legal, and social significance of the U.S. Endangered Species Act of 1973 (ESA) is widely appreciated. Much of the significance of the act arises from the legal definitions that the act provides for the terms threatened species and endangered species. The meanings of these terms are important because they give legal meaning to the concept of a recovered species. Unfortunately, the meanings of these terms are often misapprehended and rarely subjected to formal analysis. We analyzed the legal meaning of recovered species and illustrate key points with details from "recovery" efforts for the gray wolf ( Canis lupus ). We focused on interpreting the phrase "significant portion of its range," which is part of the legal definition of endangered species. We argue that recovery and endangerment entail a fundamentally normative dimension (i.e., specifying conditions of endangerment) and a fundamentally scientific dimension (i.e., determining whether a species meets the conditions of endangerment). Specifying conditions for endangerment is largely normative because it judges risks of extinction to be either acceptable or unacceptable. Like many other laws that specify what is unacceptable, the ESA largely specifies the conditions that constitute unacceptable extinction risk. The ESA specifies unacceptable risks of extinction by defining endangered species in terms of the portion of a species' range over which a species is "in danger of extinction." Our analysis indicated that (1) legal recovery entails much more than the scientific notion of population viability, (2) most efforts to recover endangered species are grossly inadequate, and (3) many unlisted species meet the legal definition of an endangered or threatened species.     

Climate Change,Marine Environments,and the U.S. Endangered Species Act

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, long‐term 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. El Cambio Climático, los Ecosistemas Marinos y el Acta Estadunidense de Especies en Peligro