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.     

What Exactly Is an Endangered Species? An Analysis of the U.S. Endangered Species List: 1985–1991

Critics of the Endangered Species Act have asserted that is protects an inordinate number of subspecies and populations, in addition to full species, and that the scientific rationale for listing decisions is absent or weak. We reviewed all U.S. plants and animals proposed for listing or added to the endangered species list from 1985 through 1991 to determine the relative proportion of species, subspecies, and populations, and their rarity at time of listing. Approximately 80% of the taxa added to the list were full species, 18% were subspecies, and 2% were distinct populations segments of more widespread vertebrate species. The proportion of subspecies and populations was considerably higher among birds and mammals than among other groups. The median populations size at time of listing for vertebrate animals was 1075 individuals; for invertebrate animals it was 999. The median population size of a plant at time of listing was less than 120 individuals. Earlier listing of declining species could significantly improve the likelihood of successful recovery, and it would provide land managers and private citizens with more options for protecting vanishing plants and animals at less social or economic cost.     

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.     

Avian Conservation under the Endangered Species Act: Expenditures versus Recovery Priorities

Abstract: Budget constraints require the U.S. Fish and Wildlife Service to prioritize species for recovery spending. Each listed species is ranked according to the degree of threat it faces, its recovery potential, and its taxonomic distinctness. We analyzed state and federal government expenditures for recovery of threatened and endangered birds ( n = 85 species) from 1992 to 1995 to determine if the priority system was being followed. Although recovery spending correlated with priority rank, priority rank explained <5% of the variation in spending. A small number of the same moderately ranked species dominated expenditures each year (41–79% of total annual budgets). Species with wide distributions, high recovery potential, and captive breeding programs received the most funding, and more funding than their priority ranks dictated. Island species received significantly less funding than expected based on priority rank. Twelve species, 10 of which resided on islands, received <$5000 at least once from 1992 to 1995. Recovery spending was unrelated to degree of threat, taxonomic distinctness, and migratory status. There also was no relationship between land-purchase expenditures and priority ranks. To improve the relationship between recovery spending on threatened and endangered birds and their priority rank, significant changes need to be made within the private sector ( less litigation and special-interest lobbying  ), U.S. Congress (increased budget and reduced earmarking  ), and the U.S. Fish and Wildlife Service (restructuring of regional offices and increased accountability).     

Resolving Critical Habitat Designation Failures: Reconciling Law, Policy, and Biology

Abstract:  The U.S. Endangered Species Act (ESA) requires designation of critical habitat concurrent with species listing. The U.S. Fish and Wildlife Service often has not designated critical habitat, based on the legal exceptions in the ESA of "not prudent" or "not determinable." This lack of habitat designation has led to numerous lawsuits and court orders to designate critical habitat for listed species. Court-mediated implementation of critical habitat is costly and delays listing for at-risk species. Legal, policy, judicial, and biological issues all contribute to the current inability of the law as enforced to lead to timely and cost-effective critical habitat designation. Although increased appropriations and delaying critical habitat designation until recovery planning have been proposed as solutions, we find that it will be essential to change the critical-habitat guidelines to a decision-analysis framework to make critical habitat scientifically and legally workable as a conservation tool.     

A Critique of the Recovery of Greenback Cutthroat Trout

Abstract: There are no examples of recovery of fish listed under the U.S. Endangered Species Act, but the number of federally threatened greenback cutthroat trout (  Oncorhynchus clarki stomias ) populations is approaching the delisting goal. We evaluated recovery of this subspecies in light of developing theory in conservation biology and with regard to recovery of other salmonids in the inland western United States. Four of the five criteria used to define populations that would count toward delisting appeared to underestimate the risk of extinction of those populations. Typically, recovery goals for numbers of greenback cutthroat trout populations were less stringent than those for other inland salmonids petitioned for listing or listed as threatened under the Endangered Species Act and were comparable to those for a federally endangered species. Before delisting is considered, we propose that historical populations be replicated in additional waters to protect genetic diversity and that existing populations be enlarged to reduce their vulnerability to demographic variation, to increase their access to refugia, and to permit reestablishment of mobile life histories. Existing stocks should also be evaluated to determine whether they represent distinct population segments.     

The Capacity of the National Wildlife Refuge System to Conserve Threatened and Endangered Animal Species in the United States

Abstract:  The U.S. Fish and Wildlife Service manages the 38-million-ha National Wildlife Refuge System, which is devoted primarily to wildlife conservation. I examined the capacity of the refuge system to conserve federally listed threatened and endangered animal species. Population viability data for a random sample of these species were analyzed and extrapolated. Three levels of population viability were distinguished: outbreeding, demographic, and evolutionary. One hundred eighty-six of the 514 federally listed animal species reside in whole or in part on the refuge system. Of these 186 species, approximately 81, 101, and 107 are supported by the system at evolutionary, demographic, and outbreeding viability levels, respectively. These figures correspond to 16%, 19%, and 21% of the 514 federally listed animal species, respectively. Various federal policies and programs facilitate the expansion of the refuge system, but other federal policies and programs facilitate economic growth, which tends to require the conversion of habitats faster than it provides for habitat conservation. Therefore the long-run effectiveness, extent, and endurance of the refuge system will depend largely on macroeconomic policy context.     

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.     

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.     

The Biopolitics of the Mt. Graham Red Squirrel (Tamiasciuris hudsonicus grahamensis)

This essay presents (1) a short status summary on the population biology of the Mt. Graham red squirrel on the Pinaleño Mountains, Arizona; (2) a biopolitical history of the controversy surrounding the Mt. Graham red squirrel, the Endangered Species Act (ESA), and the astronomical consortium that has constructed two telescopes within the squirrel's critical habitat; and (3) a discussion of specific biopolitical issues related to the squirrel's taxonomy, minimal viable habitat, critical habitat, population viability analysis, risk management, and Congressional actions to by-pass its own laws. The biopolitical history shows how specific administrative actions within the U.S. Forest Service and the U.S. Fish and Wildlife Service and special interest politics by the Arizona Congressional delegation and the University of Arizona prevented an accurate assessment of the status of the Mt. Graham red squirrel and implementation of alternatives to insure its survival and recovery. Conservation biology can influence management decisions when not overridden by special-favor politics. To improve the influence of the science of conservation biology, I recommend that the ESA language protecting isolated populations (Section 3) remain intact and that the ESA make a legal distinction (Section 4) between minimal viable habitat and critical habitat. To improve the application of the ESA, I recommend that Congress require committee hearings before it can exempt a project from federal environmental laws; that fraudulent Biological Opinions automatically trigger a complete review of long-term viability; that conservation biologists prepare a handbook for the Fish and Wildlife Service on risk assessment techniques; that all data and analyses within the Biological Opinion include a ranking by their statistical and biological certainty as well as a worst-case scenario; and that each Biological Opinion be certified as risk averse.     

Importance of Well-Designed Monitoring Programs for the Conservation of Endangered Species: Case Study of the Snail Kite

Abstract:  Monitoring natural populations is often a necessary step to establish the conservation status of species and to help improve management decisions. Nevertheless, many monitoring programs do not effectively address primary sources of variability in monitoring data, which ultimately may limit the utility of monitoring in identifying declines and improving management. To illustrate the importance of taking into account detectability and spatial variation, we used a recently proposed estimator of abundance (superpopulation estimator) to estimate population size of and number of young produced by the Snail Kite ( Rostrhamus sociabilis plumbeus ) in Florida. During the last decade, primary recovery targets set by the U.S. Fish and Wildlife Service for the Snail Kite that were based on deficient monitoring programs (i.e., uncorrected counts) were close to being met (by simply increasing search effort during count surveys). During that same period, the Snail Kite population declined dramatically (by 55% from 1997 to 2005) and the number of young decreased by 70% between 1992–1998 and 1999–2005. Our results provide a strong practical case in favor of the argument that investing a sufficient amount of time and resources into designing and implementing monitoring programs that carefully address detectability and spatial variation is critical for the conservation of endangered species.     

The Importance of Analysis Method for Breeding Bird Survey Population Trend Estimates

Population trends from the Breeding Bird Survey are widely used to focus conservation efforts on species thought to be in decline and to test preliminary hypotheses regarding the causes of these declines. A number of statistical methods have been used to estimate population trends, but there is no consensus as to which is the most reliable. We quantified differences in trend estimates or different analysis methods applied to the same subset of Breeding Bird Survey data. We estimated trends for 115 species in British Columbia using three analysis methods: U.S. National Biological Service route regression, Canadian Wildlife Service route regression, and nonparametric rank-trends analysis. Overall, the number of species estimated to be declining was similar among the three methods, but the number of statistically significant declines was not similar (15, 8, and 29 respectively). In addition, many differences existed among methods in the trend estimates assigned to individual species. Comparing the two route regression methods, Canadian Wildlife Service estimates had a greater absolute magnitude on average than those of the U.S. National Biological Service method. U.S. National Biological Service estimates were on average more positive than the Canadian Wildlife Service estimates when the respective agency's data selection criteria were applied separately. These results imply that our ability to detect population declines and to prioritize species of conservation concern depend strongly upon the analysis method used. This highlights the need for further research to determine how best to accurately estimate trends from the data. We suggest a method for evaluating the performance of the analysis methods by using simulated Breeding Bird Survey data.     

Molecular Taxonomy and the Conservation of the Red Wolf and Other Endangered Carnivores

Recent publications have reaffirmed that the red wolf ( Canis rufus ) is a hybrid of the coyote and the gray wolf. Besides the implications these results will likely have for future conservation efforts and allotment of resources through the Endangered Species Act for recovery of the red wolf, it is likely that broader consequences will be felt throughout the conservation community as species come under the scrutiny of a more powerful means of taxonomic identification. As molecular technology is refined in its ability to resolve taxonomic histories and uncertainties, it is likely that hybridization event(s) will be recognized in more species. This may be of particular importance for large carnivores, whose small population sizes make them susceptible to hybridization episodes with closely related, sympatric species. Because of negative perceptions, powerful antipredator advocates, conservation and resource constraints, and an enigmatic hybrid policy within the Endangered Species Act, how red-wolf taxonomy is decided by the U.S. Fish and Wildlife Service may affect the future of large carnivores in general.     

A Framework for Developing Objective and Measurable Recovery Criteria for Threatened and Endangered Species

For species listed under the U.S. Endangered Species Act (ESA), the U.S. Fish and Wildlife Service and National Marine Fisheries Service are tasked with writing recovery plans that include “objective, measurable criteria” that define when a species is no longer at risk of extinction, but neither the act itself nor agency guidelines provide an explicit definition of objective, measurable criteria. Past reviews of recovery plans, including one published in 2012, show that many criteria lack quantitative metrics with clear biological rationale and are not meeting the measureable and objective mandate. I reviewed how objective, measureable criteria have been defined implicitly and explicitly in peer‐reviewed literature, the ESA, other U.S. statutes, and legal decisions. Based on a synthesis of these sources, I propose the following 6 standards be used as minimum requirements for objective, measurable criteria: contain a quantitative threshold with calculable units, stipulate a timeframe over which they must be met, explicitly define the spatial extent or population to which they apply, specify a sampling procedure that includes sample size, specify a statistical significance level, and include justification by providing scientific evidence that the criteria define a species whose extinction risk has been reduced to the desired level. To meet these 6 standards, I suggest that recovery plans be explicitly guided by and organized around a population viability modeling framework even if data or agency resources are too limited to complete a viability model. When data and resources are available, recovery criteria can be developed from the population viability model results, but when data and resources are insufficient for model implementation, extinction risk thresholds can be used as criteria. A recovery‐planning approach centered on viability modeling will also yield appropriately focused data‐acquisition and monitoring plans and will facilitate a seamless transition from recovery planning to delisting. Un Marco de Referencia para Desarrollar Criterios de Recuperación Objetivos y Medibles para Especies Amenazadas y en Peligro     

Predicting Recovery Criteria for Threatened and Endangered Plant Species on the Basis of Past Abundances and Biological Traits

Recovery plans for species listed under the U.S. Endangered Species Act are required to specify measurable criteria that can be used to determine when the species can be delisted. For the 642 listed endangered and threatened plant species that have recovery plans, we applied recursive partitioning methods to test whether the number of individuals or populations required for delisting can be predicted on the basis of distributional and biological traits, previous abundance at multiple time steps, or a combination of traits and previous abundances. We also tested listing status (threatened or endangered) and the year the recovery plan was written as predictors of recovery criteria. We analyzed separately recovery criteria that were stated as number of populations and as number of individuals (population‐based and individual‐based criteria, respectively). Previous abundances alone were relatively good predictors of population‐based recovery criteria. Fewer populations, but a greater proportion of historically known populations, were required to delist species that had few populations at listing compared with species that had more populations at listing. Previous abundances were also good predictors of individual‐based delisting criteria when models included both abundances and traits. The physiographic division in which the species occur was also a good predictor of individual‐based criteria. Our results suggest managers are relying on previous abundances and patterns of decline as guidelines for setting recovery criteria. This may be justifiable in that previous abundances inform managers of the effects of both intrinsic traits and extrinsic threats that interact and determine extinction risk. Predicción de Criterios de Recuperación para Especies de Plantas en Peligro y Amenazadas con Base en Abundancias Pasadas y Atributos Biológicos     

Genetic Data and the Listing of Species Under the U.S. Endangered Species Act

Abstract:  Genetic information is becoming an influential factor in determining whether species, subspecies, and distinct population segments qualify for protection under the U.S. Endangered Species Act. Nevertheless, there are currently no standards or guidelines that define how genetic information should be used by the federal agencies that administer the act. I examined listing decisions made over a 10-year period (February 1996–February 2006) that relied on genetic information. There was wide variation in the genetic data used to inform listing decisions in terms of which genomes (mitochondrial vs. nuclear) were sampled and the number of markers (or genetic techniques) and loci evaluated. In general, whether the federal agencies identified genetic distinctions between putative taxonomic units or populations depended on the type and amount of genetic data. Studies that relied on multiple genetic markers were more likely to detect distinctions, and those organisms were more likely to receive protection than studies that relied on a single genetic marker. Although the results may, in part, reflect the corresponding availability of genetic techniques over the given time frame, the variable use of genetic information for listing decisions has the potential to misguide conservation actions. Future management policy would benefit from guidelines for the critical evaluation of genetic information to list or delist organisms under the Endangered Species Act.     

Molecular Variation and Evolutionarily Significant Units in the Endangered Gila Topminnow

Determining evolutionarily significant units in endangered species is one of the most significant challenges facing conservation biology. Often genetic information has been used as the primary basis of recommendations for evolutionarily significant units, but these data should be evaluated carefully and used in conjunction with other information. The endangered Gila topminnow ( Poeciliopsis. o. occidentalis ) has been the subject of extensive conservation biology research and genetic investigation. We extended these data to highly variable genetic markers, examined variation in microsatellite loci, and compared it with previous measures of genetic diversity for the Gila topminnow from the four watersheds in Arizona in which they are still naturally extant. Fish from Monkey Spring were the most highly differentiated from the other populations. Overall, the amounts and patterns of genetic variation were consistent with known historical and physical differences among sites. The four watersheds are highly physically isolated from one another and differ in a number of important factors in their physical habitat, biota, and the life-history of the topminnows. Based on these geographic patterns and the genetic results, we recommend that the four watersheds all be managed and conserved separately.     

Status of Species Conservation Banking in the United States

Abstract:  Receiving financial gains for protecting habitat may be necessary to proactively protect endangered species in the United States. Species conservation banking, the creation and trading of "credits" that represent biodiversity values on private land, is nearly a decade old. We detail the biological, financial, and political experience of conservation banking in the United States. We contacted agencies, nongovernmental organizations, and bank owners and compiled comprehensive accounts of the experiences of current banks. There are 76 properties identified as conservation banks in the United States, but only 35 of these are established under a conservation banking agreement approved by the U.S. Fish and Wildlife Service (USFWS). The 35 official conservation banks cumulatively cover 15,987 ha and shelter a range of biodiversity, including more than 22 species listed under the U.S. Endangered Species Act. Financial motives drove the establishment of 91% of conservation banks, and the majority of for-profit banks are breaking even or making money. With credit prices ranging from $3,000 to $125,000/0.41 ha (1 acre), banking agreements offer financial incentives that compete with development and provide a business-based argument for conserving habitat. Although the bureaucracy of establishing an agreement with the USFWS was burdensome, 63% of bank owners reported they would set up another agreement given the appropriate opportunity. Increasing information sharing, decreasing the time to establish agreements (currently averaging 2.18 years), and reducing bureaucratic challenges can further increase the amount of private property voluntarily committed to banking. Although many ecological uncertainties remain, conservation banking offers at least a partial solution to the conservation versus development conflict over biodiversity.     

Developing Classification Criteria under the U.S. Endangered Species Act: Bowhead Whales as a Case Study

Abstract: Under the U.S. Endangered Species Act, a species is classified as endangered, threatened, or recovered based on the extent to which its survival is affected by one or more of five subjective factors. A key criticism of the act is that it makes no reference to quantitative or even qualitative parameters of what constitutes "danger of extinction." Without objective standards to guide decisionmakers, classification decisions fall prey to political and social influences. We recommend the development of species-specific, status-determining criteria as a means to rationalize and expedite the listing process and reclassification decisions, independent of the requirement for delisting criteria in recovery plans. Such criteria should (1) clearly define levels of vulnerability, (2) identify gaps in information on life-history parameters, and (3) address uncertainty in existing data. As a case study, we developed preliminary criteria for bowhead whales (    Balaena mysticetus ). Thresholds for endangered and threatened status were based on World Conservation Union ( IUCN) Red List criteria and population viability analyses. Our analysis indicates that particular attention must be focused on population structure within the species to appropriately classify the degree to which one or more components of a species are vulnerable to extinction. A similar approach could be used in the classification of other species. According to our application of the IUCN criteria and those developed for similar species by Gerber and DeMaster (1999) , the Bering Sea population of bowhead whales should be delisted, whereas the other four populations of bowheads should continue to be considered endangered.     

Robust population management under uncertainty for structured population models.

Structured population models are increasingly used in decision making, but typically have many entries that are unknown or highly uncertain. We present an approach for the systematic analysis of the effect of uncertainties on long-term population growth or decay. Many decisions for threatened and endangered species are made with poor or no information. We can still make decisions under these circumstances in a manner that is highly defensible, even without making assumptions about the distribution of uncertainty, or limiting ourselves to discussions of single, infinitesimally small changes in the parameters. Suppose that the model (determined by the data) for the population in question predicts long-term growth. Our goal is to determine how uncertain the data can be before the model loses this property. Some uncertainties will maintain long-term growth, and some will lead to long-term decay. The uncertainties are typically structured, and can be described by several parameters. We show how to determine which parameters maintain long-term growth. We illustrate the advantages of the method by applying it to a Peregrine Falcon population. The U.S. Fish and Wildlife Service recently decided to allow minimal harvesting of Peregrine Falcons after their recent removal from the Endangered Species List. Based on published demographic rates, we find that an asymptotic growth rate lambda > 1 is guaranteed with 5% harvest rate up to 3% error in adult survival if no two-year-olds breed, and up to 11% error if all two-year-olds breed. If a population growth rate of 3% or greater is desired, the acceptable error in adult survival decreases to between 1% and 6% depending of the proportion of two-year-olds that breed. These results clearly show the interactions between uncertainties in different parameters, and suggest that a harvest decision at this stage may be premature without solid data on adult survival and the frequency of breeding by young adults.