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     

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.     

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     

Decision‐Making Triggers in Adaptive Management

We analyzed whether decision‐making triggers increase accountability of adaptive‐management plans. Triggers are prenegotiated commitments in an adaptive‐management plan that specify what actions are to be taken and when on the basis of information obtained from monitoring. Triggers improve certainty that particular actions will be taken by agencies in the future. We conducted an in‐depth, qualitative review of the political and legal contexts of adaptive management and its application by U.S. federal agencies. Agencies must satisfy the judiciary that adaptive‐management plans meet substantive legal standards and comply with the U.S. National Environmental Policy Act. We examined 3 cases in which triggers were used in adaptive‐management plans: salmon (Oncorhynchus spp.) in the Columbia River, oil and gas development by the Bureau of Land Management, and a habitat conservation plan under the U.S. Endangered Species Act. In all the cases, key aspects of adaptive management, including controls and preidentified feedback loops, were not incorporated in the plans. Monitoring and triggered mitigation actions were limited in their enforceability, which was contingent on several factors, including which laws applied in each case and the degree of specificity in how triggers were written into plans. Other controversial aspects of these plans revolved around who designed, conducted, interpreted, and funded monitoring programs. Additional contentious issues were the level of precaution associated with trigger mechanisms and the definition of ecological baselines used as points of comparison. Despite these challenges, triggers can be used to increase accountability, by predefining points at which an adaptive management plan will be revisited and reevaluated, and thus improve the application of adaptive management in its complicated political and legal context. Detonadores de la Toma de Decisiones en el Manejo Adaptativo     

Species‐level persistence probabilities for recovery and conservation status assessment

Recovery planning for species listed under the U.S. Endangered Species Act has been hampered by a lack of consistency and transparency, which can be improved by implementing a standardized approach for evaluating species status and developing measurable recovery criteria. However, managers lack an assessment method that integrates threat abatement and can be used when demographic data are limited. To help meet these needs, we demonstrated an approach for evaluating species status based on habitat configuration data. We applied 3 established persistence measures (patch occupancy, metapopulation capacity, and proportion of population lost) to compare 2 conservation strategies (critical habitat designated by the U.S. Fish and Wildlife Service and the Forest Service's Carbonate Habitat Management Strategy) and 2 threat scenarios (maximum limestone mining, removal of all habitat in areas with mining claims; minimum mining, removal of habitat only in areas with existing operations and high‐quality ore) against a baseline of existing habitat for 3 federally listed plant species. Protecting all area within the designated critical habitat maintained a similar level (83.9–99.9%) of species persistence as the baseline, whereas maximum mining greatly reduced persistence (0.51–38.4% maintained). The 3 persistence measures provided complementary insights reflecting different aspects of habitat availability (total area, number of patches, patch size, and connectivity). These measures can be used to link recovery criteria developed following the 3 R principles (representation, redundancy, and resilience) to the resulting improvements in species viability. By focusing on amount and distribution of habitat, our method provides a means of assessing the status of data‐poor species to inform decision making under the Endangered Species Act.     

Current practices in the identification of critical habitat for threatened species

The term critical habitat is used to describe the subset of habitat that is essential to the survival and recovery of species. Some countries legally require that critical habitat of listed threatened and endangered species be identified and protected. However, there is little evidence to suggest that the identification of critical habitat has had much impact on species recovery. We hypothesized that this may be due at least partly to a mismatch between the intent of critical habitat identification, which is to protect sufficient habitat for species persistence and recovery, and its practice. We used content analysis to systematically review critical habitat documents from the United States, Canada, and Australia. In particular, we identified the major trends in type of information used to identify critical habitat and in occupancy of habitat identified as critical. Information about population viability was used to identify critical habitat for only 1% of the species reviewed, and for most species, designated critical habitat did not include unoccupied habitat. Without reference to population viability, it is difficult to determine how much of a species’ occupied and unoccupied habitat will be required for persistence. We therefore conclude that the identification of critical habitat remains inconsistent with the goal of protecting sufficient habitat to support persistence and recovery of the species. Ensuring that critical habitat identification aligns more closely with its intent will improve the accuracy of the designations and may therefore help improve the benefits to species recovery when combined with adequate implementation and enforcement of legal protections.     

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.     

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     

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.     

Importance of Habitat Quality and Landscape Connectivity for the Persistence of Endangered Natterjack Toads

Abstract: The natterjack toad (Bufo calamita) is endangered in several parts of its distribution, including Belgium, where it occurs mainly in artificial habitats. We parameterized a general model for natterjack population viability analysis (PVA) and tested its sensitivity to changes in the values of basic parameters. Then we assessed the relative efficiency of various conservation measures in 2 situations: a small isolated population and a system of 4 populations connected by rare dispersal movements. We based the population viability analysis on a stage‐structured model of natterjack population dynamics. We parameterized the model in the RAMAS GIS platform with vital rates obtained from our own field experience and from published studies. Simulated natterjack populations were highly sensitive to habitat quality (particularly pond drying), to dispersal from surrounding local populations, and to a lesser extent to values of fecundity and survival of terrestrial stages. Population trajectories were nearly insensitive to initial abundances, carrying capacities, and the frequency of extreme climatic conditions. The simulations showed that in habitats with highly ephemeral ponds, where premetamorphosis mortality was high, natterjack populations nearly always had a very high extinction risk. We also illustrated how low dispersal rates (<1 dispersing individual/generation) efficiently rescued declining local populations. Such source‐sink dynamics demonstrate that the identification and management of source populations should be a high priority.     

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.     

Biodiversity Conservation and Indigenous Land Management in the Era of Self‐Determination

Abstract: Indigenous people inhabit approximately 85% of areas designated for biodiversity conservation worldwide. They also continue to struggle for recognition and preservation of cultural identities, lifestyles, and livelihoods—a struggle contingent on control and protection of traditional lands and associated natural resources (hereafter, self‐determination). Indigenous lands and the biodiversity they support are increasingly threatened because of human population growth and per capita consumption. Application of the Endangered Species Act (ESA) to tribal lands in the United States provides a rich example of the articulation between biodiversity conservation and indigenous peoples' struggle for self‐determination. We found a paradoxical relationship whereby tribal governments are simultaneously and contradictorily sovereign nations; yet their communities depend on the U.S. government for protection through the federal‐trust doctrine. The unique legal status of tribal lands, their importance for conserving federally protected species, and federal environmental regulations' failure to define applicability to tribal lands creates conflict between tribal sovereignty, self‐determination, and constitutional authority. We reviewed Secretarial Order 3206, the U.S. policy on “American Indian tribal rights, federal–tribal trust responsibilities, and the ESA,” and evaluated how it influences ESA implementation on tribal lands. We found improved biodiversity conservation and tribal self‐determination requires revision of the fiduciary relationship between the federal government and the tribes to establish clear, legal definitions regarding land rights, applicability of environmental laws, and financial responsibilities. Such actions will allow provision of adequate funding and training to tribal leaders and resource managers, government agency personnel responsible for biodiversity conservation and land management, and environmental policy makers. Increased capacity, cooperation, and knowledge transfer among tribes and conservationists will improve biodiversity conservation and indigenous self‐determination.     

Influence of Political Opposition and Compromise on Conservation Outcomes in the Tongass National Forest,Alaska

Abstract: To understand how a highly contentious policy process influenced a major conservation effort, I examined the origins, compromises, and outcomes of the Alaska National Interest Lands Conservation Act of 1980 (ANILCA) for the Tongass National Forest. Tongass wilderness designation was among the most controversial issues in the ANILCA debate, and it faced strong opposition from influential lawmakers, land managers, and Alaska residents. To investigate the influence of this opposition on Tongass conservation outcomes, I conducted a gap analysis of Tongass reserves and a policy analysis of the ANILCA debate and traced the influence of specific interests through the amendments, negotiations, and resulting compromises needed to enact ANILCA. Overall, I found that Tongass reserves comprise a broadly representative cross‐section of ecosystems and species habitats in southeastern Alaska. Redrawn reserve boundaries, industry subsidies, and special access regulations reflected compromises to minimize the impact of wilderness conservation on mining, timber, and local stakeholder interests, respectively. Fragmentation of the Admiralty Island National Monument—the most ecologically valuable and politically controversial reserve—resulted from compromises with Alaskan Native (indigenous peoples of Alaska) corporations and timber interests. Despite language to accommodate “reasonable access” to wilderness reserves, ongoing access limitations highlight the concerns of Alaska residents that opposed ANILCA several decades ago. More broadly, the Tongass case suggests that early and ambitious conservation action may offset strong political opposition; compromises needed to establish key reserves often exacerbate development impacts in unprotected areas; and efforts to minimize social conflicts are needed to safeguard the long‐term viability of conservation measures.