Genetic diversity and IUCN Red List status

The International Union for Conservation of Nature (IUCN) Red List is an important and widely used tool for conservation assessment. The IUCN uses information about a species’ range, population size, habitat quality and fragmentation levels, and trends in abundance to assess extinction risk. Genetic diversity is not considered, although it affects extinction risk. Declining populations are more strongly affected by genetic drift and higher rates of inbreeding, which can reduce the efficiency of selection, lead to fitness declines, and hinder species’ capacities to adapt to environmental change. Given the importance of conserving genetic diversity, attempts have been made to find relationships between red-list status and genetic diversity. Yet, there is still no consensus on whether genetic diversity is captured by the current IUCN Red List categories in a way that is informative for conservation. To assess the predictive power of correlations between genetic diversity and IUCN Red List status in vertebrates, we synthesized previous work and reanalyzed data sets based on 3 types of genetic data: mitochondrial DNA, microsatellites, and whole genomes. Consistent with previous work, species with higher extinction risk status tended to have lower genetic diversity for all marker types, but these relationships were weak and varied across taxa. Regardless of marker type, genetic diversity did not accurately identify threatened species for any taxonomic group. Our results indicate that red-list status is not a useful metric for informing species-specific decisions about the protection of genetic diversity and that genetic data cannot be used to identify threat status in the absence of demographic data. Thus, there is a need to develop and assess metrics specifically designed to assess genetic diversity and inform conservation policy, including policies recently adopted by the UN's Convention on Biological Diversity Kunming-Montreal Global Biodiversity Framework.     

Interspecific Patterns of Genetic Diversity in Birds: Correlations with Extinction Risk

Abstract:  Birds are frequently used as indicators of ecosystem health and are the most comprehensively studied class in the animal kingdom. Nevertheless, a comprehensive, interspecific assessment of the correlates of avian genetic diversity is lacking, even though indices of genetic diversity are of considerable interest in the conservation of threatened species. We used published data on variation at microsatellite loci from 194 bird species to examine correlates of diversity, particularly with respect to conservation status and population size. We found a significant decline in mean heterozygosity with increasing extinction risk, and showed, by excluding species whose heterozygosity values were calculated with heterospecific primers, that this relationship was not dependent on ascertainment bias. Results of subsequent regression analyses suggested that smaller population sizes of threatened species were largely responsible for this relationship. Thus, bird species at risk of extinction are relatively depauperate in terms of neutral genetic diversity, which is expected to make population recovery more difficult if it reflects adaptive genetic variation. Conservation policy will need to minimize further loss of diversity if the chances of saving threatened species are to be maximized.     

Limited contributions of released animals from zoos to North American conservation translocations

With the loss of biodiversity accelerating, conservation translocations such as reintroductions are becoming an increasingly common conservation tool. Conservation translocations must source individuals for release from either wild or captive-bred populations. We asked what proportion of North American conservation translocations rely on captive breeding and to what extent zoos and aquaria (hereafter zoos) fulfill captive breeding needs. We searched for mention of captive breeding and zoo involvement in all 1863 articles included in the North American Conservation Translocations database, which comprises journal articles and grey literature published before 2014 on conservation translocations in Canada, the United States, Mexico, the Caribbean, and Central America before 2014 as identified by a comprehensive literature review. Conservation translocations involved captive breeding for 162 (58%) of the 279 animal species translocated. Fifty-four zoos contributed animals for release. The 40 species of animals bred for release by zoos represented only 14% of all animal species for which conservation translocations were published and only 25% of all animal species that were bred for releases occurring in North America. Zoo contributions varied by taxon, ranging from zoo-bred animals released in 42% of amphibian conservation translocations to zero contributions for marine invertebrates. Proportional involvement of zoos in captive-breeding programs for release has increased from 1974 to 2014 (r = 0.325, p = 0.0313) as has the proportion of translocation-focused scientific papers coauthored by zoo professionals (from 0% in 1974 to 42% in 2013). Although zoos also contribute to conservation translocations through education, funding, and professional expertise, increasing the contribution of animals for release in responsible conservation translocation programs presents a future conservation need and opportunity. We especially encourage increased dialogue and planning between the zoo community, academic institutions, and governments to optimize the direct contribution zoos can make to wildlife conservation through conservation translocations.     

Regional IUCN Red Listing: the Process as Applied to Birds in the United Kingdom

Abstract:  The World Conservation Union (IUCN) has developed guidelines that enable the assessment of extinction risk at a regional scale. We used these guidelines to assess the extinction risk of birds in the United Kingdom for comparison with an existing assessment of conservation status. Sixty-four species were categorized as regionally threatened, of which 12 were critically endangered. The categorizations of the 223 species assessed agreed broadly with those from the existing U.K. system, which considers more than extinction risk, thus giving a more complete assessment of conservation status. There was, however, a tendency for the IUCN process to give higher risk status to edge-of-range species (some of which are relatively recent colonists considered of comparatively low conservation concern) and low status to those that have declined substantially but remain common (such as many farmland birds, the focus of considerable conservation effort in the United Kingdom). The final red list depended heavily on the subjective decisions made during the assessment process. An alternative interpretation of the guidelines could have resulted in as many as 19 or as few as 6 species being listed as critically endangered. We recommend the revision of the IUCN guidelines to reduce this subjectivity, in particular with respect to the effect of extralimital populations on the likelihood of regional extinction, and hence the potential for variation in the manner of application between regional red-list assessors. Preventing extinction does not have to be the principal driving force behind conservation action at a regional scale if the continuance of a species is safeguarded in other regions.     

Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep

Evidence of inbreeding depression is commonly detected from the fitness traits of animals, yet its effects on population growth rates of endangered species are rarely assessed. We examined whether inbreeding depression was affecting Sierra Nevada bighorn sheep (Ovis canadensis sierrae), a subspecies listed as endangered under the U.S. Endangered Species Act. Our objectives were to characterize genetic variation in this subspecies; test whether inbreeding depression affects bighorn sheep vital rates (adult survival and female fecundity); evaluate whether inbreeding depression may limit subspecies recovery; and examine the potential for genetic management to increase population growth rates. Genetic variation in 4 populations of Sierra Nevada bighorn sheep was among the lowest reported for any wild bighorn sheep population, and our results suggest that inbreeding depression has reduced adult female fecundity. Despite this population sizes and growth rates predicted from matrix-based projection models demonstrated that inbreeding depression would not substantially inhibit the recovery of Sierra Nevada bighorn sheep populations in the next approximately 8 bighorn sheep generations (48 years). Furthermore, simulations of genetic rescue within the subspecies did not suggest that such activities would appreciably increase population sizes or growth rates during the period we modeled (10 bighorn sheep generations, 60 years). Only simulations that augmented the Mono Basin population with genetic variation from other subspecies, which is not currently a management option, predicted significant increases in population size. Although we recommend that recovery activities should minimize future losses of genetic variation, genetic effects within these endangered populations-either negative (inbreeding depression) or positive (within subspecies genetic rescue)-appear unlikely to dramatically compromise or stimulate short-term conservation efforts. The distinction between detecting the effects of inbreeding depression on a component vital rate (e.g., fecundity) and the effects of inbreeding depression on population growth underscores the importance of quantifying inbreeding costs relative to population dynamics to effectively manage endangered populations.     

Area-based assessment of extinction risk

Underpinning the International Union for Conservation of Nature (IUCN) Red List is the assessment of extinction risk as determined by the size and degree of loss of populations. The IUCN system lists a species as Critically Endangered, Endangered, or Vulnerable if its population size declines 80%, 50%, or 30% within a given time frame. However, effective implementation of the system faces substantial challenges and uncertainty because geographic scale data on population size and long-term dynamics are scarce. I develop a model to quantify extinction risk using a measure based on a species' distribution, a much more readily obtained quantity. The model calculates the loss of the area of occupancy that is equivalent to the loss of a given proportion of a population. It is a very simple yet general model that has no free parameters and is independent of scale. The model predicted well the distributions of 302 tree species at a local scale and the distributions of 348 species of North American land birds. This area-based model provides a solution to the long-standing problem for IUCN assessments of lack of data on population sizes, and thus it will contribute to facilitating the quantification of extinction risk worldwide.     

Guidelines for genetic monitoring of translocated plant populations

Plant translocation is a useful tool for implementing assisted gene flow in recovery plans of critically endangered plant species. Although it helps to restore genetically viable populations, it is not devoid of genetic risks, such as poor adaptation of transplants and outbreeding depression in the hybrid progeny, which may have negative consequences in terms of demographic growth and plant fitness. Hence, a follow-up genetic monitoring should evaluate whether the translocated populations are genetically viable and self-sustaining in the short and long term. The causes of failure to adjust management responses also need to be identified. Molecular markers and fitness-related quantitative traits can be used to determine whether a plant translocation enhanced genetic diversity, increased fitness, and improved the probability of long-term survival. We devised guidelines and illustrated them with studies from the literature to help practitioners determine the appropriate genetic survey methods so that management practices can better integrate evolutionary processes. These guidelines include methods for sampling and for assessing changes in genetic diversity and differentiation, contemporary gene flow, mode of local recruitment, admixture level, the effects of genetic rescue, inbreeding or outbreeding depression and local adaptation on plant fitness, and long-term genetic changes.     

Applying habitat and population-density models to land-cover time series to inform IUCN Red List assessments

The IUCN (International Union for Conservation of Nature) Red List categories and criteria are the most widely used framework for assessing the relative extinction risk of species. The criteria are based on quantitative thresholds relating to the size, trends, and structure of species’ distributions and populations. However, data on these parameters are sparse and uncertain for many species and unavailable for others, potentially leading to their misclassification or classification as data deficient. We devised an approach that combines data on land-cover change, species-specific habitat preferences, population abundance, and dispersal distance to estimate key parameters (extent of occurrence, maximum area of occupancy, population size and trend, and degree of fragmentation) and hence predict IUCN Red List categories for species. We applied our approach to nonpelagic birds and terrestrial mammals globally (∼15,000 species). The predicted categories were fairly consistent with published IUCN Red List assessments, but more optimistic overall. We predicted 4.2% of species (467 birds and 143 mammals) to be more threatened than currently assessed and 20.2% of data deficient species (10 birds and 114 mammals) to be at risk of extinction. Incorporating the habitat fragmentation subcriterion reduced these predictions 1.5–2.3% and 6.4–14.9% (depending on the quantitative definition of fragmentation) for threatened and data deficient species, respectively, highlighting the need for improved guidance for IUCN Red List assessors on the application of this aspect of the IUCN Red List criteria. Our approach complements traditional methods of estimating parameters for IUCN Red List assessments. Furthermore, it readily provides an early-warning system to identify species potentially warranting changes in their extinction-risk category based on periodic updates of land-cover information. Given our method relies on optimistic assumptions about species distribution and abundance, all species predicted to be more at risk than currently evaluated should be prioritized for reassessment.     

Longitudinal monitoring of neutral and adaptive genomic diversity in a reintroduction

Restoration programs in the form of ex-situ breeding combined with reintroductions are becoming critical to counteract demographic declines and species losses. Such programs are increasingly using genetic management to improve conservation outcomes. However, the lack of long-term monitoring of genetic indicators following reintroduction prevents assessments of the trajectory and persistence of reintroduced populations. We carried out an extensive monitoring program in the wild for a threatened small-bodied fish (southern pygmy perch, Nannoperca australis) to assess the long-term genomic effects of its captive breeding and reintroduction. The species was rescued prior to its extirpation from the terminal lakes of Australia's Murray-Darling Basin, and then used for genetically informed captive breeding and reintroductions. Subsequent annual or biannual monitoring of abundance, fitness, and occupancy over a period of 11 years, combined with postreintroduction genetic sampling, revealed survival and recruitment of reintroduced fish. Genomic analyses based on data from the original wild rescued, captive born, and reintroduced cohorts revealed low inbreeding and strong maintenance of neutral and candidate adaptive genomic diversity across multiple generations. An increasing trend in the effective population size of the reintroduced population was consistent with field monitoring data in demonstrating successful re-establishment of the species. This provides a rare empirical example that the adaptive potential of a locally extinct population can be maintained during genetically informed ex-situ conservation breeding and reintroduction into the wild. Strategies to improve biodiversity restoration via ex-situ conservation should include genetic-based captive breeding and longitudinal monitoring of standing genomic variation in reintroduced populations.     

Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel

Abstract:  Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel ( Falco punctatus ) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N _eI= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N _eV= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.     

From Red Lists to Species of Conservation Concern

Abstract:  National red lists of threatened animal and plant species prepared according to the criteria of the World Conservation Union (IUCN) adequately reflect the extinction risk of species within a country but cannot be used directly to set conservation priorities. In particular, the significance of national populations for the conservation of the species as a whole is not taken into account. We present a procedure that can be used to assess national responsibility based on the national red-list status of a species, the international importance of the national population, and the species' "historical rarity" status. We distinguished five responsibility classes for breeding birds: B1, threatened species with internationally important populations in Switzerland; B2, threatened species with internationally less important populations; B3, nonthreatened species with internationally important populations; B4, nonthreatened species with internationally less important populations; and B5, species that have never been common in Switzerland. Two responsibility classes were distinguished for birds occurring in Switzerland as visitors: G1, species with large concentrations in Switzerland and an unfavorable conservation status in Europe, and G2, species with large concentrations in Switzerland and a favorable conservation status in Europe. Two additional classes (G3 and G4) for visiting species occurring in internationally less important numbers are possible but were not analyzed in detail. Responsibility classes B1, B2, B3, G1, and G2 were defined as species of national conservation concern. We developed the method for birds in Switzerland, but it can be used in other countries and for other taxonomic groups as well. It is particularly suitable where national red lists are established according to IUCN guidelines.     

Making Consistent IUCN Classifications under Uncertainty

Abstract: The World Conservation Union (IUCN) defined a set of categories for conservation status supported by decision rules based on thresholds of parameters such as distributional range, population size, population history, and risk of extinction. These rules have received international acceptance and have become one of the most important decision tools in conservation biology because of their wide applicability, objectivity, and simplicity of use. The input data for these rules are often estimated with considerable uncertainty due to measurement error, natural variation, and vagueness in definitions of parameters used in the rules. Currently, no specific guidelines exist for dealing with uncertainty. Interpretation of uncertain data by different assessors may lead to inconsistent classifications because attitudes toward uncertainty and risk may have an important influence on the classification of threatened species. We propose a method of dealing with uncertainty that can be applied to the current IUCN criteria without altering the rules, thresholds, or intent of these criteria. Our method propagates the uncertainty in the input parameters and assigns the evaluated species either to a single category (as the current criteria do) or to a range of plausible categories, depending on the nature and extent of uncertainties.     

Evaluating the outcomes of genetic rescue attempts

Augmenting gene flow is a powerful tool for the conservation of small, isolated populations. However, genetic rescue attempts have largely been limited to populations at the brink of extinction, in part due to concerns over negative outcomes (e.g., outbreeding depression). Increasing habitat fragmentation may necessitate more proactive genetic management. Broader application of augmented gene flow will, in turn, require rigorous evaluation to increase confidence and identify pitfalls in this approach. To date, there has been no assessment of best monitoring practices for genetic rescue attempts. We used genomically explicit, individual-based simulations to examine the effectiveness of common approaches (i.e., tests for increases in fitness, migrant ancestry, heterozygosity, and abundance) for determining whether genetic rescue or outbreeding depression occurred. Statistical power to detect the effects of gene flow on fitness was high (≥0.8) when effect sizes were large, a finding consistent with those from previous studies on severely inbred populations. However, smaller effects of gene flow on fitness can appreciably affect persistence probability but current evaluation approaches fail to provide results from which reliable inferences can be drawn. The power of the metrics we examined to evaluate genetic rescue attempts depended on the time since gene flow and whether gene flow was beneficial or deleterious. Encouragingly, the use of multiple metrics provided nonredundant information and improved inference reliability, highlighting the importance of intensive monitoring efforts. Further development of best practices for evaluating genetic rescue attempts will be crucial for a responsible transition to increased use of translocations to decrease extinction risk.     

Erosion of Heterozygosity in Fluctuating Populations

Abstract: Demographic, environmental, and genetic stochasticity threaten the persistence of isolated populations. The relative importance of these intertwining factors remains unresolved, but a common view is that random demographic and environmental events will usually drive small populations to the brink of extinction before genetic deterioration poses a serious threat. To evaluate the potential importance of genetic factors, we analyzed a model linking demographic and environmental conditions to the loss of genetic diversity in isolated populations undergoing natural levels of fluctuation. Nongenetic processes—environmental stochasticity and population demography—were modeled according to a bounded diffusion process. Genetic processes were modeled by quantifying the rate of drift according to the effective population size, which was predicted from the same parameters used to describe the nongenetic processes. We combined these models to predict the heterozygosity remaining at the time of extinction, as predicted by the nongenetic portion of the model. Our model predicts that many populations will lose most or all of their neutral genetic diversity before nongenetic random events lead to extinction. Given the abundant evidence for inbreeding depression and recent evidence for elevated extinction rates of inbred populations, our findings suggest that inbreeding may be a greater general threat to population persistence than is generally recognized. Therefore, conservation biologists should not ignore the genetic component of extinction risk when assessing species endangerment and developing recovery plans.     

Toward quantification of the impact of 21st‐century deforestation on the extinction risk of terrestrial vertebrates

Conservation actions need to be prioritized, often taking into account species’ extinction risk. The International Union for Conservation of Nature (IUCN) Red List provides an accepted, objective framework for the assessment of extinction risk. Assessments based on data collected in the field are the best option, but the field data to base these on are often limited. Information collected through remote sensing can be used in place of field data to inform assessments. Forests are perhaps the best‐studied land‐cover type for use of remote‐sensing data. Using an open‐access 30‐m resolution map of tree cover and its change between 2000 and 2012, we assessed the extent of forest cover and loss within the distributions of 11,186 forest‐dependent amphibians, birds, and mammals worldwide. For 16 species, forest loss resulted in an elevated extinction risk under red‐list criterion A, owing to inferred rapid population declines. This number increased to 23 when data‐deficient species (i.e., those with insufficient information for evaluation) were included. Under red‐list criterion B2, 484 species (855 when data‐deficient species were included) were considered at elevated extinction risk, owing to restricted areas of occupancy resulting from little forest cover remaining within their ranges. The proportion of species of conservation concern would increase by 32.8% for amphibians, 15.1% for birds, and 24.7% for mammals if our suggested uplistings are accepted. Central America, the Northern Andes, Madagascar, the Eastern Arc forests in Africa, and the islands of Southeast Asia are hotspots for these species. Our results illustrate the utility of satellite imagery for global extinction‐risk assessment and measurement of progress toward international environmental agreement targets.     

Genetically informed captive breeding of hybrids of an extinct species of Galapagos tortoise

Hybridization poses a major challenge for species conservation because it threatens both genetic integrity and adaptive potential. Yet, hybridization can occasionally offer unprecedented opportunity for species recovery if the genome of an extinct taxon is present among living hybrids such that selective breeding could recapture it. We explored the design elements for establishing a captive-breeding program for Galapagos tortoises (Chelonoidis spp.) built around individuals with admixed ancestry involving an extinct species. The target individuals were hybrids between the extinct species from Floreana Island, C. niger, and an extant species, C. becki, which were recently found in the endemic range of C. becki, from Wolf Volcano on Isabela Island. We combined genotypic data from 35 tortoises with high ancestry from C. niger with forward-in-time simulations to explore captive breeding strategies that maximized overall genetic diversity and ancestry from C. niger while accommodating resource constraints, species biology, and the urgency to return tortoises to Floreana Island for facilitating ecosystem restoration. Overall genetic diversity was maximized when in the simulation tortoises were organized in relatively small breeding groups. Substantial amounts of the C. niger genome were captured despite limited resources available for selectively breeding tortoises in captivity. Genetic diversity was maximized when captive-bred offspring were released to the wild rather than being used as additional breeders. Our results provide genetic-based and practical guidance on the inclusion of hybrids with genomic representation from extinct taxa into species restoration programs and informs the ongoing debate on the value of hybrids in biodiversity conservation.     

Scaling up private land conservation to meet recovery goals for grassland birds

Long-term population declines have elevated recovery of grassland avifauna to among the highest conservation priorities in North America. Because most of the Great Plains is privately owned, recovery of grassland bird populations depends on voluntary conservation with strong partnerships between private landowners and resource professionals. Despite large areas enrolled in voluntary practices through U.S. Department of Agriculture's Lesser Prairie-chicken (Tympanuchus pallidicinctus) Initiative (LPCI), the effectiveness of Farm Bill investments for meeting wildlife conservation goals remains an open question. Our objectives were to evaluate extents to which Conservation Reserve Program (CRP) and LPCI-grazing practices influence population densities of grassland birds; estimate relative contributions of practices to regional bird populations; and evaluate percentages of populations conserved relative to vulnerability of species. We designed a large-scale impact-reference study and used the Integrated Monitoring in Bird Conservation Regions program to evaluate bird population targets of the Playa Lakes Joint Venture. We used point transect distance sampling to estimate density and population size for 35 species of grassland birds on private lands enrolled in native or introduced CRP plantings and LPCI-prescribed grazing. Treatment effects indicated CRP plantings increased densities of three grassland obligates vulnerable to habitat loss, and LPCI grazing increased densities of four species requiring heterogeneity in dense, tall-grass structure (α = 0.1). Population estimates in 2016 indicated the practices conserved breeding habitat for 4.5 million birds (90% CI: 4.0–5.1), and increased population sizes of 16 species , totaling 1.8 million birds (CI: 1.4–2.4). Conservation practices on private land benefited the most vulnerable grassland obligate species (AIC_c weight = 0.53). By addressing habitat loss and degradation in agricultural landscapes, conservation on private land provides a solution to declining avifauna of North America and scales up to meet population recovery goals for the most imperiled grassland birds.     

Mutation and Conservation

Mutation can critically affect the viability of small populations by causing inbreeding depression, by maintaining potentially adaptive genetic variation in quantitative characters, and through the erosion of fitness by accumulation of mildly detrimental mutations. I review and integrate recent empirical and theoretical work on spontaneous mutation and its role in population viability and conservation planning. I analyze both the maintenance of potentially adaptive genetic variation in quantitative characters and the role of detrimental mutations in increasing the extinction risk of small populations. Recent experiments indicate that the rate of production of quasineutral, potentially adaptive genetic variance in quantitative characters is an order of magnitude smaller than the total mutational variance because mutations with large phenotypic effects tend to be strongly detrimental. This implies that, to maintain normal adaptive potential in quantitative characters under a balance between mutation and random genetic drift (or among mutation, drift, and stabilizing natural selection), the effective population size should be about 5000 rather than 500 (the Franklin-Soulé number). Recent theoretical results suggest that the risk of extinction due to the fixation of mildly detrimental mutations may be comparable in importance to environmental stochasticity and could substantially decrease the long-term viability of populations with effective sizes as large as a few thousand. These findings suggest that current recovery goals for many threatened and endangered species are inadequate to ensure long-term population viability.     

Effects of roost specialization on extinction risk in bats

Understanding causes and consequences of ecological specialization is of major concern in conservation. Specialist species are particularly vulnerable to human activities. If their food or habitats are depleted or lost, they may not be able to exploit alternative resources, and population losses may result. We examined International Union for Conservation of Nature (IUCN) Red List bat data and the number of roosts used per species (accounting for phylogenetic independence) to determine whether roost specialization is correlated with extinction risk. We found a significant correlation between the IUCN Red List category and the number of roost types used. Species that use fewer roost types had a higher risk of extinction. We found that caves and similar structures were the most widely used roost types, particularly by species under some level of risk of extinction. Many critically endangered, endangered, or vulnerable species used natural roosts exclusively, whereas less threatened species used natural and human‐made roosts. Our results suggest that roost loss, particularly in species that rely on a single roost type, may be linked to extinction risk. Our focus on a single life history trait prevented us from determining how important this variable is for extinction risk relative to other variables, but we have taken a first step toward prioritizing conservation actions. Our results also suggest that roost specialization may exacerbate population declines due to other risk factors, such as hunting pressure or habitat loss, and thus that management actions to preserve species under risk of extinction should prioritize protection of roosting sites.     

Trait‐based prediction of extinction risk of small‐bodied freshwater fishes

Small body size is generally correlated with r‐selected life‐history traits, including early maturation, short‐generation times, and rapid growth rates, that result in high population turnover and a reduced risk of extinction. Unlike other classes of vertebrates, however, small freshwater fishes appear to have an equal or greater risk of extinction than large fishes. We explored whether particular traits explain the International Union for Conservation of Nature (IUCN) Red List conservation status of small‐bodied freshwater fishes from 4 temperate river basins: Murray‐Darling, Australia; Danube, Europe; Mississippi‐Missouri, North America; and the Rio Grande, North America. Twenty‐three ecological and life‐history traits were collated for all 171 freshwater fishes of ≤120 mm total length. We used generalized linear mixed‐effects models to assess which combination of the 23 traits best explained whether a species was threatened or not threatened. We used the best models to predict the probability of 29 unclassified species being listed as threatened. With and without controlling for phylogeny at the family level, small body size—among small‐bodied species—was the most influential trait correlated with threatened species listings. The k‐folds cross‐validation demonstrated that body size and a random effect structure that included family predicted the threat status with an accuracy of 78% (SE 0.5). We identified 10 species likely to be threatened that are not listed as such on the IUCN Red List. Small body size is not a trait that provides universal resistance to extinction, particularly for vertebrates inhabiting environments affected by extreme habitat loss and fragmentation. We hypothesize that this is because small‐bodied species have smaller home ranges, lower dispersal capabilities, and heightened ecological specialization relative to larger vertebrates. Trait data and further model development are needed to predict the IUCN conservation status of the over 11,000 unclassified freshwater fishes, especially those under threat from proposed dam construction in the world's most biodiverse river basins.