Human Population Density and Extinction Risk in the World's Carnivores

Understanding why some species are at high risk of extinction, while others remain relatively safe, is central to the development of a predictive conservation science. Recent studies have shown that a species' extinction risk may be determined by two types of factors: intrinsic biological traits and exposure to external anthropogenic threats. However, little is known about the relative and interacting effects of intrinsic and external variables on extinction risk. Using phylogenetic comparative methods, we show that extinction risk in the mammal order Carnivora is predicted more strongly by biology than exposure to high-density human populations. However, biology interacts with human population density to determine extinction risk: biological traits explain 80% of variation in risk for carnivore species with high levels of exposure to human populations, compared to 45% for carnivores generally. The results suggest that biology will become a more critical determinant of risk as human populations expand. We demonstrate how a model predicting extinction risk from biology can be combined with projected human population density to identify species likely to move most rapidly towards extinction by the year 2030. African viverrid species are particularly likely to become threatened, even though most are currently considered relatively safe. We suggest that a preemptive approach to species conservation is needed to identify and protect species that may not be threatened at present but may become so in the near future.     

Phylogenetic distributions of British birds of conservation concern

Recent studies suggest that species' life histories and ecology can be used to forecast future extinction risk. Threatened species often share similar traits such that if a trait predisposing a species to decline or extinction is evolutionarily conserved, then close relatives of threatened species are themselves likely to be at risk. The phylogenetic distribution of current threat has been argued to provide insight into the species that could be threatened in the future when trait data are not available. Conservation criteria are typically based on multiple indices that capture different symptoms of threat including population trends and range contraction. However, there is no reason to assume consistent phylogenetic distributions of different symptoms. I construct a molecular phylogeny of 249 species of British birds (more than 93% of the breeding and wintering species) and use this to show that the species that are threatened due to population declines are phylogenetically more closely related than expected by chance alone. However, species that are listed for other reasons, including range contraction, are distributed randomly with respect to phylogeny. I suggest that while phylogeny can be informative with respect to identifying clades that are susceptible to some measures of extinction risk, such patterns are likely to be idiosyncratic with respect to symptom and taxa.     

Phylogenetically-informed priorities for amphibian conservation

The amphibian decline and extinction crisis demands urgent action to prevent further large numbers of species extinctions. Lists of priority species for conservation, based on a combination of species' threat status and unique contribution to phylogenetic diversity, are one tool for the direction and catalyzation of conservation action. We describe the construction of a near-complete species-level phylogeny of 5713 amphibian species, which we use to create a list of evolutionarily distinct and globally endangered species (EDGE list) for the entire class Amphibia. We present sensitivity analyses to test the robustness of our priority list to uncertainty in species' phylogenetic position and threat status. We find that both sources of uncertainty have only minor impacts on our 'top 100' list of priority species, indicating the robustness of the approach. By contrast, our analyses suggest that a large number of Data Deficient species are likely to be high priorities for conservation action from the perspective of their contribution to the evolutionary history.     

Predicting extinction risk in declining species

What biological attributes predispose species to the risk of extinction? There are many hypotheses but so far there has been no systematic analysis for discriminating between them. Using complete phylogenies of contemporary carnivores and primates, we present, to our knowledge, the first comparative test showing that high trophic level, low population density slow life history and, in particular, small geographical range size are all significantly and independently associated with a high extinction risk in declining species. These traits together explain nearly 50% of the total between-species variation in extinction risk. Much of the remaining variation can be accounted for by external anthropogenic factors that affect species irrespective of their biology.     

Integrating species traits with extrinsic threats: closing the gap between predicting and preventing species declines

In studies of extinction risk, it is often insufficient to conclude that species with narrow ranges or small clutch sizes require prioritized protection. To improve conservation outcomes, we also need to know which threats interact with these traits to endanger some species but not others. In this study, we integrated the spatial patterns of key threats to Australian amphibians with species' ecological/life-history traits to both predict declining species and identify their likely threats. In addition to confirming the importance of previously identified traits (e.g. narrow range size), we find that extrinsic threats (primarily the disease chytridiomycosis and invasive mosquitofish) are equally important and interact with intrinsic traits (primarily ecological group) to create guild-specific pathways to decline in our model system. Integrating the spatial patterns of extrinsic threats in extinction risk analyses will improve our ability to detect and manage endangered species in the future, particularly where data deficiency is a problem.     

Unravelling the structure of species extinction risk for predictive conservation science

Extinction risk varies across species and space owing to the combined and interactive effects of ecology/life history and geography. For predictive conservation science to be effective, large datasets and integrative models that quantify the relative importance of potential factors and separate rapidly changing from relatively static threat drivers are urgently required. Here, we integrate and map in space the relative and joint effects of key correlates of The International Union for Conservation of Nature-assessed extinction risk for 8700 living birds. Extinction risk varies significantly with species' broad-scale environmental niche, geographical range size, and life-history and ecological traits such as body size, developmental mode, primary diet and foraging height. Even at this broad scale, simple quantifications of past human encroachment across species' ranges emerge as key in predicting extinction risk, supporting the use of land-cover change projections for estimating future threat in an integrative setting. A final joint model explains much of the interspecific variation in extinction risk and provides a remarkably strong prediction of its observed global geography. Our approach unravels the species-level structure underlying geographical gradients in extinction risk and offers a means of disentangling static from changing components of current and future threat. This reconciliation of intrinsic and extrinsic, and of past and future extinction risk factors may offer a critical step towards a more continuous, forward-looking assessment of species' threat status based on geographically explicit environmental change projections, potentially advancing global predictive conservation science.     

Predicting how populations decline to extinction

Global species extinction typically represents the endpoint in a long sequence of population declines and local extinctions. In comparative studies of extinction risk of contemporary mammalian species, there appear to be some universal traits that may predispose taxa to an elevated risk of extinction. In local population-level studies, there are limited insights into the process of population decline and extinction. Moreover, there is still little appreciation of how local processes scale up to global patterns. Advancing the understanding of factors which predispose populations to rapid declines will benefit proactive conservation and may allow us to target at-risk populations as well as at-risk species. Here, we take mammalian population trend data from the largest repository of population abundance trends, and combine it with the PanTHERIA database on mammal traits to answer the question: what factors can be used to predict decline in mammalian abundance? We find in general that environmental variables are better determinants of cross-species population-level decline than intrinsic biological traits. For effective conservation, we must not only describe which species are at risk and why, but also prescribe ways to counteract this.     

Doomed to die? Predicting extinction risk in the true hawks Accipitridae

One of the most important tasks in conservation biology is identifying species at risk from extinction and establishing the most likely factors influencing this risk. Here, we consider an ecologically well-defined, monophyletic group of organisms, the true hawks of the family Accipitridae, which are not only among the most studied, but also contain some of the rarest bird species in the world. We investigate which intrinsic and extrinsic factors, covering morphology, life history and ecology, covary with International Union for the Conservation of Nature and Natural Resources threat status, as well as global population size and geographic range size. By decomposing threat status into population size and range size, we test whether any factors are generally important: we found that species with less habitat specialization, a larger clutch size and more plumage polymorphism were associated with lower extinction risk and larger population and range sizes. Species with special habitat requirements might be less capable of dealing with habitat transformation and fragmentation, while species with small clutch sizes might not be able to reverse population declines. Plumage polymorphism might indicate the size of the species' gene pool and could be a good marker of extinction risk. The analyses also emphasized that no single factor is likely to be sufficient when predicting the threat of extinction.     

Analysing Extinction Risk in Parrots using Decision Trees

Comparative analysis techniques have been successfully applied in a number of recent attempts to identify the species traits associated with a current threat of extinction although less often to predict which species may become threatened in the future. Although prediction of risk is obviously a priority, such analyses are undermined by the fact that there may be non-linear and non-additive relationships between the species traits used. A Decision Tree analysis can accommodate with such relationships and here it is used to explore factors affecting extinction risk in parrots. The results firstly verify that simple biological and biogeographical traits can separate threatened from non-threatened species. It is also possible to predict which species are likely to become threatened in the future. The utility of the method is not in testing evolutionary-based hypotheses to explain extinction risk, rather it is a simple and practical method of confirming and/or predicting levels of risk. For well known taxonomic groups it could be used to confirm current IUCN threat categories and identify which species should receive closest attention when the group is next reviewed. For poorly known groups it could be used to predict categories of threat for unclassified species from small groups of classified ones.     

Behavioral Correlates of Primates Conservation Status: Intrinsic Vulnerability to Anthropogenic Threats

Behavioral traits are likely to influence species vulnerability to anthropogenic threats and in consequence, their risk of extinction. Several studies have addressed this question and have highlighted a correlation between reproductive strategies and different viability proxies, such as introduction success and local extinction risk. Yet, very few studies have investigated the effective impact of social behaviour, and evidence regarding global extinction risk remains scant. Here we examined the effects of three main behavioral factors: the group size, the social and reproductive system, and the strength of sexual selection on global extinction risk. Using Primates as biological model, we performed comparative analysis on 93 species. The conservation status as described by the IUCN Red List was considered as a proxy for extinction risk. In addition, we added previously identified intrinsic factors of vulnerability to extinction, and a measure of the strength of the human impact for each species, described by the human footprint. Our analysis highlighted a significant effect of two of the three studied behavioral traits, group size and social and reproductive system. Extinction risk is negatively correlated with mean group size, which may be due to an Allee effect resulting from the difficulties for solitary and monogamous species to find a partner at low densities. Our results also indicate that species with a flexible mating system are less vulnerable. Taking into account these behavioral variables is thus of high importance when establishing conservation plans, particularly when assessing species relative vulnerability.     

Assessing Extinction Risk in Small Metapopulations of Golden‐headed Lion Tamarins (Leontopithecus chrysomelas) in Bahia State,Brazil

Golden‐headed lion tamarins (GHLTs; Leontopithecus chrysomelas) are endangered primates endemic to the Brazilian Atlantic Forest, where loss of forest and its connectivity threaten species survival. Understanding the role of habitat availability and configuration on population declines is critical for guiding proactive conservation for this, and other, endangered species. We conducted population viability analysis to assess vulnerability of ten GHLT metapopulations to habitat loss and small population size. Seven metapopulations had a low risk of extirpation (or local extinction) over the next 100 years assuming no further forest loss, and even small populations could persist with immediate protection. Three metapopulations had a moderate/high risk of extirpation, suggesting extinction debt may be evident in parts of the species’ range. When deforestation was assumed to continue at current rates, extirpation risk significantly increased while abundance and genetic diversity decreased for all metapopulations. Extirpation risk was significantly negatively correlated with the size of the largest patch available to metapopulations, underscoring the importance of large habitat patches for species persistence. Finally, we conducted sensitivity analysis using logistic regression, and our results showed that local extinction risk was sensitive to percentage of females breeding, adult female mortality, and dispersal rate and survival; conservation or research programs that target these aspects of the species’ biology/ecology could have a disproportionately important impact on species survival. We stress that efforts to protect populations and tracts of habitat of sufficient size throughout the species’ distribution will be important in the near‐term to protect the species from continuing decline and extinction.     

Phylogenetic autocorrelation of extinction threat in globally imperilled amphibians

The global extinction crisis demands immediate action to conserve species at risk. However, if entire clades such as superfamilies are at risk due to shared evolutionary history, a shift towards conserving clades rather than individual species may be needed. Using phylogenetic autocorrelation analysis, we demonstrate that multiple kinds of extinction threat clump within the amphibian tree of life. Our study provides insight into how these threats may collectively influence the extinction risk of whole clades, consistent with the supposition that related species, with similar traits, share an intrinsic vulnerability to common kinds of threat. Most strikingly, we find a significant concentration of 'enigmatic' decline and critically endangered status within families of the hyloid frogs. This phylogenetic clumping of risk is also geographically concentrated, with most threats found in Central and South America, and Australia, coinciding with reported outbreaks of chytridiomycosis. We speculate that the phylogenetic clumping of threat represents, in part, shared extinction proneness due to shared evolutionary history. However, even if the phylogenetic clumping of threat were simply a by-product of shared geography, this concordance between phylogenetic and geographical patterns represents a prime opportunity. Where practical, we should implement conservation plans that focus on biogeographical regions where threatened clades occur, thereby improving our ability to conserve species. This approach could outperform the usual triage approach of saving individual species after they have become critically endangered.     

Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics

Whereas previous studies have investigated correlates of extinction risk either at global or regional scales, our study explicitly models regional effects of anthropogenic threats and biological traits across the globe. Using phylogenetic comparative methods with a newly-updated supertree of 5020 extant mammals, we investigate the impact of species traits on extinction risk within each WWF ecoregion. Our analyses reveal strong geographical variation in the influence of traits on risk: notably, larger species are at higher risk only in tropical regions. We then relate these patterns to current and recent-historical human impacts across ecoregions using spatial modelling. The body–mass results apparently reflect historical declines of large species outside the tropics due to large-scale land conversion. Narrow-ranged and rare species tend to be at high risk in areas of high current human impacts. The interactions we describe between biological traits and anthropogenic threats increase understanding of the processes determining extinction risk.     

The comparative method in conservation biology

The phylogenetic comparative approach is a statistical method for analyzing correlations between traits across species. Whilst it has revolutionized evolutionary biology, can it work for conservation biology? Although it is correlative, advocates of the comparative method hope that it will reveal general mechanisms in conservation, provide shortcuts for prioritizing conservation research, and enable us to predict which species will experience (or create) problems in the future. Here, we ask whether these stated management goals are being achieved. We conclude that comparative methods are stimulating research into the ecological mechanisms underlying conservation, and are providing information for preemptive screening of problem species. But comparative analyses of extinction risk to date have tended to be too broad in scope to provide shortcuts to conserving particular endangered species. Correlates of vulnerability to conservation problems are often taxon, region and threat specific, so models must be narrowly focused to be of maximum practical use.     

Ecological correlates of extinction risk in Chinese birds

China is one of the countries with the richest bird biodiversity in the world. Among the 1372 Chinese birds, 146 species are considered threatened and three species are regionally extinct according to the officially released China Biodiversity Red List in 2015. Here, we conducted the first extensive analysis to systematically investigate the patterns and processes of extinction and threat in Chinese birds. We addressed the following four questions. First, is extinction risk randomly distributed among avian families in Chinese birds? Second, which families contain more threatened species than would be expected by chance? Third, which species traits are important in determining the extinction risk in Chinese birds using a multivariate phylogenetic comparative approach? Finally, is the form of the relationship between traits additive or nonadditive (synergistic)? We found that the extinction risk of Chinese birds was not randomly distributed among taxonomic families. The families that contained significantly more threatened species than expected were the hornbills, cranes, pittas, pheasants and hawks and eagles. We obtained eleven species traits that are commonly hypothesized to influence extinction risk from the literature: body size, clutch size, trophic level, mobility, habitat specificity, geographical range size, nest type, nest site, flocking tendency, migrant status and hunting vulnerability. After phylogenetic correction, model selection based on Akaike's information criterion identified the synergistic interaction between body size and hunting vulnerability as the single best correlate of extinction risk in Chinese birds. Our results suggest that, in order to be effective, priority management efforts should be given both to certain extinction‐prone families, particularly the hornbills, pelicans, cranes, pittas, pheasants and hawks and eagles, and to bird species with large body size and high hunting vulnerability.     

Human Population Density and Extinction Risk in the World's Carnivores

Understanding why some species are at high risk of extinction, while others remain relatively safe, is central to the development of a predictive conservation science. Recent studies have shown that a species' extinction risk may be determined by two types of factors: intrinsic biological traits and exposure to external anthropogenic threats. However, little is known about the relative and interacting effects of intrinsic and external variables on extinction risk. Using phylogenetic comparative methods, we show that extinction risk in the mammal order Carnivora is predicted more strongly by biology than exposure to high-density human populations. However, biology interacts with human population density to determine extinction risk: biological traits explain 80% of variation in risk for carnivore species with high levels of exposure to human populations, compared to 45% for carnivores generally. The results suggest that biology will become a more critical determinant of risk as human populations expand. We demonstrate how a model predicting extinction risk from biology can be combined with projected human population density to identify species likely to move most rapidly towards extinction by the year 2030. African viverrid species are particularly likely to become threatened, even though most are currently considered relatively safe. We suggest that a preemptive approach to species conservation is needed to identify and protect species that may not be threatened at present but may become so in the near future.     

Taxonomic selectivity in amphibians: ignorance, geography or biology?

Many taxa, including amphibians, have been shown to have a taxonomically non-random distribution of threatened species. There are three possible non-exclusive reasons for this selectivity: non-random knowledge of species conservation status, clades endemic to different regions experiencing different intensities of threatening process and the effects of clade-specific biological attributes on the susceptibility of species to these processes. This paper tests the sufficiency of the first two explanations using extinction risk evaluations from the 2004 Global Amphibian Assessment. Our results indicate that they cannot alone account for the degree of non-randomness in extinction risk among amphibian families. The overall distribution of threatened amphibians remained taxonomically non-random when species of unknown conservation status were omitted, and significant selectivity was detected not only at a global geographic scale but also in country- and site-specific data sets. Furthermore, the same families tend to be over- or underthreatened within different countries. Together, these results suggest that biological differences among amphibian families play an important role in determining species' susceptibility to anthropogenic threatening processes.     

LINEAGES THAT CHEAT DEATH: SURVIVING THE SQUEEZE ON RANGE SIZE

Evolutionary lineages differ greatly in their net diversification rates, implying differences in rates of extinction and speciation. Lineages with a large average range size are commonly thought to have reduced extinction risk (although linking low extinction to high diversification has proved elusive). However, climate change cycles can dramatically reduce the geographic range size of even widespread species, and so most species may be periodically reduced to a few populations in small, isolated remnants of their range. This implies a high and synchronous extinction risk for the remaining populations, and so for the species as a whole. Species will only survive through these periods if their individual populations are “threat tolerant,” somehow able to persist in spite of the high extinction risk. Threat tolerance is conceptually different from classic extinction resistance, and could theoretically have a stronger relationship with diversification rates than classic resistance. I demonstrate that relationship using primates as a model. I also show that narrowly distributed species have higher threat tolerance than widespread ones, confirming that tolerance is an unusual form of resistance. Extinction resistance may therefore operate by different rules during periods of adverse global environmental change than in more benign periods.     

Extinction risk of Chinese angiosperms varies between woody and herbaceous species

Aim

Understanding how species' traits and environmental contexts relate to extinction risk is a critical priority for ecology and conservation biology. This study aims to identify and explore factors related to extinction risk between herbaceous and woody angiosperms to facilitate more effective conservation and management strategies and understand the interactions between environmental threats and species' traits.

Location

China.

Taxon

Angiosperms.

Methods

We obtained a large dataset including five traits, six extrinsic variables, and 796,118 occurrence records for 14,888 Chinese angiosperms. We assessed the phylogenetic signal and used phylogenetic generalized least squares regressions to explore relationships between extinction risk, plant traits, and extrinsic variables in woody and herbaceous angiosperms. We also used phylogenetic path analysis to evaluate causal relationships among traits, climate variables, and extinction risk of different growth forms.

Results

The phylogenetic signal of extinction risk differed among woody and herbaceous species. Angiosperm extinction risk was mainly affected by growth form, altitude, mean annual temperature, normalized difference vegetation index, and precipitation change from 1901 to 2020. Woody species' extinction risk was strongly affected by height and precipitation, whereas extinction risk for herbaceous species was mainly affected by mean annual temperature rather than plant traits.

Main conclusions

Woody species were more likely to have higher extinction risks than herbaceous species under climate change and extinction threat levels varied with both plant traits and extrinsic variables. The relationships we uncovered may help identify and protect threatened plant species and the ecosystems that rely on them.     

Genetics and conservation biology

Conservation genetics encompasses genetic management of small populations, resolution of taxonomic uncertainties and management units, and the use of molecular genetic analyses in forensics and to understanding species' biology. The role of genetic factors in extinctions of wild populations has been controversial, but evidence now shows that they make important contributions to extinction risk. Inbreeding has been shown to cause extinctions of wild populations, computer projections indicate that inbreeding depression has important effects on extinction risk, and most threatened species show signs of genetic deterioration. Inappropriate management is likely to result if genetic factors are ignored in threatened species management.