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.     

Predicting loss of evolutionary history: Where are we?

The Earth's evolutionary history is threatened by species loss in the current sixth mass extinction event in Earth's history. Such extinction events not only eliminate species but also their unique evolutionary histories. Here we review the expected loss of Earth's evolutionary history quantified by phylogenetic diversity (PD) and evolutionary distinctiveness (ED) at risk. Due to the general paucity of data, global evolutionary history losses have been predicted for only a few groups, such as mammals, birds, amphibians, plants, corals and fishes. Among these groups, there is now empirical support that extinction threats are clustered on the phylogeny; however this is not always a sufficient condition to cause higher loss of phylogenetic diversity in comparison to a scenario of random extinctions. Extinctions of the most evolutionarily distinct species and the shape of phylogenetic trees are additional factors that can elevate losses of evolutionary history. Consequently, impacts of species extinctions differ among groups and regions, and even if global losses are low within large groups, losses can be high among subgroups or within some regions. Further, we show that PD and ED are poorly protected by current conservation practices. While evolutionary history can be indirectly protected by current conservation schemes, optimizing its preservation requires integrating phylogenetic indices with those that capture rarity and extinction risk. Measures based on PD and ED could bring solutions to conservation issues, however they are still rarely used in practice, probably because the reasons to protect evolutionary history are not clear for practitioners or due to a lack of data. However, important advances have been made in the availability of phylogenetic trees and methods for their construction, as well as assessments of extinction risk. Some challenges remain, and looking forward, research should prioritize the assessment of expected PD and ED loss for more taxonomic groups and test the assumption that preserving ED and PD also protects rare species and ecosystem services. Such research will be useful to inform and guide the conservation of Earth's biodiversity and the services it provides.     

Macroecology and extinction risk correlates of frogs

Aim  Our aim was to test whether extinction risk of frog species could be predicted from their body size, fecundity or geographical range size. Because small geographical range size is a correlate of extinction risk in many taxa, we also tested hypotheses about correlates of range size in frogs.
Location  Global.
Methods  Using a large comparative data set ( n  = 527 species) compiled from the literature, we performed bivariate and multiple regressions through the origin of independent contrasts to test proposed macroecological patterns and correlates of extinction risk in frogs. We also created minimum adequate models to predict snout–vent length, clutch size, geographical range size and IUCN Red List status in frogs. Parallel non-phylogenetic analyses were also conducted. We verified the results of the phylogenetic analyses using gridded data accounting for spatial autocorrelation.
Results  The most threatened frog species tend to have small geographical ranges, although the relationship between range and extinction risk is not linear. In addition, tropical frogs with small clutches have the smallest ranges. Clutch size was strongly positively correlated with geographical range size ( r ² = 0.22) and body size ( r ² = 0.28).
Main conclusions  Our results suggest that body size and fecundity only affect extinction risk indirectly through their effect on geographical range size. Thus, although large frogs with small clutches tend to be endangered, there is no comparative evidence that this relationship is direct. If correct, this inference has consequences for conservation strategy: it would be inefficient to allocate conservation resources on the basis of low fecundity or large body size; instead it would be better to protect areas that contain many frog species with small geographical ranges.     

Phylogenetic,spatial and environmental components of extinction risk in carnivores

Aim Extinction risk is non‐randomly distributed across phylogeny and space and is influenced by environmental conditions. We quantified the relative contribution of these factors to extinction risk to unveil the underlying macroecological processes and derive predictive models. Location Global. Methods Based on the IUCN global assessments, we divided 192 carnivore species into two dichotomous classes representing different levels of extinction risk. We used spatial proximity, phylogenetic relationship and environmental variables together with phylogenetic eigenvector regression and spatial eigenvector filters to model and predict threat status. Results Our full models explained between 57% and 96% of the variance in extinction risk. Phylogeny and spatial proximity roughly explained between 21% and 70% of the total variation in all analyses, while the explanatory power of environmental conditions was relatively weaker (up to 15%). Phylogeny and spatial proximity contributed equally to the explained variance in the lower threat level, while spatial proximity was the most important factor in the models of the higher threat level. Prediction of threat status achieved 97% correct assignments. Main conclusions Our approach differs fundamentally from current studies of extinction risk because it does not necessarily rely on life‐history information. We clearly show that instead of treating phylogenetic inertia and spatial signal as statistical nuisances, space and phylogeny should be viewed as very useful in explaining a wide range of phenomena in comparative studies.     

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.     

Examining the extinction risk of specialized folivores: a comparative study of Colobine monkeys

Species extinctions are nonrandom with some taxa appearing to possess traits that increase their extinction risk. In this study, eight predictors of extinction risk were used as independent variables to predict the IUCN category of a subfamily of specialized folivorous primates, the Colobinae. All data were transformed into phylogenetically independent contrasts and were analyzed using bivariate regressions, multiple regression, and a maximum likelihood approach using Akaike's Information Criterion to assess model performance. Once an outlier was removed from the data set, species that devote a smaller proportion of their diet to mature leaf consumption appear to be at a greater risk of extinction. Also, as female body mass increases, so does extinction risk. In contrast, as maximum latitude and the number of habitat types increase, extinction risk appears to decrease. These findings emphasize the importance of examining detailed dietary variation for predicting extinction risk at a relatively fine taxonomic scale and, consequently, may help improve conservation management.     

Phylogenetic Patterns of Extinction Risk in the Eastern Arc Ecosystems,an African Biodiversity Hotspot

There is an urgent need to reduce drastically the rate at which biodiversity is declining worldwide. Phylogenetic methods are increasingly being recognised as providing a useful framework for predicting future losses, and guiding efforts for pre-emptive conservation actions. In this study, we used a reconstructed phylogenetic tree of angiosperm species of the Eastern Arc Mountains – an important African biodiversity hotspot – and described the distribution of extinction risk across taxonomic ranks and phylogeny. We provide evidence for both taxonomic and phylogenetic selectivity in extinction risk. However, we found that selectivity varies with IUCN extinction risk category. Vulnerable species are more closely related than expected by chance, whereas endangered and critically endangered species are not significantly clustered on the phylogeny. We suggest that the general observation for taxonomic and phylogenetic selectivity (i.e. phylogenetic signal, the tendency of closely related species to share similar traits) in extinction risks is therefore largely driven by vulnerable species, and not necessarily the most highly threatened. We also used information on altitudinal distribution and climate to generate a predictive model of at-risk species richness, and found that greater threatened species richness is found at higher altitude, allowing for more informed conservation decision making. Our results indicate that evolutionary history can help predict plant susceptibility to extinction threats in the hyper-diverse but woefully-understudied Eastern Arc Mountains, and illustrate the contribution of phylogenetic approaches in conserving African floristic biodiversity where detailed ecological and evolutionary data are often lacking.     

Extinction

In the life of any species, extinction is the final evolutionary process. It is a common one at present, as the world is entering a major extinction crisis. The pattern of extinction and threat is very non-random, with some taxa being more vulnerable than others. Explaining why some taxa are affected and some escape is a major goal of conservation biology. More ambitiously, a predictive model could, in principle, be built by integrating comparable studies of past and present extinctions. We review progress towards both explanatory and predictive frameworks, comparing correlates of extinction in different groups at different times. Progress towards explanatory models for the current crisis is promising, at least in some well-studied taxa, but the development of a truly predictive model is hampered by the formidable difficulties of integrating studies of present and past extinctions.     

A Global Trend towards the Loss of Evolutionarily Unique Species in Mangrove Ecosystems

The mangrove biome stands out as a distinct forest type at the interface between terrestrial, estuarine, and near-shore marine ecosystems. However, mangrove species are increasingly threatened and experiencing range contraction across the globe that requires urgent conservation action. Here, we assess the spatial distribution of mangrove species richness and evolutionary diversity, and evaluate potential predictors of global declines and risk of extinction. We found that human pressure, measured as the number of different uses associated with mangroves, correlated strongly, but negatively, with extinction probability, whereas species ages were the best predictor of global decline, explaining 15% of variation in extinction risk. Although the majority of mangrove species are categorised by the IUCN as Least Concern, our finding that the more threatened species also tend to be those that are more evolutionarily unique is of concern because their extinction would result in a greater loss of phylogenetic diversity. Finally, we identified biogeographic regions that are relatively species-poor but rich in evolutionary history, and suggest these regions deserve greater conservation priority. Our study provides phylogenetic information that is important for developing a unified management plan for mangrove ecosystems worldwide.     

Scale of population synchrony confirms macroecological estimates of minimum viable range size

Global ecosystems are facing a deepening biodiversity crisis, necessitating robust approaches to quantifying species extinction risk. The lower limit of the macroecological relationship between species range and body size has long been hypothesized as an estimate of the relationship between the minimum viable range size (MVRS) needed for species persistence and the organismal traits that affect space and resource requirements. Here, we perform the first explicit test of this assumption by confronting the MVRS predicted by the range-body size relationship with an independent estimate based on the scale of synchrony in abundance among spatially separated populations of riverine fish. We provide clear evidence of a positive relationship between the scale of synchrony and species body size, and strong support for the MVRS set by the lower limit of the range-body size macroecological relationship. This MVRS may help prioritize first evaluations for unassessed or data-deficient taxa in global conservation assessments.     

A Comprehensive Quantitative Assessment of Bird Extinction Risk in Brazil

In an effort to avoid species loss, scientists have focused their efforts on the mechanisms making some species more prone to extinction than others. However, species show different responses to threats given their evolutionary history, behavior, and intrinsic biological features. We used bird biological features and external threats to (1) understand the multiple pathways driving Brazilian bird species to extinction, (2) to investigate if and how extinction risk is geographically structured, and (3) to quantify how much diversity is currently represented inside protected areas. We modeled the extinction risk of 1557 birds using classification trees and evaluated the relative contribution of each biological feature and external threat in predicting extinction risk. We also quantified the proportion of species and their geographic range currently protected by the network of Brazilian protected areas. The optimal classification tree showed different pathways to bird extinction. Habitat conversion was the most important predictor driving extinction risk though other variables, such as geographic range size, type of habitat, hunting or trapping and trophic guild, were also relevant in our models. Species under higher extinction risk were concentrated mainly in the Cerrado Biodiversity Hotspot and were not quite represented inside protected areas, neither in richness nor range. Predictive models could assist conservation actions, and this study could contribute by highlighting the importance of natural history and ecology in these actions.     

A macroecological approach to evolutionary rescue and adaptation to climate change

Despite the widespread use of ecological niche models (ENMs) for predicting the responses of species to climate change, these models do not explicitly incorporate any population‐level mechanism. On the other hand, mechanistic models adding population processes (e.g. biotic interactions, dispersal and adaptive potential to abiotic conditions) are much more complex and difficult to parameterize, especially if the goal is to predict range shifts for many species simultaneously. In particular, the adaptive potential (based on genetic adaptations, phenotypic plasticity and behavioral adjustments for physiological responses) of local populations has been a less studied mechanism affecting species’ responses to climatic change so far. Here, we discuss and apply an alternative macroecological framework to evaluate the potential role of evolutionary rescue under climate change based on ENMs. We begin by reviewing eco‐evolutionary models that evaluate the maximum sustainable evolutionary rate under a scenario of environmental change, showing how they can be used to understand the impact of temperature change on a Neotropical anuran species, the Schneider's toad Rhinella diptycha. Then we show how to evaluate spatial patterns of species’ geographic range shift using such models, by estimating evolutionary rates at the trailing edge of species distribution estimated by ENMs and by recalculating the relative amount of total range loss under climate change. We show how different models can reduce the expected range loss predicted for the studied species by potential ecophysiological adaptations in some regions of the trailing edge predicted by ENMs. For general applications, we believe that parameters for large numbers of species and populations can be obtained from macroecological generalizations (e.g. allometric equations and ecogeographical rules), so our framework coupling ENMs with eco‐evolutionary models can be applied to achieve a more accurate picture of potential impacts from climate change and other threats to biodiversity.     

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.     

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 correlates of extinction risk in mammals: species in older lineages are not at greater risk

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.     

Guiding the prioritization of the most endangered and evolutionary distinct birds for new zoo conservation programs

Zoos have played a pivotal role in the successful reinforcement and reintroduction of species threatened with extinction, but prioritization is required in the face of increasing need and limited capacity. One means of prioritizing between species of equal threat status when establishing new breeding programs is the consideration of evolutionary distinctness (ED). More distinct species have fewer close relatives such that their extinction would result in a greater overall loss to the Tree of Life. Considering global ex situ holdings of birds (a group with a complete and well‐detailed evolutionary tree), we investigate the representation of at‐risk and highly evolutionarily distinct species in global zoo holdings. We identified a total of 2,236 bird species indicated by the Zoological Information Management System as being held in zoological institutions worldwide. As previously reported, imperiled species (defined as those possessing endangered or critically endangered threat status) in this database are less likely to be held in zoos than non‐imperiled species. However, we find that species possessing ED scores within the top 10% of all bird species are more likely to be held in zoos than other species, possibly because they possess unique characteristics that have historically made them popular exhibits. To assist with the selection of high priority ED species for future zoo conservation programs, we provide a list of imperiled species currently not held in zoos, ranked by ED. This list highlights species representing particular priorities for ex situ conservation planners, and represents a practical tool for improving the conservation value of zoological collections.     

How does the 50/500 rule apply to MVPs?

The 50/500 rule has been used as a guiding principle in conservation for assessing minimum viable effective population size (N(e)). There is much confusion in the recent literature about how the 500 value should be applied to assess extinction risk and set priorities in conservation biology. Here, we argue that the confusion arises when the genetic basis for a short-term N(e) of 50 to avoid inbreeding depression is used to justify a long-term N(e) of 500 to maintain evolutionary potential. This confusion can result in misleading conclusions about how genetic arguments alone are sufficient to set minimum viable population (MVP) thresholds for assessing the extinction risk of threatened species, especially those that emphasize that MVPs should be in the thousands to maintain evolutionary potential.     

Threatened reef corals of the world

A substantial proportion of the world's living species, including one-third of the reef-building corals, are threatened with extinction and in pressing need of conservation action. In order to reduce biodiversity loss, it is important to consider species' contribution to evolutionary diversity along with their risk of extinction for the purpose of setting conservation priorities. Here I reconstruct the most comprehensive tree of life for the order Scleractinia (1,293 species) that includes all 837 living reef species, and employ a composite measure of phylogenetic distinctiveness and extinction risk to identify the most endangered lineages that would not be given top priority on the basis of risk alone. The preservation of these lineages, not just the threatened species, is vital for safeguarding evolutionary diversity. Tests for phylogeny-associated patterns show that corals facing elevated extinction risk are not clustered on the tree, but species that are susceptible, resistant or resilient to impacts such as bleaching and disease tend to be close relatives. Intensification of these threats or extirpation of the endangered lineages could therefore result in disproportionate pruning of the coral tree of life.     

Nested communities,invasive species and Holocene extinctions: evaluating the power of a potential conservation tool

General ecological methods and models that require a minimum amount of information yet are still able to inform conservation planning are particularly valuable. Nested subset analysis has been advocated as such a tool for the prediction of extinction-prone species and populations. However, such advocacy has not been without skepticism and debate, and in the majority of published examples assessing extinction vulnerability, actual extinctions are based on assumptions rather than direct evidence. Here, we empirically test the power of nested subset analysis to predict extinction-prone species, using documented Holocene insular mammal extinctions on three island archipelagos off the west coast of North America. We go on to test whether the introduction of invasive mammals promotes nestedness on islands via extinction. While all three archipelagos were significantly nested before and after the extinction events, nested subset analysis largely failed to predict extinction patterns. We also failed to detect any correlations between the degree of nestedness at the genus-level with area, isolation, or species richness and extinction risk. Biogeography tools, such as nested subset analysis, must be critically evaluated before they are prescribed widely for conservation planning. For these island archipelagos, it appears detailed natural history and taxa-specific ecology may prove critical in predicting patterns of extinction risk.     

Drivers of extinction risk in African mammals: the interplay of distribution state,human pressure,conservation response and species biology

Although conservation intervention has reversed the decline of some species, our success is outweighed by a much larger number of species moving towards extinction. Extinction risk modelling can identify correlates of risk and species not yet recognized to be threatened. Here, we use machine learning models to identify correlates of extinction risk in African terrestrial mammals using a set of variables belonging to four classes: species distribution state, human pressures, conservation response and species biology. We derived information on distribution state and human pressure from satellite-borne imagery. Variables in all four classes were identified as important predictors of extinction risk, and interactions were observed among variables in different classes (e.g. level of protection, human threats, species distribution ranges). Species biology had a key role in mediating the effect of external variables. The model was 90% accurate in classifying extinction risk status of species, but in a few cases the observed and modelled extinction risk mismatched. Species in this condition might suffer from an incorrect classification of extinction risk (hence require reassessment). An increased availability of satellite imagery combined with improved resolution and classification accuracy of the resulting maps will play a progressively greater role in conservation monitoring.