Evaluation of assisted colonization strategies under global change for a rare,fire‐dependent plant

As a clear consensus is emerging that habitat for many species will dramatically reduce or shift with climate change, attention is turning to adaptation strategies to address these impacts. Assisted colonization is one such strategy that has been predominantly discussed in terms of the costs of introducing potential competitors into new communities and the benefits of reducing extinction risk. However, the success or failure of assisted colonization will depend on a range of population‐level factors that have not yet been quantitatively evaluated – the quality of the recipient habitat, the number and life stages of translocated individuals, the establishment of translocated individuals in their new habitat and whether the recipient habitat is subject to ongoing threats all will play an important role in population persistence. In this article, we do not take one side or the other in the debate over whether assisted colonization is worthwhile. Rather, we focus on the likelihood that assisted colonization will promote population persistence in the face of climate‐induced distribution changes and altered fire regimes for a rare endemic species. We link a population model with species distribution models to investigate expected changes in populations with climate change, the impact of altered fire regimes on population persistence and how much assisted colonization is necessary to minimize risk of decline in populations of Tecate cypress, a rare endemic tree in the California Floristic Province, a biodiversity hotspot. We show that assisted colonization may be a risk‐minimizing adaptation strategy when there are large source populations that are declining dramatically due to habitat contractions, multiple nearby sites predicted to contain suitable habitat, minimal natural dispersal, high rates of establishment of translocated populations and the absence of nonclimatic threats such as altered disturbance regimes. However, when serious ongoing threats exist, assisted colonization is ineffective.     

How ready are we to move species threatened from climate change? Insights into the assisted colonization debate from Australia

Assisted colonization, the intentional movement of species beyond their native range, has been proposed as a climate change adaptation tool for biodiversity conservation. The risks and benefits of its implementation are still being debated but already the climate is changing, species are moving and the pressure on at‐risk species must therefore be increasing. However, instances where moving species beyond their natural range purely for conservation purposes due to climate change are few, and the opportunity for science to inform practice is limited. Here we survey active participants in flora translocations and/or flora conservation in Australia in order to investigate the gap between theoretical and conceptual ideas about assisted colonization and to gauge preparedness for its implementation. We found that actions that mitigate proximal threats are preferred over those that move species beyond their current range. A lack of knowledge of species biology and ecology is an impediment to the acceptance of assisted colonization. In addition, prohibitive costs and the potential increased risk of the spread of diseases, pests and/or pathogens are viewed as more important obstacles of successful assisted colonization than potential for invasion at the recipient site. Full approval from all stakeholders at the source and recipient sites was found to be the most important factor for the successful assisted colonization of flora.     

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.     

Elucidating biological opportunities and constraints on assisted colonization

Assisted colonization is a proposed climate change adaptation strategy. Martin‐Alc?n et al. (Applied Vegetation Science, this issue) report an experiment to evaluate the efficacy of assisted colonization and identify thermal distance as a critical consideration. By extension, we should consider the role that ecological distance and socio‐political distance play within any plan to reduce extinction risk through assisted colonization.     

Body size and activity times mediate mammalian responses to climate change

Model predictions of extinction risks from anthropogenic climate change are dire, but still overly simplistic. To reliably predict at‐risk species we need to know which species are currently responding, which are not, and what traits are mediating the responses. For mammals, we have yet to identify overarching physiological, behavioral, or biogeographic traits determining species' responses to climate change, but they must exist. To date, 73 mammal species in North America and eight additional species worldwide have been assessed for responses to climate change, including local extirpations, range contractions and shifts, decreased abundance, phenological shifts, morphological or genetic changes. Only 52% of those species have responded as expected, 7% responded opposite to expectations, and the remaining 41% have not responded. Which mammals are and are not responding to climate change is mediated predominantly by body size and activity times (phylogenetic multivariate logistic regressions, P < 0.0001). Large mammals respond more, for example, an elk is 27 times more likely to respond to climate change than a shrew. Obligate diurnal and nocturnal mammals are more than twice as likely to respond as mammals with flexible activity times (P < 0.0001). Among the other traits examined, species with higher latitudinal and elevational ranges were more likely to respond to climate change in some analyses, whereas hibernation, heterothermy, burrowing, nesting, and study location did not influence responses. These results indicate that some mammal species can behaviorally escape climate change whereas others cannot, analogous to paleontology's climate sheltering hypothesis. Including body size and activity flexibility traits into future extinction risk forecasts should substantially improve their predictive utility for conservation and management.     

An empirical test of the relative and combined effects of land‐cover and climate change on local colonization and extinction

Land‐cover and climate change are two main drivers of changes in species ranges. Yet, the majority of studies investigating the impacts of global change on biodiversity focus on one global change driver and usually use simulations to project biodiversity responses to future conditions. We conduct an empirical test of the relative and combined effects of land‐cover and climate change on species occurrence changes. Specifically, we examine whether observed local colonization and extinctions of North American birds between 1981–1985 and 2001–2005 are correlated with land‐cover and climate change and whether bird life history and ecological traits explain interspecific variation in observed occurrence changes. We fit logistic regression models to test the impact of physical land‐cover change, changes in net primary productivity, winter precipitation, mean summer temperature, and mean winter temperature on the probability of Ontario breeding bird local colonization and extinction. Models with climate change, land‐cover change, and the combination of these two drivers were the top ranked models of local colonization for 30%, 27%, and 29% of species, respectively. Conversely, models with climate change, land‐cover change, and the combination of these two drivers were the top ranked models of local extinction for 61%, 7%, and 9% of species, respectively. The quantitative impacts of land‐cover and climate change variables also vary among bird species. We then fit linear regression models to test whether the variation in regional colonization and extinction rate could be explained by mean body mass, migratory strategy, and habitat preference of birds. Overall, species traits were weakly correlated with heterogeneity in species occurrence changes. We provide empirical evidence showing that land‐cover change, climate change, and the combination of multiple global change drivers can differentially explain observed species local colonization and extinction.     

Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change

Poleward range expansions are widespread responses to recent climate change and are crucial for the future persistence of many species. However, evolutionary change in traits such as colonization history and habitat preference may also be necessary to track environmental change across a fragmented landscape. Understanding the likelihood and speed of such adaptive change is important in determining the rate of species extinction with ongoing climate change. We conducted an amplified fragment length polymorphism (AFLP)‐based genome scan across the recently expanded UK range of the Brown Argus butterfly, Aricia agestis, and used outlier‐based (DFDIST and BayeScan) and association‐based (Isolation‐By‐Adaptation) statistical approaches to identify signatures of evolutionary change associated with range expansion and habitat use. We present evidence for (i) limited effects of range expansion on population genetic structure and (ii) strong signatures of selection at approximately 5% AFLP loci associated with both the poleward range expansion of A. agestis and differences in habitat use across long‐established and recently colonized sites. Patterns of allele frequency variation at these candidate loci suggest that adaptation to new habitats at the range margin has involved selection on genetic variation in habitat use found across the long‐established part of the range. Our results suggest that evolutionary change is likely to affect species’ responses to climate change and that genetic variation in ecological traits across species’ distributions should be maximized to facilitate range shifts across a fragmented landscape, particularly in species that show strong associations with particular habitats.     

Assisted Colonization: A Question of Focal Units and Recipient Localities

Assisted colonization as an adaptation strategy to conserve or restore biodiversity in the face of climate change deservedly evokes controversy. Assisted colonization is perceived by some as a last option for conserving endangered species and by others as a risky and unwise management effort due to current gaps of knowledge. Based on the pros and cons of the recent debate, we show that the current discussion mainly focuses on the assisted colonization of rare and endangered species beyond their natural range of distribution. We suggest that a more useful approach for the conservation of endangered species could occur by focusing on the relevant foundation or keystone species, which ensure ecosystem integrity for a multitude of dependent species by governing the habitat structure and micro‐climate of the site. Examples of foundation species include dominant tree species in forests or dominant corals in coral reefs. For a given conservation or restoration need (e.g. conservation of rare species), we recommend the assisted colonization of pre‐adapted ecotypes of the relevant foundation species from climates similar to future expectations for the target site. This approach could lead to climate‐safe habitats for endangered species with minimal adverse effects on recipient ecosystems.     

Plant extinction risk under climate change: are forecast range shifts alone a good indicator of species vulnerability to global warming?

Models that couple habitat suitability with demographic processes offer a potentially improved approach for estimating spatial distributional shifts and extinction risk under climate change. Applying such an approach to five species of Australian plants with contrasting demographic traits, we show that: (i) predicted climate‐driven changes in range area are sensitive to the underlying habitat model, regardless of whether demographic traits and their interaction with habitat patch configuration are modeled explicitly; and (ii) caution should be exercised when using predicted changes in total habitat suitability or geographic extent to infer extinction risk, because the relationship between these metrics is often weak. Measures of extinction risk, which quantify threats to population persistence, are particularly sensitive to life‐history traits, such as recruitment response to fire, which explained approximately 60% of the deviance in expected minimum abundance. Dispersal dynamics and habitat patch structure have the strongest influence on the amount of movement of the trailing and leading edge of the range margin, explaining roughly 40% of modeled structural deviance. These results underscore the need to consider direct measures of extinction risk (population declines and other measures of stochastic viability), as well as measures of change in habitat area, when assessing climate change impacts on biodiversity. Furthermore, direct estimation of extinction risk incorporates important demographic and ecosystem processes, which potentially influence species’ vulnerability to extinction due to climate change.     

Do species’ traits predict recent shifts at expanding range edges?

Although some organisms have moved to higher elevations and latitudes in response to recent climate change, there is little consensus regarding the capacity of different species to track rapid climate change via range shifts. Understanding species' abilities to shift ranges has important implications for assessing extinction risk and predicting future community structure. At an expanding front, colonization rates are determined jointly by rates of reproduction and dispersal. In addition, establishment of viable populations requires that individuals find suitable resources in novel habitats. Thus, species with greater dispersal ability, reproductive rate and ecological generalization should be more likely to expand into new regions under climate change. Here, we assess current evidence for the relationship between leading-edge range shifts and species' traits. We found expected relationships for several datasets, including diet breadth in North American Passeriformes and egg-laying habitat in British Odonata. However, models generally had low explanatory power. Thus, even statistically and biologically meaningful relationships are unlikely to be of predictive utility for conservation and management. Trait-based range shift forecasts face several challenges, including quantifying relevant natural history variation across large numbers of species and coupling these data with extrinsic factors such as habitat fragmentation and availability.     

A framework for the identification of hotspots of climate change risk for mammals

As rates of global warming increase rapidly, identifying species at risk of decline due to climate impacts and the factors affecting this risk have become key challenges in ecology and conservation biology. Here, we present a framework for assessing three components of climate‐related risk for species: vulnerability, exposure and hazard. We used the relationship between the observed response of species to climate change and a set of intrinsic traits (e.g. weaning age) and extrinsic factors (e.g. precipitation seasonality within a species geographic range) to predict, respectively, the vulnerability and exposure of all data‐sufficient terrestrial non‐volant mammals (3,953 species). Combining this information with hazard (the magnitude of projected climate change within a species geographic range), we identified global hotspots of species at risk from climate change that includes the western Amazon basin, south‐western Kenya, north‐eastern Tanzania, north‐eastern South Africa, Yunnan province in China, and mountain chains in Papua‐New Guinea. Our framework identifies priority areas for monitoring climate change effects on species and directing climate mitigation actions for biodiversity.     

Projections of suitable habitat under climate change scenarios: Implications for trans-boundary assisted colonization

? Premise of the study: Climate change may threaten endemic species with extinction, particularly relicts of the Arcto-Tertiary Forest, by elimination of their contemporary habitat. Projections of future habitat are necessary to plan for conservation of these species. ? Methods: We used spline climatic models and modified Random Forests statistical procedures to predict suitable habitats for Brewer spruce (Picea breweriana), which is endemic to the Klamath Region of California and Oregon. We used three general circulation models and two sets of carbon emission scenarios (optimistic and pessimistic) for future climates. ? Key results: Our procedures predicted present occurrence of Brewer spruce perfectly. For the decades 2030, 2060, and 2090, its projected range within the Klamath Region progressively declined, to the point of disappearance in the decade 2090. The climate niche was projected to move north to British Columbia, the Yukon Territory, and southeastern Alaska. ? Conclusion: The results emphasize the necessity of assisted colonization and trans-boundary movement to prevent extinction of Brewer spruce. The projections provide a framework for formulating conservation plans, but planners must also consider regulations regarding international plant transfers.     

Marine extinction risk shaped by trait–environment interactions over 500 million years

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait‐based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta‐analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait‐based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life‐habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow‐ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3–3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.     

Climate Change Risks and Conservation Implications for a Threatened Small-Range Mammal Species

Background

Climate change is already affecting the distributions of many species and may lead to numerous extinctions over the next century. Small-range species are likely to be a special concern, but the extent to which they are sensitive to climate is currently unclear. Species distribution modeling, if carefully implemented, can be used to assess climate sensitivity and potential climate change impacts, even for rare and cryptic species.

Methodology/Principal Findings

We used species distribution modeling to assess the climate sensitivity, climate change risks and conservation implications for a threatened small-range mammal species, the Iberian desman (Galemys pyrenaicus), which is a phylogenetically isolated insectivore endemic to south-western Europe. Atlas data on the distribution of G. pyrenaicus was linked to data on climate, topography and human impact using two species distribution modeling algorithms to test hypotheses on the factors that determine the range for this species. Predictive models were developed and projected onto climate scenarios for 2070–2099 to assess climate change risks and conservation possibilities. Mean summer temperature and water balance appeared to be the main factors influencing the distribution of G. pyrenaicus. Climate change was predicted to result in significant reductions of the species'' range. However, the severity of these reductions was highly dependent on which predictor was the most important limiting factor. Notably, if mean summer temperature is the main range determinant, G. pyrenaicus is at risk of near total extinction in Spain under the most severe climate change scenario. The range projections for Europe indicate that assisted migration may be a possible long-term conservation strategy for G. pyrenaicus in the face of global warming.

Conclusions/Significance

Climate change clearly poses a severe threat to this illustrative endemic species. Our findings confirm that endemic species can be highly vulnerable to a warming climate and highlight the fact that assisted migration has potential as a conservation strategy for species threatened by climate change.     

Temperature‐related geographical shifts among passerines: contrasting processes along poleward and equatorward range margins

Climate change is causing widespread geographical range shifts, which likely reflects different processes at leading and trailing range margins. Progressive warming is thought to relax thermal barriers at poleward range margins, enabling colonization of novel areas, but imposes increasingly unsuitable thermal conditions at equatorward margins, leading to range losses from those areas. Few tests of this process during recent climate change have been possible, but understanding determinants of species’ range limits will improve predictions of their geographical responses to climate change and variation in extinction risk. Here, we examine the relationship between poleward and equatorward range margin dynamics with respect to temperature‐related geographical limits observed for 34 breeding passerine species in North America between 1984–1988 and 2002–2006. We find that species’ equatorward range margins were closer to their upper realized thermal niche limits and proximity to those limits predicts equatorward population extinction risk through time. Conversely, the difference between breeding bird species’ poleward range margin temperatures and the coolest temperatures they tolerate elsewhere in their ranges was substantial and remained consistent through time: range expansion at species’ poleward range margins is unlikely to directly reflect lowered thermal barriers to colonization. The process of range expansion may reflect more complex factors operating across broader areas of species’ ranges. The latitudinal extent of breeding bird ranges is decreasing through time. Disparate responses observed at poleward versus equatorward margins arise due to differences in range margin placement within the realized thermal niche and suggest that climate‐induced geographical shift at equatorward range limits more strongly reflect abiotic conditions than at their poleward range limits. This further suggests that observed geographic responses to date may fail to demonstrate the true cost of climate change on the poleward portion of species’ distributions. Poleward range margins for North American breeding passerines are not presently in equilibrium with realized thermal limits.     

Terrestrial insects and climate change: adaptive responses in key traits

Understanding and predicting how adaptation will contribute to species' resilience to climate change will be paramount to successfully managing biodiversity for conservation, agriculture, and human health‐related purposes. Making predictions that capture how species will respond to climate change requires an understanding of how key traits and environmental drivers interact to shape fitness in a changing world. Current trait‐based models suggest that low‐ to mid‐latitude populations will be most at risk, although these models focus on upper thermal limits, which may not be the most important trait driving species' distributions and fitness under climate change. In this review, we discuss how different traits (stress, fitness and phenology) might contribute and interact to shape insect responses to climate change. We examine the potential for adaptive genetic and plastic responses in these key traits and show that, although there is evidence of range shifts and trait changes, explicit consideration of what underpins these changes, be that genetic or plastic responses, is largely missing. Despite little empirical evidence for adaptive shifts, incorporating adaptation into models of climate change resilience is essential for predicting how species will respond under climate change. We are making some headway, although more data are needed, especially from taxonomic groups outside of Drosophila, and across diverse geographical regions. Climate change responses are likely to be complex, and such complexity will be difficult to capture in laboratory experiments. Moving towards well designed field experiments would allow us to not only capture this complexity, but also study more diverse species.     

Metapopulation shift and survival of woodland birds under climate change: will species be able to track?

Climate change has been widely recognized as a key factor driving changes in species distributions. In this study we use a metapopulation model, with a window of suitable climate moving polewards, to explore population shifts and survival of woodland birds under different climate change scenarios and landscape configurations. Extinction vulnerability and expansion ability are predicted for the middle spotted woodpecker Dendrocopus medius and two alternative r‐K strategies under west European climate change scenarios of 1, 2 and 4°C temperature increase per century, corresponding to isotemperature velocities of ca 2, 4 and 8 km yr^?1. The simulated northward expansion of the bird's distribution is typically in the range of only 0–3 km yr^?1, in spite of 10–20 times larger maximum dispersal distances. This is too slow to track the climate change‐driven range contraction of 4 or 8 km yr^?1 in the south resulting in metapopulation extinction. Especially K‐selected (large‐bodied) species are vulnerable in the simulations. With a temperature increase of 4°C per century bird species go extinct within 104–178 yr. We present a simple approximation formula to predict the mean time to metapopulation extinction using 1) the rate of climate change, which determines the speed of range contraction in the south, 2) the size of the distribution range, which serves as a buffer against extinction, and 3) the northward expansion velocity, determined by species traits and landscape properties. Finally, our results indicate that the northward expansion rate is not constant. It will be initially lagged suggesting that recently observed expansion rates might be underestimations of future northward expansion rates.     

Linking habitat use to range expansion rates in fragmented landscapes: a metapopulation approach

Temperature increases because of climate change are expected to cause expansions at the high latitude margins of species distributions, but, in practice, fragmented landscapes act as barriers to colonization for most species. Understanding how species distributions will shift in response to climate change therefore requires techniques that incorporate the combined effects of climate and landscape‐scale habitat availability on colonization rates. We use a metapopulation model (Incidence Function Model, IFM) to test effects of fine‐scale habitat use on patterns and rates of range expansion by the butterfly Hesperia comma. At its northern range margin in Britain, this species has increased its breadth of microhabitat use because of climate warming, leading to increased colonization rates. We validated the IFM by reconstructing expansions in five habitat networks between 1982 and 2000, before using it to predict metapopulation dynamics over 100 yr, for three scenarios based on observed changes to habitat use. We define the scenarios as “cold‐world” (only hot, south‐facing 150–250° hillsides are deemed warm enough), “warm‐world” in which 100–300° hillsides can be populated, and “hot‐world”, where the background climate is warm enough to enable use of all aspects (as increasingly observed). In the simulations, increased habitat availability in the hot‐world scenario led to faster range expansion rates, and to long‐term differences in distribution size and pattern. Thus, fine‐scale changes in the distribution of suitable microclimates led to landscape‐scale changes in population size and colonization rate, resulting in coarse‐scale changes to the species distribution. Despite use of a wider range of habitats associated with climate change, H. comma is still expected to occupy a small fraction of available habitat in 100 yr. The research shows that metapopulation models represent a potential framework to identify barriers to range expansion, and to predict the effects of environmental change or conservation interventions on species distributions and persistence.     

Impacts of climate change on national biodiversity population trends

Climate change has had well‐documented impacts on the distribution and phenology of species across many taxa, but impacts on species’ abundance, which relates closely to extinction risk and ecosystem function, have not been assessed across taxa. In the most comprehensive multi‐taxa comparison to date, we modelled variation in national population indices of 501 mammal, bird, aphid, butterfly and moth species as a function of annual variation in weather variables, which through time allowed us to identify a component of species’ population growth that can be associated with post‐1970s climate trends. We found evidence that these climate trends have significantly affected population trends of 15.8% of species, including eight with extreme (> 30% decline per decade) negative trends consistent with detrimental impacts of climate change. The modelled effect of climate change could explain 48% of the significant across‐species population decline in moths and 63% of the population increase in winged aphids. The other taxa did not have significant across‐species population trends or consistent climate change responses. Population declines in species of conservation concern were linked to both climatic and non‐climatic factors respectively accounting for 42 and 58% of the decline. Evident differential impacts of climate change between trophic levels may signal the potential for future ecosystem disruption. Climate change has therefore already driven large‐scale population changes of some species, had significant impacts on the overall abundance of some key invertebrate groups and may already have altered biological communities and ecosystems in Great Britain.     

Tools for integrating range change,extinction risk and climate change information into conservation management

Ecological niche models (ENMs) are the primary tool used to describe and forecast the potential influence of climate change on biodiversity. However, ENMs do not directly account for important biological and landscape processes likely to affect range dynamics at a variety of spatial scales. Recent advances to link ENMs with population models have focused on the fundamental step of integrating dispersal and metapopulation dynamics into forecasts of species geographic ranges. Here we use a combination of novel analyses and a synthesis of findings from published plant and animal case studies to highlight three seldom recognised, yet important, advantages of linking ENMs with demographic modelling approaches: 1) they provide direct measures of extinction risk in addition to measures of vulnerability based on change in the potential range area or total habitat suitability. 2) They capture life‐history traits that permit population density to vary in different ways in response to key spatial drivers, conditioned by the processes of global change. 3) They can be used to explore and rank the cost effectiveness of regional conservation alternatives and demographically oriented management interventions. Given these advantages, we argue that coupled methods should be used preferentially where data permits and when conservation management decisions require intervention, prioritization, or direct estimates of extinction risk.