The Importance of Assessing Climate Change Vulnerability to Address Species Conservation

Climate change is already altering ecosystems and presents a substantial threat to the conservation of biodiversity (Hughes 2000; Peñuelas and Filella 2001; Root et al. 2003). By adding to or altering impacts already affecting species, climate change modifies extinction risk and creates a complex challenge for conservation practitioners (McCarty 2001; MacNally et al. 2009). The Intergovernmental Panel on Climate Change projected that global extinction risk would increase by 20–30% as average temperature increases exceed 3.5°C (Solomon et al. 2007). In other cases, species extinction risk may be reduced if conditions related to climate become more favorable (Peterson et al. 2001; Erasmus et al. 2002; Reino et al. 2009). Change in extinction risk will vary by species, taxonomic group, region, and time elapsed leading to questions about where to focus conservation efforts (McDonald and Brown 1992; Peterson et al. 2002; Thomas et al. 2004; MacLean and Wilson 2011).

There are large numbers of species affected by a multitude of threats and limited resources for managing them; thus, conservation practitioners select a subset of species to actively manage (Mace and Lande 1991; Hannah et al. 2002; Millar et al. 2007). Although management priorities are influenced by a wide range of factors, such as cultural values, legal protection, and economics, the identification of species for conservation (often designated as “special status species”) generally focuses on those species most likely to go extinct (Master 1991; Mace et al. 2008). Estimating extinction risk for a species may be based on a set of quantitative criteria such as geographic range, population size and trends, and number of threats (Terborgh and Winter 1980; Gilpin and Soulé 1986).

Threats to species from climate change can be, but are not necessarily, distinct from other threats associated with extinction risk; nor are they independent (Hughes 2000; Fordham et al. 2012). For example, habitat loss is a major threat to many populations, but could be driven by climate (e.g., extended drought) or nonclimate (e.g., mining) forces. We have relatively little data on how populations will respond to changing climate over time or how other threats associated with extinction risk could be altered (Hughes 2000). Climate change threats also comprise many uncertainties because manifestations we currently observe will not match future impacts (Thomas et al. 2004; MacNally et al. 2009). Existing methodologies to identify species vulnerable to extinction, such as the International Union for Conservation of Nature Red List criteria, can accommodate climate change threats, but are not explicitly designed to do so (Mace and Lande 1991; Akçakaya et al. 2006). Effects of climate change fall within the criteria used to identify species at risk of extinction under the US Endangered Species Act (ESA 1973, as amended), but climate change has only recently been considered and for relatively few species (Scott et al. 2005; Ruhl 2008). Because integration of climate change as a threat is relatively new, it is unclear to what extent our current designations of special status species address extinction risk inclusive of climate change response. Climate change vulnerability assessments are a potentially valuable tool because they are designed to examine the potential response of species, or other targets, to relevant climate projections.

To examine the adequacy of current lists of species at high extinction risk to accommodate the added threat of projected climate change, we compared species identified as having special status from widely available lists with those vulnerable to climate change. By special status, we refer to species selected from a given suite of species in need of active management or attention to achieve conservation goals (e.g., persistence for 100 y) by various government and nongovernment entities. We compiled data on extinction risk from climate change for terrestrial vertebrate species from an assessment for the Middle Río Grande, New Mexico, United States (Finch et al. 2011; Friggens et al. 2013b). The Río Grande region makes a good example for examining species priorities because, not only are data for an entire suite of species available, but climate projections of hotter, drier conditions along with a rapidly expanding human populations portends high susceptibility to climate change impacts (Seager et al. 2007). Species that have already been identified as special status might be expected to remain at risk in the future, because climate change can exacerbate current threats that are often implicated in population decline, such as habitat fragmentation or small population size (Laurance and Williamson 2001). Furthermore, high extinction risk is commonly indicated for species that are specialized and restricted in range because they are sensitive to fluctuating or changing conditions, including climate. Alternatively, climate change presents new threats not traditionally considered in extinction risk, such as timing mismatches and exceeding physiological thresholds (Hughes 2000). Amelioration of threats by climate change and increasing populations are also possible through reduced predator populations, milder winters, or lower disease transmission (Harvell et al. 2002).

A similar comparison for birds, amphibians, and warm-water corals was conducted using climate change susceptibility (an index based on traits associated with greater vulnerability to extinction) as compared against threatened species from the International Union for Conservation of Nature Red List (Foden et al. 2008). That study found the majority of threatened species were susceptible to negative impacts of climate change and found that large numbers of nonthreatened species were also susceptible, highlighting the need for conservation action (Foden et al. 2008). Because of the consensus that more species will be at risk of extinction in the future, we expected to find vulnerable species missing from lists of special status for the terrestrial species of the Middle Rio Grande. We compared special status designation with climate change vulnerability to investigate 1) how well designation of special status aligned with climate change vulnerability, 2) whether results varied among taxonomic groups, 3) opportunities for improved species conservation under climate change, and 4) implications for future species conservation efforts.

To obtain predictions of extinction risk with climate change, we used a vulnerability assessment of terrestrial vertebrates to climate change for the Middle Río Grande, New Mexico, United States (Friggens et al. 2013b). This report focused on the “bosque” or riparian forest that is characterized by remnant gallery cottonwood (Populus sp.) forests that border the stretch of river between Elephant Butte Reservoir (33°20′58.10″N, 107°10′40.12″W, elevation 1,345 m) and Cochiti Dam (35°37′13.46″N, 106°19′21.03″W, elevation 1,610 m) that bisects the city of Albuquerque (Figure 1). The assessment report lists climate-change vulnerability scores for 117 regularly occurring species under projected climate changes up to 2050. Importantly for this comparison, assessed species were not selected based on special status or other criteria related to extinction risk, making it possible to examine climate change vulnerability of species considered not at risk for the region. Our analysis excluded one species (hoary bat, Lasiurus cinereus) included in the assessment that occurs only as a migrant in the region.

The extracted vulnerability scores were calculated from a pilot version of the System for Assessing Vulnerability of Species (Bagne et al. 2011), a scoring system based on a series of criteria or questions related to changes in survival or reproduction from projected climate change and climate-related factors (Table 1). This system included all three elements of species vulnerability; exposure, sensitivity, and adaptive capacity (Glick et al. 2011). Vulnerability of species to climate change was equated with extinction risk and estimated from a set of criteria representing species traits; this strategy has been shown to be predictive of population response (Allendorf et al. 1997; Broennimann et al. 2006; Jiguet et al. 2007; Young et al. 2011; Gardali et al. 2012). Traits associated with sensitivity may respond similarly to nonclimate threats; thus, factors influencing extinction risk in System for Assessing Vulnerability of Species are not necessarily unique to climate change assessment. Additionally, it is one of few assessment methods that consider migration and nonbreeding habitats (Small-Lorenz et al. 2013). The vulnerability score for a species is related to extinction risk through the number of criteria expected to result in population declines balanced by those resulting in population increases for factors related to climate change only. To facilitate comparison with conservation priorities, we converted vulnerability scores into categories of highly vulnerable (overall score >5), vulnerable (overall score >2), neutral (2 ≥overall score ≥−2), resilient (overall score <−2), and highly resilient (overall score <−5). Resilient categories under the scoring system indicate more criteria for a species are associated with population increase than decline and, therefore, extinction risk is reduced.

To capture a broad range of approaches to identifying species at risk of extinction, we extracted special status from three sources plus an additional two sources addressing only birds. Climate change effects were not necessarily excluded from any of these approaches, but all consider other threats. The three sources covering all taxonomic groups were U.S. Fish and Wildlife Service, NatureServe, and State of New Mexico, with special status defined as follows. Special status species at the national level were compiled from Federal endangered and threatened species listed by U.S. Fish and Wildlife Service under the U.S. Endangered Species Act (ESA 1973, as amended) as well as designated candidate species (www.fws.gov/endangered/; data accessed April 2011). We obtained subnational conservation status for New Mexico for each of our targeted species from the NatureServe website (version 7.1, http://explorer.natureserve.org/; data accessed March 2012) and included any species listed as “vulnerable,” “imperiled,” or “critically imperiled” (status  =  S1, S2, S3) as a special status species (Faber-Langendoen et al. 2012). We included a species as special status if designated as threatened, sensitive, and endangered under the New Mexico Wildlife Conservation Act or as the Species of Greatest Conservation Need by the New Mexico Comprehensive Wildlife Conservation Strategy (NMDGF 2006; data accessed March 2012). Note that information on distribution and population trend in New Mexico was taken from NatureServe and used, in part, to determine species of greatest conservation need (NMDGF 2006).

More estimates for extinction risk were available for birds from the Partners in Flight species assessment database and State of the Birds report on climate change (NABCI 2010, Panjabi et al. 2012). From Partners in Flight, we extracted threats to breeding scores, which evaluated current and future threats over the next 30 y for species in North America (Panjabi et al. 2012; http://rmbo.org/pifassessment/Database.aspx; data accessed February 2014). We included both scores where future conditions were expected to improve (score  =  1), which could be equated with resilience from the climate change assessment, and three categories of deteriorating conditions (score ≥ 3), which we equated with at risk of extinction. State of the Birds highlighted climate change by evaluating two climate factors (sensitivity and exposure) in addition to three factors unrelated to climate (NABCI 2010). Species were evaluated by broad habitat relationships and we extracted scores from western forest or aridlands habitats categorizing those species with medium to high vulnerability (score ≥ 2) as special status (http://www.stateofthebirds.org/2010/results-for-species; data accessed February 2014).

We compared the status of each species compiled from the special status species lists with those identified as vulnerable or highly vulnerable from the climate change assessment report. We used two categories of climate change vulnerability for the comparison because the selected threshold of vulnerability would affect the results. The Federal, New Mexico, and NatureServe lists enabled us to compare taxonomic groups, but given the additional information available for birds, we did a second comparison adding the two bird assessments to see how more information might alter the results. We evaluated the adequacy of current special status designation to capture climate change vulnerability by examining how often species overlapped or were missing between the compiled lists. A species was categorized as “overlapping” if it was vulnerable or highly vulnerable in the climate change assessment and had special status from any of the current special status lists. A species was categorized as “missing” if it was identified as climate-change vulnerable or highly vulnerable, but was not identified as special status on any of the lists. Introduced species were omitted from calculations of “overlapping” and “missing” for all but the birds-only comparison, because they were not evaluated in the other lists of special status. This only affected the number “missing” from climate-change vulnerable (score >2) for reptiles. We summed the number of overlapping and missing species across all species and for four taxonomic groups: birds, reptiles, amphibians, and mammals. We calculated the proportion of special status species that overlapped with the two categories of climate change vulnerability and the proportion of climate-change vulnerable species for both categories that were missing from current lists of special status. We also noted cases where special status overlapped with climate change resilience, climate-change vulnerable species were expected to experience improved conditions, or an introduced species was expected to be negatively affected by climate change; because, in these cases, climate change could create an opportunity (as opposed to a challenge) for more effective conservation management.

Of the 116 species we evaluated, 22 species were special status based on three current lists, 71 were identified as vulnerable to negative impacts of climate change, 30 of those were categorized as highly vulnerable, and 7 had a reduced extinction risk by 2050 for the Middle Río Grande (Tables 2 and 3). Although the climate change assessment was conducted specifically for the Middle Río Grande, we can expect species vulnerability scores to be comparable across a broader region with similar projections for climate and climate-related phenomena (Figure 1; Bagne et al. 2011). Current species conservation efforts will best accommodate changing climate when the overlap between species with special status and climate change vulnerability is high and the number of vulnerable species missing from priority lists is low. We found that climate change vulnerability often overlapped with special status (≥75% for all groups except reptiles). This is similar to results found for bird species of special concern in California, where 72% of those listed as at risk of extinction by the U.S. Fish and Wildlife Service were vulnerable to climate change (Gardali et al. 2012). When we focused on highly vulnerable species, overlap between special status and climate change vulnerability was reduced, particularly for mammals, indicating that inclusion of species on special status lists was not more likely with increasing impact of climate change (Table 3). Overlap implies that special status captures continuing extinction risk, although conservation measures may need to be intensified with additional or exacerbating threats (NABCI 2010). Conversely, many species vulnerable to climate change were missing from current special status lists and will potentially need intervention or monitoring (Table 3).

The need to reassess species conservation status to address climate change was not equal among taxonomic groups. Special status for amphibians best encompassed climate change vulnerability with the most overlap and the fewest missing, partly due to the fact that amphibians had the highest proportion of special status species, but only nine species were assessed. The International Union for Conservation of Nature comparison of the Red List and climate change susceptibility found that 75% of climate-change susceptible amphibian species overlapped those currently threatened with extinction and 53% of climate-change susceptible amphibian species were not listed as currently threatened, which closely matches our estimates for the other taxonomic groups (Foden et al. 2008). Reptiles fared worst in the comparison, with few reptile species identified as special status across three lists and poor agreement between current status and climate change vulnerability. Of potential benefit to reptiles was the finding that two introduced turtle species were vulnerable to declines, which could increase effectiveness of control measures and ultimately benefit some native species. Our findings add to the concern many have voiced about the rising threat of extinction for amphibians and reptiles due to climate change threats (Araujo et al. 2006; Sinervo et al. 2010).

Bird species, although exhibiting a large degree of overlap between special status and climate change vulnerability, had more than half of species vulnerable to climate change missing from special status lists (Table 3). Adding two special status lists for birds reduced the high number of vulnerable species missing from special status, but the proportion of overlap remained relatively unchanged (Tables 3 and 4). Although overlap between climate change vulnerability and special status did not improve, it is noteworthy that at-risk species from the State of the Birds (which had a climate change focus) were all identified as climate-change vulnerable in the Middle Río Grande assessment (Table 2). The majority of special status bird species only appeared on one list; thus, efforts adopting a single method of estimating extinction risk may overlook a large number of potentially declining species (Table 2).

We found no instances where special status species were predicted to be at lower extinction risk and few where introduced species would decline with climate change for the Middle Río Grande (Tables 3 and 4). This suggests that species subject to positive effects of climate change are not likely to be those at risk of extinction. Although opportunities may be few, they present a potentially cost-effective route to improved conservation and should garner greater recognition from those evaluating climate change impacts (Bradley et al. 2009).

Examination of individual species showed a tendency toward overlap between special status and climate change vulnerability when climate change exacerbated a current threat to a species, such as decline in riparian forests and drying of wetlands. For example, population declines leading to listing of the southwestern willow flycatcher Empidonax traillii extimus as an endangered species were attributed to the loss of dense riparian habitats, which is expected to continue under climate change and contributed to the species' vulnerability (McAda and Barroll 2002; U.S. Fish and Wildlife Service 2002; Hurd and Coonrod 2008; Finch et al. 2011; Friggens et al. 2013b). Similarly threatened by continued wetland loss, amphibian species overlapped well in our comparison as well as the one conducted by International Union for Conservation of Nature (Foden et al. 2008). Overlap under exacerbated threats was supported by an analysis of vulnerability for birds of conservation concern in California that found wetland birds to be the most vulnerable as climate change threatens already diminished habitats (Gardali et al. 2012). A species tended to be missing from special status lists when climate change introduced a new threat, such as exceeding thermal tolerances and altered timing of temporary pools. The checkered gartersnake Thamnophis marcianus, a species currently considered not at risk, was found highly vulnerable where changes to timing and quantity of rainfall were expected to impact onset and success of reproduction, dispersal opportunity, and prey availability (Friggens et al. 2013b). The appearance of new climate-related threats may have been responsible for the poor alignment we found for reptiles in general.

Current methods of determining special status primarily focus on rare or range-restricted species; thus, not surprisingly, several of the climate vulnerable species missing from priorities could be currently classified as common or abundant. Common or abundant species, however, are not immune to extinction nor are they necessarily resilient to climate change. History has shown that common species can decline rapidly under certain circumstances (Gaston and Fuller 2007a). Importantly, abundant species represent a large proportion of the individuals in a community and play a fundamental role in ecosystem structure and function (Gaston and Fuller 2007b). Their ecological contribution is particularly significant in light of frequently advocated climate change adaptation strategies that seek to enhance resilience of ecological communities and maintain critical ecosystem services.

Climate change vulnerability assessments of species are meant to supplement and not replace current species conservation priorities, but the lack of agreement among lists in our comparison demonstrates the importance of reexamining our reliance on special status lists within the context of a rapidly changing climate (Bagne and Finch 2012; Coe et al. 2012). To add just the species categorized as highly vulnerable to climate change to current special status lists would require a >80% increase. An almost 50% increase would be needed to include all highly vulnerable birds species even with the addition of two lists of at-risk species (Table 4). The solution is not necessarily to add all species that are climate-change vulnerable to special status lists, but we need to be more aware of what threats these lists are missing and find ways to respond to the growing challenge ahead. Methodology used to estimate extinction risk clearly affects special status designation and this should be recognized when applying the results of any assessment (Friggens et al. 2013a; Lankford et al. 2014). A critique of methods used to determine special status is outside the scope of this paper, but inadequacies of current lists to address climate change can be partly attributed to the retrospective approach taken where designation as special status often occurs after a species' numbers have declined to critical levels (Taylor et al. 2005).

Many advocate taking proactive steps to address the large magnitude and rapid pace of climate change threats, which will require conservation advocates to take a more prospective approach that uses projections in addition to observed population measures (Harris et al. 2006; Glick et al. 2011). Species conservation efforts need to consider the unique effects of climate change and anticipate rapidly increasing numbers of at-risk species. Many new methods are available or in development to predict species climate change response, including vulnerability indices (Czúcz et al. 2011; Bagne et al. 2011; Young et al. 2011), species distribution models (Schwartz et al. 2006; Keith et al. 2008; Thuiller et al. 2009), landscape connectivity (Cushman and Landuth 2012), and bioenergetic models (Buckley 2008; Sinervo et al. 2010). Work remains to be done to determine how to best balance traditional and climate-related threats in evaluating extinction risk given that threats will vary in time, space, and by species. Climate change vulnerability assessments can contribute by identifying species that may need further evaluation and by revealing mechanisms of species response that can be targeted by management actions. Other strategies to select conservation targets focus not on vulnerability, but on uncertainty, cost, public perception, or potential effectiveness of various management options (Regan et al. 2005; McDonald-Madden et al. 2008; Dawson et al. 2011). We are left with many questions: which species should receive management as threats to persistence increase, how can we incorporate disparate and interacting threats in estimating extinction risk, and should prioritization for management action be directed toward ecological function over rarity? However imperfect our knowledge, adding climate change vulnerability to the identification of at-risk species is a step that can be taken now and that will encourage proactive solutions.

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Reference S2. Table 3.1, climate change vulnerability scores from Friggens et al. 2013b; Reference S1.

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The development of this article was supported by U.S. Department of Agriculture Forest Service Rocky Mountain Research Station; University of Arizona School of Natural Resources and the Environment; a Research and Development grant through the U.S. Department of Agriculture Forest Service, Washington Office Climate Change Initiative; and by a U.S. Fish and Wildlife Service (USFWS) Bosque Initiative Grant (Final product for Agreement No. 201819H705). We thank C. Abeyta for her administration of the USFWS grant. Thank you to T. Rich and the anonymous reviewers for providing productive criticism and suggestions that greatly improved this paper.

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