Seeking shelter from the storm: Conservation and management of imperiled species in a changing climate

Abstract Climate change is anticipated to exacerbate the extinction risk of species whose persistence is already compromised by habitat loss, invasive species, disease, or other stressors. In coastal areas of the southeastern United States (USA), many imperiled vertebrates are vulnerable to hurricanes, which climate models predict to become more severe in the 21st century. Despite this escalating threat, explicit adaptation strategies that address hurricane threats, in particular, and climate change more generally, are largely underrepresented in recovery planning and implementation. We provide a basis for stronger emphasis on strategic planning for imperiled species facing the increasing threat of catastrophic hurricanes. Our reasoning comes from observations of short‐term environmental and biological impacts of Hurricane Michael, which impacted the Gulf Coast of the southeastern USA in October 2018. During this storm, St. Marks National Wildlife Refuge, located along the northern Gulf of Mexico's coast in the panhandle region of Florida, received storm surge that was 3.0–3.6 m (NAVD88) above sea level. Storm surge pushed sea water into some ephemeral freshwater ponds used for breeding by the federally threatened frosted flatwoods salamander (Ambystoma cingulatum). After the storm, specific conductance across all ponds measured varied from 80 to 23,100 µS/cm, compared to 75 to 445 µS/cm in spring 2018. For 17 overwashed wetlands that were measured in both spring and fall 2018, posthurricane conductance observations were, on average, more than 90 times higher than in the previous spring, setting the stage for varying population responses across this coastal landscape. Importantly, we found live individual flatwoods salamanders at both overwashed and non‐overwashed sites, although we cannot yet assess the demographic consequences of this storm. We outline actions that could be incorporated into climate adaptation strategies and recovery planning for imperiled species, like A. cingulatum, that are associated with freshwater coastal wetlands in hurricane‐prone regions.


| INTRODUC TI ON
A species' viability is shaped by local and landscape scale processes that reflect three fundamental conservation principles, collectively known as "the 3Rs" (Shaffer & Stein, 2000;Smith et al., 2018; U.S. Fish & Wildlife Service [USFWS], 2016). At the local scale, resiliency refers to the ability of individual populations to withstand environmental and demographic stochasticity. At the landscape scale, a viable species has sufficient representation across a variety of ecological settings, enabling it to adapt to changing environmental conditions over space and time. Lastly, a species' viability depends on redundancy, the existence of multiple populations at both scales, minimizing extinction risk due to catastrophic events. Most species of conservation concern are deficient in one or more of these three measures, but those that have few, small, isolated populations with limited geographic ranges are especially at risk (Purvis, Gittleman, Cowlishaw, & Mace, 2000;Soulé, 1987), as "no single population is immune to the chance of catastrophic extinction" (Shaffer & Stein, 2000).
Climate change is already negatively impacting many taxaincluding global fisheries that are critical food resources for a growing human population (Free et al., 2019;Pacifici et al., 2017).
Consequently, climate change is anticipated to be one of the most significant drivers of ecological and societal change in the coming century (Lawler et al., 2009). For freshwater coastal wetlands, accelerated sea level rise and saltwater intrusion have been the focal points of climate change research and management planning . However, tropical cyclonic storms (hurricanes) also pose a formidable threat to coastal ecosystems. Since the 1970s, both frequency and intensity of the strongest North Atlantic tropical cyclones have increased (Bhatia et al., 2019;Hartmann et al., 2013). Current climate change models (e.g., the CMIP3-A1B scenario and the CMIP5-early and late 21st century scenarios) predict fewer Atlantic tropical storms in warmer climates and an increase in the frequency of the most intense hurricanes (Categories 4 and 5), although this predicted increased frequency varies among models (i.e., a substantially increased frequency is predicted for Categories 4 and 5 hurricanes using the CMIP3 model, but smaller increases are projected using the CMIP5-early and CMIP5-late models; Knutson et al., 2013). This projected escalation of catastrophic hurricanes is an unprecedented challenge for conservation and management of imperiled species that inhabit coastal ecosystems.
Freshwater wetlands provide critical habitat for a diverse array of organisms, including many sensitive species of conservation concern (Howard et al., 2015). For example, flatwoods salamanders (Ambystoma cingulatum and Ambystoma bishopi) are specialists of mesic pine flatwoods and savannas on the Coastal Plain of the southeastern USA; these two species currently exist only as isolated metapopulations in a few locations within their historic range (Semlitsch, Walls, Barichivich, & O'Donnell, 2017) The impacts of hurricane-related saltwater intrusion have been well documented for wetland vegetation and many vertebrates found in coastal habitats (e.g., Guntenspergen et al., 1995;Gunzburger, Hughes, Barichivich, & Staiger, 2010;Roman et al., 1994;Schriever, Ramspott, Crother, & Fontenot, 2009;Steyer et al., 2010), yet proactive approaches to reduce threats from hurricanes before they occur are often lacking. This deficiency provides an opportunity to revisit existing strategies for managing vulnerable species in hurricane-prone areas and to develop or update action plans where needed (sensu Povilitis & Suckling, 2010).
We provide preliminary assessments of some environmental and biological impacts from storm surge associated with Hurricane Michael. On 10 October 2018, this storm made landfall in the panhandle region of Florida and resulted in saltwater inundation in some areas of the Refuge, including many wetlands used by A. cingulatum for breeding. We also explore the extent to which hurricane-adaptation strategies have been developed for imperiled vertebrates in hurricane-prone coastal areas. Based on our assessments, we outline the need for a proactive management framework to reduce risk of future catastrophic storm impacts on vulnerable populations of this species, in particular, and for imperiled species in hurricaneprone regions, in general.

| S T. MARK S NATI ONAL WILDLIFE REFUG E , FROS TED FL AT WOODS SAL AMANDER S , AND HURRIC ANE MICHAEL
St. Marks National Wildlife Refuge is a wetland-rich region in one of the five richest biodiversity hotspots in North America (Blaustein, 2008;Noss et al., 2015). The Gulf Coast of the southeastern USA is also extremely vulnerable to sea level rise (Enwright, Griffith, & Osland, 2016). The Refuge consists of 32,042 ha of upland and wetland habitats broadly classified as sandhills, flatwoods, and hammocks. A diverse amphibian community consisting of 31 species (20 anurans, 11 salamanders) can be found on the Refuge (Dodd, Barichivich, Johnson, & Staiger, 2007). Ambystoma cingulatum is confined to hydric flatwoods located in the eastern-most region of the Refuge, the St. Marks Unit (Figure 1).
Historically, flatwoods salamanders occurred across southern Alabama, the panhandle and north central regions of Florida, southern Georgia, and South Carolina (Palis & Means, 2005). In recent years, however, and despite intense efforts to monitor and locate new populations, the two flatwoods salamander species have collectively experienced an 86.8% loss of populations (Semlitsch et al., 2017). The primary threats currently affecting flatwoods salamanders are changes in habitat (loss, fragmentation, and degradation), climate (particularly drought and variation in the timing of rainfall), and interactions between these threats ( Figure 2). Extreme precipitation events, resulting in drought and flooding, along with hurricane-induced storm surge (Lin, Lane, Emanuel, Sullivan, & Donnelly, 2014), can potentially impact amphibians that use freshwater coastal wetlands (Walls, Barichivich, & Brown, 2013). Moreover, phenological shifts in the timing of key climatic events (e.g., pond-filling and drying) can have significant consequences for individual survival and species persistence , and references therein).
Because of proximity to the Gulf of Mexico and potential exposure to hurricane-related storm surge and sea level rise, the St. Marks   Table S1; USFWS, 2018a). These ponds were the only ones we were able to measure; assuming other ponds located between these 17 were also inundated, the total number of inundated ponds would be at least 35. Although this water would normally recede within approximately a day, the area in which many of these ponds are located was covered with seawater for at least a week because of an elevated tram road south of the ponds (Figure 1), which impeded the outward flow of water.
From 16 October to 30 November 2018, we measured specific conductance (SpC) using a HydroLab Quanta water quality meter during each visit to each wetland according to standard USGS protocols (USGS, 1997 to present). We report the median of five water quality readings at each site (Table S1). We identified overwashed wetlands by comparing poststorm SpC levels to prestorm levels (before the storm, a single measurement of SpC was taken per site each spring). As defined by Gunzburger et al. (2010) Table S1). For the 17 ponds that were overwashed, conductivity increased by a factor of 11.2-216.7 (mean ± 1 SD = 92.8 ± 65.2) per pond, whereas it only changed by a factor of 0.8-2.0 (mean ± 1 SD = 1.2 ± 0.4) for the remaining 10 ponds that were not overwashed (Table S1) After the hurricane, we opportunistically observed (during systematic trapping and assessments of storm damage) both terrestrial and wetland-associated species and noted their status (alive or dead). We confined our observation period of dead individuals to F I G U R E 3 SLOSH models of maximum surge level during a (a) Category 1 and (  We hypothesize that there will be differences in salamander vital rates across the Refuge: not all wetlands were inundated by storm surge and specific conductance varied among those that were ( Figure 1;

| NEED FOR A PROAC TIVE CLIMATE CHANG E ADAP TATION PL AN
Species' declines and extinctions are predicted to escalate as changes in land-use, climate, and other stressors intensify (Selwood, McGeoch, & Mac Nally, 2015). Many conservation plans focus on the impacts from mean, long-term climatic changes but fail to consider changes in the frequency and intensity of extreme weather and climatic events (Maxwell et al., 2019). Moreover, compared to cli- accommodating options (those that increase flexibility), and retreat options (those that enhance adaptability) (Nicholls et al., 2007). For amphibians in coastal wetlands, appropriate protective actions may include (a) minimizing or eliminating landscape features that are conduits for future inundation by plugging ditches and installing water control structures; (b) restoring habitat and maintaining its suitability using prescribed fire and other tools; and (c) engineering protective structures such as sea walls, flood levees, dikes, culverts, and impoundments for flood abatement Noble et al., 2014). Examples of accommodating actions include (a) enhancing population resilience (e.g., increasing genetic diversity), (b) increasing connectivity among populations, and (c) acquiring land to allow future managed translocations. Although building resilience is fundamental to future conservation of populations in coastal environments, more active planning and management will likely be needed to protect the most vulnerable coastal environments (Fisk, Haines, & Toki, 2017). Meeting this need may require implementing a range of retreat measures, including assisted migration or managed translocation, establishment of ecological corridors, and ex situ conservation (Fisk et al., 2017;Noble et al., 2014).
Of 381  A need to improve preparation for climate change in recovery planning is not unique to the United States; mention of specific actions to address climate change is relatively uncommon in recovery plans in Australia as well (Hoeppner & Hughes, 2018). In part because of the difficulty in keeping recovery plans up-to-date, the U.S.
Fish and Wildlife Service (USFWS) has revised its approach to recovery planning and implementation (USFWS, 2017

| CON CLUS IONS
Globally, coastal wetlands are among those anticipated to be the most severely impacted by climate change because of increased frequency and intensity of coastal storms, as well as increased flooding and secondary salinization from sea level rise (Albecker & McCoy, 2017 For A. cingulatum, reducing vulnerability to hurricanes and related storm surge events will ultimately depend on the existence of resilient, redundant, and representative populations throughout this species' historical range. Both species of flatwoods salamanders are experiencing severe population losses, and, of those that remain, resiliency is likely low to moderate (USFWS, 2019a).
In terms of redundancy, A. cingulatum currently exists only as isolated metapopulations in a few locations within its historical range (Semlitsch et al., 2017).