The goal of this study was to understand past and predict future responses of an aquatic‐obligate species to changes in climate suitability and aquatic connectivity in a vast, arid landscape. To this end, we examined the climate relationships and interpopulation connectivity of the Columbia spotted frog ( Rana luteiventris ) across the Great Basin, the largest (>400,000 km 2 ) desert in North America. The objectives of this study were to (1) quantify the past, recent, and future climate suitability and surface water availability for Columbia spotted frogs at currently occupied locations and across the Great Basin and (2) quantify interpopulation connectivity, based on hydrology and genetic data, as a means to examine potential consequences of changes in the amount and timing of available surface water. If this species' disjunct distribution and observed population declines in the Great Basin are related to climate changes, we expected to find that climate suitability and surface water availability have declined at currently occupied sites and across the Great Basin over the past 100 years. We also expected interpopulation connectivity and gene flow to be (1) related to surface water availability, (2) low between neighboring sites, (3) greater between sites on stream networks than between ponds or between ponds and nearby streams, (4) lower between sites in more distant regions of the Great Basin, and (5) higher through private, rather than federal or state land given that most private lands in the Great Basin occur along valley bottoms where water is available for agriculture. Support for these hypotheses does not necessarily imply a causal link between climate change and the current status of the Columbia spotted frog in the Great Basin, but combining information on climate suitability, surface water availability, and landscape connectivity could provide an important means of examining potential climate change effects on some of the most potentially vulnerable species: amphibians or other aquatic organisms living in arid and semiarid regions of the world.

The ability of amphibians to persist under rapidly changing climate conditions may depend on their ability to disperse to suitable locations. Amphibians are able to exploit both aquatic and terrestrial resources for food, shelter, and travel, and many species move considerable distances (e.g., >1 km) to reach distant habitats (Smith and Green 2005 ). Interpopulation movements facilitate genetic diversity and metapopulation dynamics (Sjögren 1991 ). Exceptionally hot, cold, or dry conditions can preclude the use of certain habitats or limit the use to brief periods when favorable conditions exist (Lemckert et al. 2012 ).

Amphibian species have relatively narrow climate niches (Bonetti and Wiens 2014 ), and changes in temperature and precipitation patterns may influence the life history, and possibly persistence, of some species (Corn 2005 ; Araújo et al. 2006 ; Lowe 2012 ; McCaffery et al. 2012 ; Walls et al. 2013 ). Amphibians depend on sustained moisture (i.e., usually surface water) and optimal temperatures in their environment for successful reproduction and survival. A species' response to climate change likely depends on the specificity of these habitat relationships, as well as adaptive genetic variation within populations (Carey and Alexander 2003 ; Cahill et al. 2013 ; Gerick et al. 2014 ). Species living in desert habitats, for example, are adapted to hot, arid conditions, but some desert environments may become too hot or dry in the near future to allow the species to persist (Gerick et al. 2014 ).

Ongoing and impending changes to Earth's climate have important implications for suitability and connectivity within species' current ranges (Walther et al. 2002 ). Aquatic species living in arid and semiarid regions of the world may experience earlier and more severe consequences of changes in precipitation and temperature because these areas are already water limited and may approach thermal tolerances for some species (Arismendi et al. 2013 ). Although many arid regions are predicted to have warmer temperatures in the near future, predictions for more variability in the amount and timing of precipitation could also be problematic for aquatic species (Hamlet et al. 2005 ; Cayan et al. 2010 ; Walls et al. 2013 ). Such variability is likely to lead to altered stream hydrology and wetland hydroperiods causing connectivity among populations in arid landscapes to decrease during extended drought or possibly increase during periods of deluge. Hence, an understanding of how climate change may affect aquatic species in arid environments is a high priority for conservation of aquatic biodiversity in many parts of the world.

Methods

Study species The Columbia spotted frog is a widely distributed species that once occupied large portions of the Intermountain West, from central Nevada to Alaska. The success of the species may be related to its ability to breed in a variety of freshwater habitats and climates, ranging in elevation from 500 to 3036 m (Reaser and Pilliod 2005). In spite of these broad environmental tolerances, in the southern portion of the species' range (i.e., the Great Basin), Columbia spotted frogs now only persist in disjunct populations. Phylogenetic analyses suggest little gene flow among these isolated remnant populations in the Great Basin, apparently because the intervening habitats have become unsuitable (i.e., warmer, drier, and occupied by nonnative predators) during the present interglacial period (Green et al. 1996; Bos and Sites 2001; Funk et al. 2008). Further, the availability of habitat patches (e.g., water bodies) and corridors connecting them may have declined sharply with widespread trapping of beaver in the 1800s and the diversion of streams and draining of wetlands for agricultural development (Engilis and Reid 1996; Gibson and Olden 2014). These changes have fragmented suitable habitat for Columbia spotted frogs across the Great Basin and likely led to increased isolation of populations as movement of individuals between sites became less frequent, similar to isolating mechanisms observed in the northern part of the species' range (Funk et al. 2005a; Goldberg and Waits 2010). Columbia spotted frogs in the Great Basin are now considered to be a genetically distinct population segment (DPS), isolated from populations in the northern part of the species' range (Funk et al. 2008). The Great Basin DPS is of conservation concern due to the apparent isolation of remnant populations and various threats to their habitats; these conservation issues are not unique to spotted frogs and represent broader issues for aquatic species in the Great Basin and other arid regions of the world (Sada and Vinyard 2002).

Study area The Great Basin encompasses over 400,000 km2 of the western United States and is delineated loosely by endorheic watersheds and phytogeographic provinces. We defined our study area using three Level III Ecoregions (Snake River Plain, Northern Basin and Range, and Central Basin and Range; http://www.epa.gov/wed/pages/ecoregions/level_iii_iv.htm) that included parts of southeastern Oregon, southern Idaho, Nevada, western Utah, and eastern California (Fig. 1). The Great Basin is characterized by basin and range topography with elevations ranging from near sea level to >4,000 m. Low‐elevation areas are dominated by arid and semi‐arid grasslands and shrublands, which transition into piñon‐juniper woodlands and pine‐fir forests at higher elevations. Precipitation typically ranges from 12 to 35 cm, depending on elevation, and falls mainly as winter snow and early spring rain. Summers are hot and dry throughout the region, with average daily high temperatures from 29.8 to 33.8°C in July, also depending on elevation. Figure 1 Open in figure viewer PowerPoint Geographic projections of past (1901–1930), recent (1981–2010), and future (2071–2100) climate suitability for Columbia spotted frogs in the Great Basin (black line). Projections were based on applying a model of breeding location climate to similar data from each time or carbon emission scenario (B1, A1B, and A2; ordered low to high carbon emissions). Each panel uses an equivalent color ramp, with cooler colors indicating lower probability of suitability and warmer colors indicating greater suitability (range = 0–0.97). Points shown in green are current breeding locations (points in Utah were not used in model development).

Climate suitability We used field observations of Columbia spotted frog breeding (i.e., presence of eggs or larvae) combined with 30‐year average monthly temperature and precipitation data for each breeding location to develop a spatially explicit predictive model of the distribution of suitable climates across the Great Basin. Frog observation data were compiled by the U.S. Fish and Wildlife Service (from federal, state, and university studies) for the years 1993 to 2012. To reduce effects of repeat observations made at particular locations (which would result in “spatial pseudo‐replication” and subsequent over‐fitting to areas with a high density of observations) and effects of potential location error associated with early global positioning systems (GPS, precise to within 10–100 m), we buffered each of these observations by 400 m, dissolved overlapping buffers into “breeding complexes” and calculated a centroid coordinate for each complex using ArcMap10.0 (ESRI, Redlands, CA). Buffer distances assume that Columbia spotted frogs can move up to 400–500 m across dry land and that adjacent breeding sites often exchange individuals and function as metapopulations (Engle 2001; Pilliod et al. 2002). We found no difference in mean annual temperature or precipitation conditions between centroid points and the original observation points that contributed to each centroid. The average area of breeding complexes was 69.3 ha (only 1.4% larger than the area encompassed by a single observation buffered by 400 m). This resulted in 151 breeding complex locations (hereafter “breeding locations”) within the Great Basin study area, with 145 in the Great Basin DPS (Great Basin clade) and six assigned to the Utah clade based on genetic analysis of mitochondrial DNA (Funk et al. 2008). Only breeding locations in the Great Basin DPS were used in analyses; however, we extended predictions from models to the entire study area, which included part of the Utah clade. We used 30‐year (1981–2010) average monthly temperature and precipitation data to derive recent climate variables (i.e., 30‐year average temperature and precipitation values for each month of the year resulting in 24 climate parameters) for each breeding location. We rescaled climate data from 800‐m gridded PRISM data (Daly et al. 2002) to 270 m to match the spatial resolution of our other data, resulting in about 6.8 million 270‐m pixels across the Great Basin study area (see Franklin et al. 2013 for discussion of the influence of spatial grain for climate analyses). Multivariate outlier analysis and nonmetric multidimensional scaling (NMS) ordination of recent climate data were conducted (as in Arkle et al. 2014) using PC‐ORD 6.09 software (McCune and Mefford 2011) to identify breeding locations with average Sorenson distances greater than two standard deviations from the overall mean Sorenson distance between locations. Three breeding locations were identified as climatic outliers and were excluded from the input dataset because of potentially disproportionate influence on model outputs (Fig. A1), resulting in 142 breeding locations used in analyses. We used the 24 climate parameters at the 142 breeding locations as input data for a maximum entropy model in MAXENT (version 3.3.3k), a presence‐only modeling framework that is mathematically equivalent to Poisson regression and related to Poisson point process models (Renner and Warton 2013). We used this approach because we did not have reliable “absence” data or survey locations where Columbia spotted frog breeding was not observed. This modeling approach is sensitive to imperfect detection (Lahoz‐Monfort et al. 2014) and sampling biases, particularly from nonrandom sampling (Royle et al. 2012). However, locations where repeat surveys were conducted yielded relatively high (0.89) detection probabilities for adults (Arkle and Pilliod in press) and nearly all breeding locations were obtained from surveys where catchments (and water bodies within them) were randomly selected for sampling rather than convenience sampling (e.g., Wente et al. 2005). Temperature and precipitation data for each month were used, rather than totals or summary variables, because the timing of precipitation or temperature changes was hypothesized to be important for this species. The model was run using auto features and the default regularization scheme with 500 iterations and 10,142 background points. The resulting model output map reflects the probability that the climate in each 270‐m pixel is suitable for Columbia spotted frog breeding based on 1981–2010 climate conditions at known breeding locations. We used Jackknife and permutation tests to measure the importance of each variable (monthly temperature or precipitation) for predicting climate suitability (Fig. A2). We applied this recent climate model to historic (1901–1930) climate data (270‐m downscaled from 800‐m gridded PRISM data; Daly et al. 2002) to assess changes in the distribution of climate suitability within the Great Basin over the past 100 years. This “hindcasting” is based on the assumption that the climate‐space requirements of Columbia spotted frogs in the region have not changed and that they currently have access to and occupy areas at or near climate optima for the species. We used the same approach to predict the distribution of future climate suitability in the Great Basin over the 30‐year period 2071–2100. Future monthly temperature and precipitation data were derived from 16‐model ensemble averages under three carbon emission scenarios: A2, A1B, and B1 (high, medium, and low emission scenarios, respectively; IPCC‐TGICA 2007). Forecasting in this way assumes the species' niche will be conserved across time and that predictions reflect the distribution of that niche (climate suitability) across the landscape under future conditions. These model outputs do not infer probability of occupancy, structural habitat suitability, or persistence. To determine the location and extent of suitable climate in the Great Basin, we applied the final MaxEnt model to the whole study area for each of the five scenarios (i.e., time periods or carbon emission scenarios). We then generated kernel‐smoothed probability density curves (based on all pixels) under each scenario using the “sm” package in R (Bowman and Azzalini 2014; R Development Team, 2014). Probability density curves allowed us to estimate the relative amount of suitable climate for the species across the landscape under each scenario. Results from the recent climate model showed that over 95% of breeding locations were contained in areas having a probability of climate suitability ≥0.20. Consequently, we used 0.20 as a cutoff to define areas as “suitable” in subsequent analyses where a cutoff value was required. To evaluate changes in climate suitability at currently occupied locations only (i.e., not Great Basin‐wide), we compared average monthly temperature and precipitation values under past, recent, and future scenarios only for pixels underlying current breeding locations (n = 142 pixels for each of the five scenarios).

Surface water availability We used Variable Infiltration Capacity (VIC) data (Gao et al. 2010) to quantify surface water runoff in 6‐km pixels across the entire Great Basin for similar time periods as described above. VIC is a spatially explicit, coarse‐scale, surface water hydrologic model that combines gridded land surface modeling approaches with meteorological data. While we recognize the importance of ground water for the hydrology of streams and wetlands, VIC runoff data allowed us to assess at least the relative changes in surface water contributions to streams and wetlands under different scenarios. As VIC data were not available for the exact time periods used for climate modeling, we selected the closest available corresponding year ranges: 1915–1930, 1981–2006, and 2080. Data provided for 2080 were derived from a 10‐year model simulation approach, accounting for annual variability. Consequently, values from the 2080 dataset reflect projected climate conditions on a 10‐year scale, centered around 2080. We calculated monthly average surface runoff values (depth per day, where 1 mm depth = 1 million L/km2) for each time period for all 6‐km pixels in the Great Basin study area. We generated kernel‐smoothed probability density curves for the months of May and September in each time period to quantify changes in the distribution of runoff values throughout the Great Basin. These 2 months were identified by our climate suitability model as the most important hydrologic (i.e., precipitation likely to fall as rain) predictors of spotted frog climate suitability (Fig. A3). To evaluate changes in monthly runoff at currently occupied locations only (i.e., not Great Basin‐wide), we calculated the mean monthly runoff values for each time period at pixels underlying current breeding locations (n = 142 pixels for each of the three time periods).

Connectivity (landscape resistance models) We quantified habitat connectivity between breeding locations using Circuitscape 4.0 (McRae et al. 2014), which employs circuit theory and random walk theory to predict movement across resistance surfaces. Resistance surfaces are developed from information on a species' movement capabilities through a landscape of interest (McRae et al. 2008). We used the best available biological information on the species to create a resistance surface which assumes that Columbia spotted frogs move more easily or frequently through areas (i.e., pixels) nearer to permanent water, half as easily or frequently through areas near intermittent water, and least often through areas far from any water. For example, radio‐telemetry studies in a variety of landscapes have found that Columbia spotted frogs will travel 5–6 km along water courses, but only about 500 m over land depending on habitat moisture and weather conditions (Reaser 1996; Bull and Hayes 2001; Engle 2001; Pilliod et al. 2002; Funk et al. 2005b). We extracted all permanent water bodies in the NHDPlus database (http://nhd.usgs.gov/) and calculated the distance from each 270‐m pixel in the Great Basin to the nearest permanent water. We repeated this process, calculating the distance from each pixel to the nearest intermittent water source and multiplying by 2 to double the resistance under the assumption that intermittent water bodies would be available for use half of the time. We only included intermittent water sources within areas having climate suitability ≥0.20 to avoid over‐predicting movement through unsuitable areas. For each pixel, we took the minimum of those two distance values such that our resulting resistance surface was composed of 270‐m pixels, with the value of each pixel based on the minimum of (1) its distance to the nearest perennial water or (2) twice its distance to the nearest intermittent water. We first modeled connectivity for all 151 breeding locations in the Great Basin using a “one‐to‐all” method where one amp of electrical current is injected into each breeding location iteratively with all others tied to ground. This analysis depends on the particular sites included for analysis because current flows from a single site to (potentially) all 150 other sites in each iteration. Current values were recorded for each pixel in each iteration, and cumulative current flow was mapped across the landscape. We included six sites in the Utah genetic group for reference.