Abstract

Many cave-roosting bats are declining in number throughout their range because of multiple threats, including disease, disturbance by humans, and habitat loss. Successful conservation of cave-roosting bats requires an understanding of the roles of microclimate, cave structure, and the surrounding landscape on the distribution and abundance of bats, and in particular, the use of winter cave roosts. Cave bats have been well studied in temperate climates, but we know little about these bats in subtropical climates. From 2015 to 2017, we conducted 399 winter surveys of 162 caves in Florida to evaluate factors affecting the presence and abundance of bats at cave roosts. We also determined whether temperatures at these cave roosts were suitable for Pseudogymnoascus destructans, the fungus that causes white-nose syndrome. Across all 3 y, we detected three species of bats: tricolored bat Perimyotis subflavus in 126 (77.8%) caves, southeastern myotis Myotis austroriparius in 51 (31.5%) caves, and a single Rafinesque's big-eared bat Corynorhinus rafinesquii. We analyzed the presence of both tricolored bats and southeastern myotis in caves by using mixed-effects models with a binomial distribution and the number of tricolored bats by using generalized linear mixed-effects models with a Poisson error distribution. Tricolored bat presence was significantly and positively influenced by a cooler cave surface temperature, larger cave entrance size, a single entrance, and the presence of solution holes. Tricolored bat abundance increased in longer, cooler caves that had solution holes, a single, unobstructed entrance, and had no signs of flooding. Southeastern myotis presence was positively associated with longer, domed caves. To be most effective, conservation efforts in subtropical climates should focus on caves with the identified characteristics. More than 90% of caves surveyed each year had a cave interior surface temperature below the upper critical growth limit for P. destructans (19.8°C), indicating that most Florida caves are suitable for growth of P. destructans. Therefore, regular monitoring of winter bat populations in subtropical caves may be important for detecting P. destructans and white-nose syndrome.

Introduction

More than half of North America's 47 bat species hibernate in caves; these caves enable them to maintain a stable, low body temperature that reduces energy demands during times of limited prey availability (Perry 2013). Caves provide stable, above-freezing temperatures and high humidity, representing ideal conditions for successful torpor (Speakman and Thomas 2003) and necessary conditions for survival in temperate regions. Factors known to affect the selection of caves for winter roosts by bats differ by species and region (Raesly and Gates 1987; Briggler and Prather 2003; Dixon 2011). For bats in temperate caves, variations in microclimate seem to be the main driver of roost selection because of the effects of temperature and humidity on energy costs and water loss and therefore on overwinter survival (Speakman and Thomas 2003). However, bats in subtropical regions, such as the southeastern Coastal Plain of North America (Bailey 1994), may not face the same pressures in selecting a winter roost.

Caves in the southeastern Coastal Plain are climatically and physically distinct from temperate region caves that occur at higher latitudes and elevations. This region has a shorter, warmer winter where insects are available prey for bats on most nights (Frost 1962; McNab 1974; Perry 2013). In addition, southeastern Coastal Plain caves are structurally distinct, because they are formed by conduit and diffuse groundwater flow that is rare elsewhere, and the karst is young and highly porous, which may correspondingly impact temperature stability, humidity, and bat roost site use (Florea and Vacher 2009). Because of the unique conditions found in this region, we hypothesize that cave microclimate may not be as strong of a predictor of use by bats. Instead, the physical structure of the cave and the surrounding landscape may play a larger role.

Understanding how bats select cave roosts is increasingly important as white-nose syndrome (WNS), a disease caused by the fungus Pseudogymnoascus destructans, spreads across North America (U.S. Fish and Wildlife Service [USFWS] 2020). White-nose syndrome causes extensive mortality in some cave bat populations by disrupting hibernation and hydration cycles, causing individuals to arouse more frequently and deplete crucial fat reserves (Frick et al. 2010, 2015; Lorch et al. 2011; Warnecke et al. 2012). Conditions in the cave and surrounding landscape can influence the spread of P. destructans and affect the rate of mortality caused by WNS (Flory et al. 2012; Langwig et al. 2012, 2016; Verant et al. 2012; Johnson et al. 2014; Hayman et al. 2016). By developing a pre-WNS baseline evaluation of bat use of winter roost caves in subtropical regions, biologists can improve regional management plans to evaluate disease impacts to bat populations, track the spread of the disease, and develop mitigation plans.

Although much research has been conducted on hibernating bats in temperate climates (Rabinowitz 1981; Gates et al. 1984; Raesly and Gates 1987; Briggler and Prather 2003; Boyles et al. 2007; Brack 2007), a full evaluation of the use of caves by wintering bats in the subtropical southeastern Coastal Plain is lacking, perhaps because of the smaller size and warmer temperatures of the caves and the shorter, less intensive period of hibernation (McNab 1974; Gore et al. 2012). Historically, three species of bats in Florida use caves during the winter (McNab 1974): the tricolored bat Perimyotis subflavus, the southeastern myotis Myotis austroriparius, and the gray bat Myotis griescens. Tricolored bats have the most extended torpor period of the three species, whereas southeastern myotis may forage throughout winter when conditions are favorable (McNab 1974). Federally endangered gray bats (ESA 1973, as amended; U.S. Office of the Federal Register 1976) formerly hibernated in two caves in Florida, but with significantly declining numbers in recent years, they now seem to be absent from the state (Gore et al. 2012). Research shows that all three bat species are likely to be susceptible to P. destructans and thus potentially WNS in temperate areas (USFWS 2020). Although WNS has not yet been detected in Florida, the disease has been found in wintering bats north of the coastal plain in both bordering states (Georgia and Alabama; USFWS 2020).

For this study, we evaluated factors affecting presence and abundance of wintering bats at cave roosts in subtropical Florida. This information may be useful for identifying caves that are important for conserving populations of wintering bats across the southeastern Coastal Plain. We also determined whether the temperature in Florida caves during winter was suitable for the growth of P. destructans. Knowing whether subtropical caves are suitable for P. destructans allows biologists to better predict the potential spread of WNS to cave-roosting bats within this region.

Study Site

We reviewed data compiled by caving organizations, reports from landowners, and published papers to estimate that there are approximately 600 caves in Florida with dry passages (i.e., not fully submerged) that are potentially suitable for roosting bats. These caves are concentrated in three karst areas in northwest, north central, and extreme southeast Florida (Florea and Vacher 2009). We surveyed caves in the northwest (Jackson and Washington counties) and north central (Alachua, Citrus, Gilchrist, Levy, Marion, and Sumter counties) regions of the state (Figure 1), because they contain the greatest number of caves and support the largest populations of wintering bats. We excluded caves in southeast Florida because they are small and highly disturbed (Cunningham and Florea 2009), and we know of no records of bat use. Caves in both north Florida study areas occurred most frequently in upland hardwood, mixed wetland–hardwood, and mixed hardwood–coniferous forest habitats (FNAI 2010). The mean high temperature during northwest Florida winters (1 December–1 March) is 18.6°C, with temperatures falling below 0°C an average of 29 d/y (measured at the Tallahassee weather station; NOAA 2020). In north central Florida, the mean high temperature during winter is 20.9°C, with temperatures falling below 0°C an average of 16 d/y (measured at the Gainesville weather station; NOAA 2020).

Figure 1.

Study area comprising eight counties in northwest and north central Florida where caves were surveyed for bats in winter. Numbers indicate the number of caves in each county that were surveyed at least once from 1 January to 1 March for 2015, 2016, and 2017.

Figure 1.

Study area comprising eight counties in northwest and north central Florida where caves were surveyed for bats in winter. Numbers indicate the number of caves in each county that were surveyed at least once from 1 January to 1 March for 2015, 2016, and 2017.

Methods

Cave surveys

We selected caves for survey in three ways: known history of bat use, location nearby a known bat cave, or location selected at random. In 2015, we visited 24 caves that had current or historical records of bat use (McNab 1974; Gore and Hovis 1998; J.A.G. unpublished data) and 86 caves without bat records located on the same properties or nearby (<3 km). We repeated surveys of the original 110 caves in the two subsequent years, except when high water levels or landowner directives prevented access (5 caves in 2016 and 11 caves in 2017). In 2016 and 2017, we surveyed 42 caves selected at random to determine whether we missed some caves used by bats and to reduce potential bias caused by our original cave survey selection method. We selected random caves by placing a grid of 1-km2 cells over all areas containing known caves with dry passageway in northwest and north central Florida in ArcGIS 10.2 (ESRI, Redlands, CA). Next, we randomly selected 15 cells and surveyed all caves within each cell if we had access to and could locate the caves. We also surveyed 2 additional caves in 2016 and 17 caves in 2017 that were encountered incidentally during fieldwork or had historical records of bat use, but were previously inaccessible to us.

We surveyed caves between 1 January and 1 March of each year. During each survey, we systematically searched for bats in all accessible portions of the cave and identified the species of each bat observed. To determine abundance, we either counted each individual bat or estimated the number of bats in large clusters (>100 individuals) by estimating the area covered by the bat cluster in square meters and multiplying by 2,000 bats/m2 (Gore and Hovis 1998). To reduce disturbance to the bats, we used red lights, minimized noise, and limited the time spent inside a cave. To minimize the potential risk of transferring P. destructans between caves, we followed the recommended decontamination protocols (WNS DMWG 2020).

For each cave, we recorded values for 16 variables related to conditions inside the cave or outside the cave entrance (Table 1). We calculated a single representative temperature for each cave by averaging the interior surface temperature of two opposing walls (∼1.5 m above the ground) and the center of the ceiling near the highest concentration of bats roosting in each cave by using a Fluke 62 Max IR thermometer with a National Institute of Standards and Technology–traceable calibration certificate (Fluke Corporation, Everett, WA). If no bats were present, we measured surface temperatures in the largest room of the cave that was greater than 20 m from the cave entrance or near the back of caves less than 20 m long. We did not collect temperatures from 13 caves in 2015, 4 caves in 2016, and 1 cave in 2017. Because humidity is high in all Florida caves and difficult to reliably and precisely measure, we did not record humidity. We measured cave entrance width and height at the widest points with a Leica DISTO E7100i laser distance meter (Leica Geosystems, St. Gallen, Switzerland) and calculated entrance area post hoc. We measured cave length with the laser distance meter or obtained the length from an existing cave map. We grouped cave length as either short (<60 m) or long (>60 m) because of the difficulty in obtaining accurate distances of longer, more complex caves. We measured variables expected to vary over time during each visit to a cave (Table S1, Supplemental Material), but we measured variables expected to remain constant (e.g., entrance size, number of entrances) only on the first visit (Table S2, Supplemental Material). We measured landscape-level physiographic variables by using the Florida Natural Areas Inventory Cooperative Land Cover, Version 3.1 layer (FNAI 2010) in ArcGIS.

Table 1.

Variables recorded for each cave surveyed for bats in north Florida from 1 January to 1 March for 2015, 2016, and 2017, along with a brief description of the measurement of each variable. Variables are grouped as either constant or temporally variable and by whether they were measured inside the cave (internal), outside the entrance (external), or as an element of the landscape around the entrance. Type indicates whether the variable was categorized as binary, continuous, or categorical for statistical analyses.

Variables recorded for each cave surveyed for bats in north Florida from 1 January to 1 March for 2015, 2016, and 2017, along with a brief description of the measurement of each variable. Variables are grouped as either constant or temporally variable and by whether they were measured inside the cave (internal), outside the entrance (external), or as an element of the landscape around the entrance. Type indicates whether the variable was categorized as binary, continuous, or categorical for statistical analyses.
Variables recorded for each cave surveyed for bats in north Florida from 1 January to 1 March for 2015, 2016, and 2017, along with a brief description of the measurement of each variable. Variables are grouped as either constant or temporally variable and by whether they were measured inside the cave (internal), outside the entrance (external), or as an element of the landscape around the entrance. Type indicates whether the variable was categorized as binary, continuous, or categorical for statistical analyses.

Data analysis

To evaluate cave variables affecting presence of tricolored bat and southeastern myotis, we used mixed-effects models with a binomial distribution and logit link function by L1-penalized estimation with the glmmLasso package in program R (R Core Team 2014; Schelldorfer et al. 2014). We fit separate models for tricolored bat and southeastern myotis presence, where the dichotomous dependent variable was presence or the lack of presence by bats. To evaluate cave variables affecting tricolored bat abundance, we used generalized linear mixed-effects models with a Poisson error structure by L1-penalized estimation with the glmmLasso package (Schelldorfer et al. 2014). We could not evaluate variables affecting the abundance of southeastern myotis because three caves had more than 1,000 bats, one of which had approximately 45,000 individuals, and all other caves had fewer than 100 bats. For all models, we determined the optimal tuning parameter, lambda, by evaluating Akaike's Information Criterion at a sequence of values, where estimates of the previous fit were used as starting values for the next fit (Schelldorfer et al. 2014).

Fixed effects included binary variables of disturbance, obstruction, presence of standing water, presence of flooding, entrance orientation, presence of domed ceilings, presence of solution holes, number of entrance areas (one or multiple), and cave length (short or long; Table 1). Continuous covariates included cave temperature (°C), entrance cross-sectional area (m2), distance to nearest bat cave (km), distance to nearest permanent body of water (km), distance to nearest open (nonforested) area (km), and Julian date (Table 1). We used variance inflation factors to evaluate multicollinearity of continuous variables within the model. We removed Julian date from further analysis because it exhibited a high correlation with other continuous variables in the model, resulting in convergence issues and variance inflation factors above a common threshold (>5). We retained all other variables in the full model because they exhibited low correlation (variance inflation factor <2). We included a unique cave identification variable (cave ID) as a random effect in the model to control for possible dependence. We validated models by assessing residual plots.

Results

We conducted 399 surveys of 162 caves, including 85 caves in northwest Florida and 77 in north central Florida (Figure 1). We surveyed 102 caves in all 3 y, 33 caves in 2 y, and 27 caves only once. Of these caves, there was an association with known history of bat use and the highest proportion of occupied caves for both species (Table 2). Tricolored bat presence was lower in caves nearby those with a known history of bat use and in randomly selected caves, but all categories had greater than 70% occupied caves. The presence of southeastern myotis in caves nearby those with a known history of bat use or caves selected randomly was about one-third the proportion of caves with a known history of bat use.

Table 2.

Number of caves selected by each of the three methods and the number and percentage of caves occupied by bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.

Number of caves selected by each of the three methods and the number and percentage of caves occupied by bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.
Number of caves selected by each of the three methods and the number and percentage of caves occupied by bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.

We detected tricolored bats in 126 (78%) caves, but only 53 (52%) of the caves surveyed in all 3 y had bats in every year. Few caves (n = 28; 17%) had more than 10 tricolored bats in any year; however, eight of these caves contained more than 40 tricolored bats in at least 1 y. Only two of these caves that had more than 40 bats in every year, and these two caves also each had more than 130 tricolored bats in every year. In 2015, we recorded the highest total number of tricolored bats (1,049) and the highest number in a single cave (220; Table 3).

Table 3.

Number of caves surveyed, caves occupied by bats, and individual bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.

Number of caves surveyed, caves occupied by bats, and individual bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.
Number of caves surveyed, caves occupied by bats, and individual bats, by species (tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius), in winter across north Florida from 1 January to 1 March for 2015, 2016, and 2017.

We detected southeastern myotis in 51 (32%) caves, but not in all 51 caves each winter. Of the caves surveyed in all 3 y, southeastern myotis occupied only 11 (11%) of the caves in all 3 y. Total numbers of southeastern myotis recorded in a year varied greatly from 1,230 in 2015 to more than 48,690 in 2016 (Table 3). The number of southeastern myotis observed varied widely across caves and within years, from single individuals to a colony of approximately 45,000 bats in 2016. Most winter colonies were small (median = 5), with only seven caves containing more than 100 bats in at least 1 y and only three of these caves containing more than 1,000 bats in at least one winter. No caves in 2015 contained more than 1,000 bats, but two caves had more than 1,000 bats in both 2016 and 2017 and a third cave had more than 1,000 bats in 2017.

We observed both tricolored bats and southeastern myotis in 44 caves (27%), whereas we observed only tricolored bats in 84 (52%) of the caves and only southeastern myotis in 7 (4%) of the caves. We documented a single Rafinesque's big-eared bat Corynorhinus rafinesquii, but we did not observe any gray bats. In 27 (17%) caves, we found no bats in any year.

The L1-penalized model selection (Lasso regression) on the presence of tricolored bats resulted in support for four predictors describing bat presence (Table 4). Tricolored bats were more likely to occupy cooler caves with solution holes and with a larger cave entrance size and greater distance to the nearest permanent body of water. Tricolored bats were less likely to be present in caves with two or more entrances. Variation across caves within the model resulted in a standard deviation (SD) of 0.32 for the random effect.

Table 4.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for solution holes are false = 0 and true = 1 and for number of entrances are one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for solution holes are false = 0 and true = 1 and for number of entrances are one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.
Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for solution holes are false = 0 and true = 1 and for number of entrances are one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.

Lasso regression for abundance of tricolored bats retained 13 predictors, of which 6 have strong effects in describing bat abundance (Table 5). Longer caves, with a single entrance, and solution holes had higher abundances of tricolored bats. In addition, tricolored bat abundance had a negative relationship with flooding, entrance obstructions, and higher cave temperatures. The SD for the random effect of caves was 1.29.

Table 5.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus abundance in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for disturbance, obstruction, and standing water are no presence = 0 and presence = 1. Codes are as follows: entrance orientation, horizontal = 0 and vertical = 1; domed and solution, false = 0 and true = 1; cave length, long = 0 and short = 1; and number of entrances, one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus abundance in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for disturbance, obstruction, and standing water are no presence = 0 and presence = 1. Codes are as follows: entrance orientation, horizontal = 0 and vertical = 1; domed and solution, false = 0 and true = 1; cave length, long = 0 and short = 1; and number of entrances, one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.
Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing tricolored bat Perimyotis subflavus abundance in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for disturbance, obstruction, and standing water are no presence = 0 and presence = 1. Codes are as follows: entrance orientation, horizontal = 0 and vertical = 1; domed and solution, false = 0 and true = 1; cave length, long = 0 and short = 1; and number of entrances, one entrance = 0 and multiple entrances = 1. Continuous variables underwent standardization before analysis.

Results of the Lasso regression for southeastern myotis presence retained only two supported predictors (Table 6), with the variation across caves being 0.24 (SD). Southeastern myotis were more likely to be present in longer caves with domed rooms.

Table 6.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing southeastern myotis Myotis austroriparius presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for domed are false = 0 and true = 1 and cave length are long = 0 and short = 1. Continuous variables underwent standardization before analysis.

Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing southeastern myotis Myotis austroriparius presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for domed are false = 0 and true = 1 and cave length are long = 0 and short = 1. Continuous variables underwent standardization before analysis.
Parameter estimate (β), standard error (SE), and P value for mixed-effects model describing southeastern myotis Myotis austroriparius presence in 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017. Codes for domed are false = 0 and true = 1 and cave length are long = 0 and short = 1. Continuous variables underwent standardization before analysis.

Cave wall and ceiling temperatures varied by year, but more than 90% of the caves had temperatures below the upper critical growth limit for P. destructans (19.8°C; Verant et al. 2012) in each year (Table 7). Furthermore, in 2016 and 2017, 79.2 and 82.5% of the caves surveyed, respectively, had temperatures within the optimal range for growth of P. destructans (12.5–15.8°C; Verant et al. 2012). Caves occupied by tricolored bats were cooler (13.0 ± 4.4°C) than unoccupied caves (15.0 ± 4.4°C), whereas caves occupied by southeastern myotis were warmer (14.3 ± 4.4°C) than unoccupied caves (13.5 ± 4.6°C; Figure 2), but there was significant overlap for both species.

Table 7.

Temperatures recorded in Florida caves during surveys conducted from 1 January to 1 March for 2015, 2016, and 2017 and conditions for growth of Pseudogymnoascus destructans (Pd). Surveys occurred at 162 caves that were surveyed over 1–3 y, depending on accessibility. Temperature was not recorded during 18 surveys.

Temperatures recorded in Florida caves during surveys conducted from 1 January to 1 March for 2015, 2016, and 2017 and conditions for growth of Pseudogymnoascus destructans (Pd). Surveys occurred at 162 caves that were surveyed over 1–3 y, depending on accessibility. Temperature was not recorded during 18 surveys.
Temperatures recorded in Florida caves during surveys conducted from 1 January to 1 March for 2015, 2016, and 2017 and conditions for growth of Pseudogymnoascus destructans (Pd). Surveys occurred at 162 caves that were surveyed over 1–3 y, depending on accessibility. Temperature was not recorded during 18 surveys.
Figure 2.

Temperatures (°C) of unoccupied and occupied caves by (a) tricolored bats Perimyotis subflavus and (b) southeastern myotis Myotis austroriparius during 381 surveys conducted in Florida from 1 January to 1 March for 2015, 2016, and 2017.

Figure 2.

Temperatures (°C) of unoccupied and occupied caves by (a) tricolored bats Perimyotis subflavus and (b) southeastern myotis Myotis austroriparius during 381 surveys conducted in Florida from 1 January to 1 March for 2015, 2016, and 2017.

Discussion

We found that tricolored bats occupied more caves during winter than was previously known and that this is the most commonly detected cave bat species in subtropical Florida caves. Tricolored bats were present in almost 90% of caves with current or historical bat use, but bats selected more than 70% of caves at random for occupation. Via extrapolation of this rate to Florida's 600 dry caves, approximately 420 caves may be used by tricolored bats in winter. This large number of caves potentially used by tricolored bats in Florida could pose management challenges because protecting all winter roosts from human disturbance is not feasible. However, roosting in small numbers in numerous caves might be advantageous from a conservation perspective because impacts from disease, disturbance, or flooding at any single cave would have less impact on the total population.

Although tricolored bats occupied 131 of the Florida caves that we surveyed, just 7 caves (5%) contained more than 50% of the winter tricolored bat population. This finding is consistent with those of studies in temperate regions where tricolored bats were found to be the species most likely to be present in caves during winter, but usually occurred in small numbers (≤40 bats per cave; Gates et al. 1984; Raesly and Gates 1987; Briggler and Prather 2003; Dixon 2011). In some areas of their range, tricolored bats have been found in much larger numbers (>1,000 bats per winter roost; Carpenter 2017; Meierhofer et al. 2019), but we do not know why tricolored bats in Florida caves do not occur in larger numbers, because long caves that host many (>40) tricolored bats do not seem to lack available roost sites that could accommodate additional bats. In the southeast where winter is less severe, tricolored bats may be less dependent on cave roosts and may also roost in culverts (Meierhofer et al. 2019), bridges, and tree roosts (Newman 2020) that would normally be unsuitable in temperate climates.

Southeastern myotis occupied fewer caves than tricolored bats. Southeastern myotis were most likely to be present in caves with current or historical bat use, probably because of their status as known maternity caves. We detected southeastern myotis in caves without known bat use approximately 19% of the time, indicating that more than 110 Florida caves may be used by southeastern myotis in winter. Colony size was smaller in caves with no known history bat use (0–50 bats), indicating that most large colonies have been previously identified.

In two of the 3 y, we found more than 90% of southeastern myotis in just two caves. Twelve of the caves we surveyed in winter support large (i.e., >10,000 individuals) maternity colonies in summer (Gore and Hovis 1998; J.A.G. unpublished data). However, we found that only three of those maternity caves contained more than 1,000 bats in at least one winter and that the number of bats fluctuated dramatically between years, confirming that most southeastern myotis disperse from maternity caves to alternate winter roosts (Rice 1957; Harvey et al. 1999). Caves may be important to winter survival of southeastern myotis in the northern, temperate portion of their range (Barbour and Davis 1969); however, in the southern, subtropical region, roosts such as buildings, bridges, and tree cavities probably host a large percentage of the winter population (Rice 1957; Humphrey and Gore 1992; Clement and Castleberry 2013; Fleming et al. 2013). Consequently, long-term management of southeastern myotis needs to focus on both cave roosts and other winter roost sites to successfully protect the species.

Despite our extensive surveys, we observed only one Rafinesque's big-eared bat, which confirms that Rafinesque's big-eared bats rarely roost in Florida caves (Smith et al. 2017). Rafinesque's big-eared bats are known to use caves in the northern, temperate portion of their range (Hurst and Lacki 1999); however, in subtropical Florida, they probably use tree cavities, abandoned buildings, and bridges as winter roosts (Clement and Castleberry 2013; Fleming et al. 2013; Smith et al. 2020). During all 3 y, we surveyed both historical gray bat hibernacula, but we did not observe gray bats in these caves or any others. Gray bats were last observed in Florida caves in 2011 (Gore et al. 2012), and our study confirms that gray bats have probably been extirpated from the state.

In temperate regions, researchers hypothesize that cave microclimate has the largest impact on roost selection (Speakman and Thomas 2003), but the ideal temperature for hibernating bats varies with species and latitude (Perry 2013). In temperate regions, caves with temperatures ranging from 7.6 to 11°C harbored tricolored bats (Rabinowitz 1981; Raesly and Gates 1987; Brack 2007; Johnson et al. 2016). In Florida's subtropical climate, we found the average temperature of an occupied cave was 13.0°C. However, 32 occupied caves in our study had interior surface temperature higher than 18°C, including one cave that reached 22°C, indicating they are probably unsuitable sites for bats to enter torpor (McNab 1974). We found a negative association between presence and abundance of tricolored bats and an increase in temperature, indicating that most bats avoid warmer caves wherein torpor may not be possible. For southeastern myotis, we found that temperature was not a significant determinant of cave use. Our finding is consistent with the conclusion of McNab (1974) that southeastern myotis remain active and forage throughout the winter in subtropical environments and do not rely on torpor to preserve energy.

Our results show that features that increase cave roost site diversity by forming a variety of microclimates, such as solution holes and rooms with domed ceilings, positively influenced presence and abundance of tricolored bats and the presence of southeastern myotis in winter roost caves. Solution holes and domed ceilings can trap body heat or stabilize environmental conditions (Zinn 1977; Churchill et al. 1997), with the size and location of these features creating different microclimatic conditions within the cave (Brunet and Medellín 2001). Cave length was associated with increased abundance of tricolored bats and higher presence of southeastern myotis, possibly because shorter caves experience more fluctuation in cave temperature, varying with external climatic conditions (Perry 2013; Boyles et al. 2017). Longer caves also offer a greater range of microhabitats and a wider variety of temperatures for roosting. The temperature an individual bat selects for hibernation varies by sex (Jonasson and Willis 2011) and body condition (Boyles et al. 2007) and may change throughout the winter (Brack 2007). Therefore, longer caves with solution holes and domes increase the variety of temperatures within the cave, allowing bats to seek specific temperatures and shift locations within a cave throughout the winter (Tuttle and Taylor 1998; Briggler and Prather 2003; Boyles et al. 2017). Unlike in subtropical Florida where cave length only influenced tricolored bat abundance, in temperate regions both presence and abundance were positively associated with cave length (Briggler and Prather 2003; Dixon 2011). The external climate in subtropical regions is mild and may allow bats to occupy caves that would otherwise reach unsuitably cold conditions in a temperate climate.

Although cave length was associated with an increase in tricolored bat abundance, it did not impact presence. Short caves (<60 m) are abundant in Florida (79% of caves we surveyed), and we observed 49.7% of the wintering tricolored bats in short caves. Each occupied short cave contained only a small number of bats, but the cumulative number of tricolored bats in all short caves is significant and needs to be considered when making management decisions. It is unclear whether tricolored bats roosting in short caves only rely on these caves when longer caves are not available nearby or whether there is limited suitable roost site availability within these longer caves to support more bats, but this does not seem to be true in our experience as there appears to be space for additional roosting bats. Alternatively, short caves probably have more variable cave temperatures (Perry 2013) that may increase the frequency and duration of arousals, which may be ideal for bats with higher energy reserves, male bats, and juveniles to avoid potential negative consequences of deep torpor (Czenze et al. 2017). Bats may also use shorter caves intermittently if they are switching roosts between caves or between caves and alternative roosts (e.g., culverts, trees). Further research into roost-switching behavior is necessary to determine the extent of this behavior, but we were unable to address this issue because we only conducted surveys once a year to limit disturbance.

Cave entrance size and entrance number had a significant effect on tricolored bat presence and abundance in Florida caves. Tricolored bat presence increased in caves with a single large entrance and abundance increased in caves with a single, unobstructed entrance. Single large-entrance caves may have a cooling effect on the cave temperature as more cold air moves into the lower portions of the cave, forcing air warmed by the cave walls to exit near the ceiling and resulting in cooler temperatures more conducive to torpor (Perry 2013). Conversely, the increased airflow caused during this cooling process may have a desiccating effect (Tuttle and Stevenson 1978; Perry 2013). Entrances obstructed by excessive vegetation or breakdown decreased tricolored bat abundance. In addition to potentially modifying airflow, obstructed entrances may impact movement of bats and increase predation risk.

Tricolored bat abundance decreased in caves that show signs of sustained flooding on the inside of the cave walls, indicating possible avoidance or historical colony loss. In winter 2017, we documented the loss of hundreds of southeastern myotis due to flooding. In 2018, flooding at one of the main hibernacula caves for tricolored bats resulted in an estimated loss of 20% of the total winter cave population in Florida. Historically, both in Florida and globally, similar losses have been observed (O'Shea et al. 2016) and colony recovery is slow or nonexistent (J.A.G. unpublished data).

Landscape-level variables did not affect the presence or abundance of tricolored bats or southeastern myotis. Distance to permanent water may not have been significant because water sources are common in karst regions of Florida, and temporary or small water sources are not represented in data used in the analysis. Distance to open habitat, meant to portray foraging areas along the forest edge, was not significant, possibly because it did not accurately reflect ideal foraging habitats for either species. The presence of nearby cave roosts did not impact bat use, possibly because of the wide availability of potential cave roosts and suitable roosts in trees, culverts, and buildings (Meierhofer et al. 2019; Newman 2020).

Despite Florida's subtropical climate, most caves had a temperature that could support the growth of P. destructans, indicating that wintering bats of the southeastern Coastal Plain are at risk of exposure. Cave temperature also effects the severity of WNS, with bats hibernating in cooler, drier caves experiencing lower mortality rates (Langwig et al. 2012, 2016; Johnson et al. 2014; Hayman et al. 2016). For example, Johnson (2014) noted that bats hibernating at 4°C had increased survival rates compared with bats hibernating at 10°C in laboratory tests. In Florida, cave temperatures rarely (n = 5) fall to 4°C. Thus, warm caves in subtropical areas may not enable bats to achieve the necessary energy savings through deeper torpor to increase survival if infected by P. destructans. Alternatively, infection by WNS results in increased activity outside the hibernacula (Bernard and McCracken 2017); therefore, warmer cave temperatures and winter weather may allow bats to improve survival through increased energy savings when arousing, shorter winters requiring lower fat reserves, and access to prey to supplement reserves during winter. Long-term data on ambient winter temperatures outside caves and within caves will help biologists evaluate the potential susceptibility of bats roosting in Florida caves to P. destructans and WNS. Additional research after the onset of WNS is necessary to determine how bat survival and behavior are affected by the disease in a subtropical climate with relatively short and mild winters.

Because subtropical caves and bats are susceptible to infection by P. destructans based on cave temperatures, regular population monitoring and disease surveillance throughout the southeastern Coastal Plain are essential to allow biologists to track the spread of the disease and evaluate impacts on bat populations. Although tricolored bats are more abundant in long caves, studies should include short caves in any long-term monitoring plan because they are more common than long caves and cumulatively support a large percentage of wintering tricolored bats. The widespread use of short caves across the landscape by tricolored bats may increase their resilience and lessen potential impacts from WNS that could devastate a single, large colony, but further research is needed after the onset of infection to confirm this hypothesis.

Caves used as a winter roost for bats in the subtropical Coastal Plain of North America exhibit some differences from caves in temperate regions. Although cave temperature is important to tricolored bats in Florida and in temperate regions, this does not hold true for southeastern myotis, who were not associated with a specific temperature profile. Unlike in temperate regions, cave length did not influence tricolored bat presence, which is probably due to a milder climate; but consistent with temperate region caves, longer caves increased the presence of southeastern myotis and abundance of tricolored bats. To maintain populations of tricolored bats in subtropical regions, we recommend protecting caves that have an increased likelihood of presence and increased abundance (cool caves that are not prone to flooding and have a single, large, unobstructed entrance and multiple solution holes). For southeastern myotis, we recommend continued monitoring and management of long, domed caves, some of which are also important maternity roosts, and identifying important winter roosts outside of caves.

Supplemental Material

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article.

Table S1. All cave data collected corresponding to temporally variable covariates during 399 surveys of 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017 and used in the analysis of tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius presence and tricolored bat abundance.

Found at DOI: https://doi.org/10.3996/JFWM-20-078.S1 (46 KB XLSX).

Table S2. All cave data collected corresponding to constant covariates of 162 caves across north Florida from 1 January to 1 March for 2015, 2016, and 2017 and used in the analysis of tricolored bat Perimyotis subflavus and southeastern myotis Myotis austroriparius presence and tricolored bat abundance.

Found at DOI: https://doi.org/10.3996/JFWM-20-078.S1 (46 KB XLSX).

Reference S1. Bailey RG. 1994. Ecoregions of North America. Washington, D.C.: U.S. Department of Agriculture, Forest Service.

Found at DOI: https://doi.org/10.3996/JFWM-20-078.S2 (2.41 MB JPG).

Reference S2. [WNS DMWG] White-Nose Syndrome Disease Management Working Group. 2020. National white-nose syndrome decontamination protocol. U.S. Fish and Wildlife Service.

Found at DOI: https://doi.org/10.3996/JFWM-20-078.S3 (1.8 MB PDF).

Acknowledgments

We thank Emily Evans, Blair Hayman, John Mayersky, Jonathan Mays, Kristy Mobley, Allen Mosler, Kevin Oxenrider, Buford Pruitt, Renee Ripley, Beth Stevenson, and Megan Wallrichs for assistance in the field. We are also grateful for the support and advice provided by Chris Hawthorne, Mark Ludlow, and Daniel Pearson of the Florida Park Service and Colleen Werner of the Florida Forest Service. We especially thank all of the landowners who kindly allowed us access to caves on their property. We also thank the Associate Editor and reviewers for their insightful comments that helped strengthen this manuscript. This research was funded by the Florida Nongame Wildlife Trust Fund and the USFWS.

Any use of trade, product, website, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government.

References

Bailey
RG.
1994
.
Ecoregions of North America
.
Washington, D.C
.:
U.S. Department of Agriculture, Forest Service (see Supplemental Material, Reference S1)
.
Barbour
RW,
Davis
WH.
1969
.
Bats of America
.
Lexington
:
University Press of Kentucky
.
Bernard
RF,
McCracken
GF.
2017
.
Winter behavior of bats and the progression of white-nose syndrome in the southeastern United States
.
Ecology and Evolution
7
:
1487
1496
.
Boyles
JG,
Boyles
E,
Dunlap
RK,
Johnson
SA,
Brack
V
Jr.
2017
.
Long-term microclimate measurement add further evidence that there is no “optimal” temperature for bat hibernation
.
Mammalian Biology
86
:
9
16
.
Boyles
JG,
Dunbar
MB,
Storm
JJ,
Brack
V
Jr.
2007
.
Energy availability influences microclimate selection of hibernating bats
.
Journal of Experimental Biology
210
:
4345
4350
.
Brack
V
Jr.
2007
.
Temperatures and locations used by hibernating bats, including Myotis sodalis (Indiana bat), in a limestone mine: implications for conservation and management
.
Environmental Management
40
:
739
746
.
Briggler
JT,
Prather
JW.
2003
.
Seasonal use and selection of caves by the eastern pipistrelle bat (Pipistrellus subflavus)
.
American Midland Naturalist
149
:
406
412
.
Brunet
AK,
Medellín
RA.
2001
.
The species-area relationship in bat assemblages in tropical caves
.
Journal of Mammalogy
82
:
1114
1112
.
Carpenter
GM.
2017
.
Bat population status and roost selection of tri-colored bats in the Great Smoky Mountains National Park in the era of white-nose syndrome. Master's thesis
.
Knoxville
:
University of Tennessee
.
Churchill
S,
Draper
R,
Marais
E.
1997
.
Cave utilization by Namibian bats: population, microclimate, and roost selection
.
South African Journal of Wildlife Research
27
:
44
50
.
Clement
MJ,
Castleberry
SB.
2013
.
Divergent roosting habits of Rafinesque's big-eared bat and southeastern myotis during winter floods
.
American Midland Naturalist
170
:
158
170
.
Cunningham
KJ,
Florea
LJ.
2009
.
The Biscayne aquifer of southeastern Florida
.
Pages
196
199
in
Caves and karst in America.
Czenze
AJ,
Jonasson
KA,
Willis,
CKR.
2017
Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate
.
Physiological and Biochemical Zoology
90
:
502
511
.
Dixon
JW.
2011
.
The role of small caves as bat hibernacula in Iowa
.
Journal of Cave and Karst Studies
73
:
21
27
.
Fleming
HL,
Belant
JL,
Richardson
DM.
2013
.
Multi-scale roost site selection by Rafinesque's big-eared bat (Corynorhinus rafinesquii) and southeastern myotis (Myotis austroriparius) in Mississippi
.
American Midland Naturalist
169
:
43
55
.
Florea
LJ,
Vacher
HL.
2009
.
The southeastern coastal plain: an overview
.
Pages
181
184
in
Caves and karst in America.
Flory
AR,
Kumar
S,
Stohlgren,
TJ,
Cryan
PM.
2012
.
Environmental conditions associated with bat white-nose syndrome mortality in the north-eastern United States
.
Journal of Applied Ecology
59
:
680
689
.
[FNAI] Florida Natural Areas Inventory.
2010
.
Guide to the natural communities of Florida, 2010 edition
.
Tallahassee
:
Florida Natural Areas Inventory
.
Available: https://www.fnai.org/landcover.cfm (May 2021).
Frick
WF,
Pollock
JF,
Hicks
AC,
Langwig
KE,
Reynolds
DS,
Turner
GG,
Butchkoski
CM,
Kunz
TH.
2010
.
An emerging disease causes regional population collapse of a common North American bat species
.
Science
329
:
679
682
.
Frick
WF,
Puechmaille
SJ,
Hoyt
JR,
Nickel
BA,
Langwig
KE,
Foster
JT,
Barlow
KE,
Bartonička
T,
Feller
D,
Haarsma
A,
Herzog
C,
Horáček
I,
van der Kooij
J,
Mulkens
B,
Petrov
B,
Reynolds
R,
Rodrigues
L,
Stihler
CW,
Turner
GG,
Kilpatrick
AM.
2015
.
Disease alters macroecological patterns of North American bats
.
Global Ecology and Biogeography
24
:
741
749
.
Frost
SW.
1962
.
Winter insect light-trapping at the Archbold Biological Station, Florida
.
Florida Entomologist
45
:
175
190
.
Gates
JE,
Feldhamer
GA,
Griffith
LA,
Raesly
RL.
1984
.
Status of cave-dwelling bats in Maryland: importance of marginal habitats
.
Wildlife Society Bulletin
12
:
162
169
.
Gore
JA.
Records of caves with bat use [unpublished]
.
Located at: Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 1105 SW Williston Road, Gainesville, Florida 32601.
Gore
JA,
Hovis
JA.
1998
.
Status and conservation of southeastern myotis maternity colonies in Florida caves
.
Florida Scientist
61
:
160
170
.
Gore
JA,
Lazure
L,
Ludlow
ME.
2012
.
Decline in the winter population of gray bats (Myotis grisescens) in Florida
.
Southeastern Naturalist
2012
:
89
98
.
Harvey
MJ,
Altenbach
JS,
Best
TL.
1999
.
Bats of the United States
.
Little Rock
:
Arkansas Game and Fish Commission
.
Hayman
DTS,
Pulliam
JRC,
Marshall
JC,
Cryan
PM,
Webb
CT.
2016
.
Environment, host, and fungal traits predict continental-scale white-nose syndrome in bats
.
Science Advances
2
:
e1500831
.
Humphrey
SR,
Gore
JA.
1992
.
Southeastern brown bat
.
Pages
52
70
in
Humphrey
SR,
editor.
Rare and endangered biota of Florida. Volume 1
.
Mammals. Gainesville: University Press of Florida.
Hurst
TE,
Lacki
MJ.
1999
.
Roost selection, population size, and habitat use by a colony of Rafinesque's big-eared bats (Corynorhinus rafinesquii)
.
American Midland Naturalist
142
:
363
371
.
Johnson
JS,
Reeder
DM,
McMichael
JW
III,
Meierhofer
MB,
Stern
DWF,
Lumadue
SS,
Sigler
LE,
Winters
HD,
Vodzak
ME,
Kurta
A,
Kath
JA,
Field
KA.
2014
.
Host, pathogen, and environmental characteristics predict white-nose syndrome mortality in captive little brown myotis (Myotis lucifugus)
.
PloS ONE
9
:
e112502
.
Jonasson
KA,
Willis
CKR.
2011
.
Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome
.
PloS ONE
6
:
e21061
.
Langwig
KE,
Frick
WF,
Bried
JT,
Hicks
AC,
Kunz
TH,
Kilpatrick
AM.
2012
.
Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome
.
Ecology Letters
15
:
1050
1057
.
Langwig
KE,
Frick
WF,
Hoyt
JR,
Parise
KL,
Drees
KP,
Kunz
TH,
Foster
JT,
Kilpatrick
AM.
2016
.
Drivers of variation in species impacts for a multi-host fungal disease of bats
.
Philosophical Transactions of the Royal Society B
371
:
20150456
.
Lorch
JM,
Meteyer
CU,
Behr
MJ,
Boyles
JG,
Cryan
PM,
Hicks
AC,
Ballman
AE,
Coleman
JTH,
Redell
DN,
Reeder
DM,
Blehert
DS.
2011
.
Experimental infection of bats with Geomyces destructans causes white-nose syndrome
.
Nature
480
:
376
378
.
McNab
BK.
1974
.
The behavior of temperate cave bats in a subtropical environment
.
Ecology
55
:
943
958
.
Meierhofer
MB,
Leivers
SJ,
Fern
RR,
Wolf
LK,
Young
LL
Jr,
Pierce
BL,
Evans
JW,
Morrison
ML.
2019
.
Structural and environmental predictors of presence and abundance of tri-colored bats in Texas culverts
.
Journal of Mammalogy
100
:
1274
1281
.
[NOAA] National Oceanic and Atmospheric Administration.
2020
.
Comparative Climatic Data Available: https://www1.ncdc.noaa.gov/pub/data/ccd-data/mnls3218.dat (May 2021)
.
Newman,
BA.
2020
.
Winter torpor and roosting ecology of tri-colored bats (Perimyotis subflavus) in trees and bridges. Master's thesis
.
Clemson, South Carolina
:
Clemson University
.
O'Shea
TJ,
Cryan
PM,
Hayman
DTS,
Plowright
RK,
Streicker
DG.
2016
.
Multiple mortality events in bats: a global review
.
Mammal Review
46
:
175
190
.
Perry
RW.
2013
.
A review of factors affecting cave climates for hibernating bats in temperate North America
.
Environmental Reviews
21
:
28
39
.
Rabinowitz
A.
1981
.
Thermal preference of the eastern pipistrelle bat (Pipistrellus subflavus) during hibernation
.
Journal of the Tennessee Academy of Science
56
:
113
.
R Core Team.
2014
.
R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
.
Raesly
RL,
Gates
JE.
1987
.
Winter habitat selection by north temperate cave bats
.
American Midland Naturalist
118
:
15
31
.
Rice
DW.
1957
.
Life history and ecology of Myotis austroriparius in Florida
.
Journal of Mammalogy
38
:
15
32
.
Schelldorfer
J,
Meier
L,
Bühlmann,
P.
2014
.
Glmmlasso: an algorithm for high-dimensional generalized linear mixed models using L1-penalization
.
Journal of Computational and Graphical Statistics
23
:
460
477
.
Smith
LM,
Mayersky
J,
Gore
JA.
2017
.
Rafinesque's big-eared bat (Corynorhinus rafinesquii) in a Florida cave in winter
.
Florida Field Naturalist
45
:
50
52
.
Smith
LM,
Oxenrider
KJ,
Hayman
RJ,
Gore
JA.
2020
.
Refining the distribution of Rafinesque's big-eared bat
.
Southeastern Naturalist
19
:
38
44
.
Speakman
JR,
Thomas
DW.
2003
.
Physiological ecology and energetics of bats
.
Pages
430
490
in
Kunz
TH,
Fenton
MB,
editors.
Bat biology
.
Chicago
:
University of Chicago Press
.
Tuttle
MD,
Stevenson
DE.
1978
.
Variations in the cave environment and its biological implications
.
Pages
108
121
in
Zuber
R,
Chester
J,
Gilbert
S,
Rhodes
D,
editors.
National Cave Management Proceedings, 3–7 October 1977, Big Sky, Montana
.
Albuquerque, New Mexico
:
Speleobooks
.
Tuttle
MD,
Taylor
DAR.
1998
.
Bats and mines
.
Austin, Texas
:
Bat Conservation International
.
Resource publication no. 3.
[ESA] U.S. Endangered Species Act of 1973, as amended, Pub. L. No. 93-205, 87 Stat. 884 (Dec. 28, 1973)
.
[USFWS] U.S. Fish and Wildlife Service.
2020
.
White-nose syndrome response team
.
Available at: https://www.whitenosesyndrome.org/ (May 2021).
U.S. Office of the Federal Register.
1976
.
Determination that two species of butterflies are threatened species and two species of mammals are endangered species
.
Federal Register
41
:
17736
17740
.
Verant
ML,
Boyles
JG,
Waldrep
W,
Jr.,
Wibbelt
G,
Blehert
DS.
2012
.
Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome
.
PloS ONE
7
: e46280.
Warnecke
L,
Turner
JM,
Bollinger
TK,
Lorch
JM,
Misra
V,
Cryan
PM,
Wibbelt
G,
Blehert
DS,
Willis
CKR.
2012
.
Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome
.
Proceedings of the National Academy of Sciences of the United States of America
109
:
6999
7003
.
[WNS DMWG] White-nose Syndrome Disease Management Working Group.
2020
.
National white-nose syndrome decontamination protocol
.
U.S. Fish and Wildlife Service
(see Supplemental Material, Reference S2).
Zinn
TL.
1977
.
Community ecology of Florida bats with emphasis on Myotis austroriparius. Master's thesis
.
Gainesville
:
University of Florida
.

The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Author notes

Citation: Smith LM, Doonan TJ, Sylvia AL, Gore JA. 2021. Characteristics of caves used by wintering bats in a subtropical environment. Journal of Fish and Wildlife Management 12(1):139–150; e1944-687X. https://doi.org/10.3996/JFWM-20-078

Supplementary data