Landscape-scale distribution of tree roosts of the northern long-eared bat in Mammoth Cave National Park, USA

Landscape-scale distribution of tree roosts of the northern long-eared bat in Mammoth Cave... Landscape Ecol https://doi.org/10.1007/s10980-018-0659-3 RESEARCH ARTICLE Landscape-scale distribution of tree roosts of the northern long-eared bat in Mammoth Cave National Park, USA . . Marissa M. Thalken Michael J. Lacki Jian Yang Received: 3 August 2017 / Accepted: 26 May 2018 The Author(s) 2018 Abstract Conclusions Our data indicate that a more compre- Context The roosting habits of many temperate zone hensive understanding of habitat requirements which bats are well documented at microhabitat scales, but includes empirically-based, landscape-scale patterns, fewer studies have included multi-scale assessments and not solely considerations at stand or local levels, of landscape patterns in bat roost site selection. could lead to better informed management policies Objectives To identify and assess at the landscape- targeting conservation of maternity habitat of forest- scale the location of spring and early season maternity dwelling bats, including the northern long-eared bat, a roosts of female northern long-eared bats (Myotis species in decline throughout much of its distribution septentrionalis) from 2015 to 2016 at Mammoth Cave in North America. National Park (MACA), Kentucky, USA. Methods We used mist-nets and radiotelemetry to Keywords Bats  Landscape patterns  Maternity catch and track bats to roost trees across the landscape season  Myotis septentrionalis  Roosting habitat of MACA. Data on roosting sites were evaluated using Spatial point pattern  Spring staging  Winter spatial point pattern analysis to examine distributional hibernacula trends of roosts. A variety of spatial covariates were used to model the effect of landscape pattern, includ- ing: forest type, elevation, and proximity to hibernac- ula, water, and road corridors. Introduction Results Data indicate that roost locations of female northern long-eared bats in MACA were typically Bats (Order: Chiroptera) constitute approximately situated within 2000 m of known winter hibernacula, one-fifth of all mammal species (Martin et al. 2011). occurring more often at higher elevations in mesic They are broadly distributed, occupy a variety of upland deciduous forests, and in close proximity to feeding guilds, and may be the most abundant water sources and roads. We present hypotheses to mammals on a local scale, especially in the tropics account for the patterns observed in relation to (Patterson et al. 2003; Gorresen et al. 2005). Anthro- landscape features and habitat resources in the Park. pogenic forces worldwide, such as deforestation and fragmentation (Burgar et al. 2015; Toth et al. 2015; Rocha et al. 2017), urbanization and habitat loss M. M. Thalken  M. J. Lacki (&)  J. Yang (Lintott et al. 2015, 2016; Caryl et al. 2016), agricul- Department of Forestry and Natural Resources, University tural intensification (Azam et al. 2016; Cleary et al. of Kentucky, Lexington, KY 40546-0073, USA e-mail: mlacki@uky.edu 123 Landscape Ecol 2016; Mendes et al. 2017), and alternate energy (i.e., pregnant or lactating) female northern long-eared technologies (Peste et al. 2015; Ferri et al. 2016) are bats, and whether patterns in landscape characteristics elevating the rates of species extinction and the loss of helped explain outcomes for spatial locations of roosts Chiropteran diversity. Globally, deforestation and of this species. Based on known patterns in roosting fragmentation represent the most abrupt form of behavior of northern long-eared bats elsewhere in the landscape change (Millennium Ecosystem Assess- distribution, we hypothesized these bats would roost ment 2005; Boughey et al. 2011). Unfortunately, an within mesic upland deciduous forests (Foster and understanding of species-specific needs of bats at Kurta 1999; Menzel et al. 2002; Broders and Forbes landscape levels, including responses to changes from 2004; Pauli et al. 2015), in close proximity to flyways anthropogenic forces, remains elusive. and corridors such as water sources and roads The majority of studies on summer roosting ecol- (Henderson and Broders 2008; Perry et al. 2008); the ogy of bats in North America has focused on habitat latter presumably to enhance access to foraging sites conditions at the scale of the roost tree or surrounding elsewhere on the landscape. We also hypothesized that forest stand (Lacki and Baker 2003; Kalcounis- topography would influence the likelihood of roosting Ru¨eppell et al. 2005; Barclay and Kurta 2007). occurrences, as topographic features known to be Theoretical and empirical evidence suggests, how- important to female northern long-eared bats else- ever, that animal species rarely follow a linear where include higher elevation sites and upper and association with gradients in habitat characteristics mid-slope positions (Lacki and Schwierjohann 2001; (Wiens 1989; Lord and Norton 1990; With and Crist Lacki et al. 2009; Krynak 2010). Finally, we hypoth- 1995; Gorresen et al. 2005), and criteria that species esized that female northern long-eared bats would use for habitat and resource selection likely vary by roost near known winter hibernacula, especially both landscape and proximal spatial scales. Use of during spring emergence, i.e., staging, when fat multi-scale analyses in examining roost selection of reserves are reduced and availability of insect prey North American bats has been achieved for foliage- remain at seasonal lows. Reproductive female bats are roosting species (Veilleux et al. 2004; Limpert et al. presumably more constrained by energy demands than 2007; Hein et al. 2008) and select Myotis species male bats (Cryan et al. 2000; Willis and Wilcox 2014; (Arnett and Hayes 2009; Lacki et al. 2010; Hammond Wilcox and Willis 2016), so it would be reasonable to et al. 2016; Jachowski et al. 2016), with a range of assume that roost selection of female bats during landscape patterns found to be beneficial depending on staging would be consistent with minimizing move- species and geographic location. Comparative studies ments and energy expenditures during an energetically are limited on landscape-level selection of tree roosts challenging season of the year. by the northern long-eared bat, Myotis septentrionalis (Pauli et al. 2015; Ford et al. 2016); a threatened species experiencing severe population declines Materials and methods across much of its distribution in North America (USDI 2015). Study area Spatial statistics of point patterns provide a rigorous format for describing distributions of species or any The study was located at Mammoth Cave National other spatially-temporally discrete events of interest Park (MACA), situated within the Green River Valley (e.g., earthquake, fire ignition) and testing hypotheses in south central Kentucky, USA (Fig. 1). The Park is about those distributions at larger spatial scales approximately 212 km and is positioned on a karst (Loosmore and Ford 2006; Law et al. 2009; Reiter landscape recognized for the longest known cave and Anderson 2013). We employed spatial point system in the world. The limestone rocks beneath date pattern analysis to quantify patterns of spring and early to 325 million years ago during the Mississippian maternity season roosts of adult, female northern long- Period (Livesay 1953). Much of the landscape on and eared bats at Mammoth Cave National Park, Ken- around the Park is pitted by depressions or sinkholes tucky, USA. Our objectives were to determine what due to the karst topography, resulting in few surface landscape characteristics, if any, were important for streams other than the Green and Nolin Rivers. The roost selection of non-reproductive and reproductive Park ranges in elevation from 128 to 281-m above sea 123 Landscape Ecol Fig. 1 Map of Mammoth Cave National Park (MACA), Kentucky, showing locations of clusters of tree roosts (roosting areas) of female northern long-eared bats recorded in 2015 and 2016 level, has a mean annual temperature of 14.9 C, and 2011, over 25% of the Park was burned with an average annual rainfall of approx. 130 cm (U.S. prescribed fire techniques (Lacki et al. 2014). Climate Data 2016). The Mammoth Cave region is dominated by Capture and telemetry second-growth oak-hickory forest (USNPS 2016). The area is considered to be a transitional zone Northern long-eared bats were captured from April to between open grasslands and oak-hickory forests to July, 2015 and 2016, using mist-nets measuring the west and mesophytic forests to the east. Likewise, 6–18 m in length and stacked 6–9 m high (Avinet, the Park is situated between colder climates to the Dryden, NY). Nets were placed at capture sites that north and sub-tropical climates to the south. The included cave entrances, backcountry roads, and different vegetation types create a mosaic of habitats ephemeral ponds. Upon capture, the mass (g), right across the Park that support a vast array of flora and forearm length (mm), reproductive condition (fe- fauna, including 43 mammal species (USNPS 2016). males: pregnant, lactating or non-reproductive; males: In 2002, a prescribed fire management plan was set in scrotal or non-scrotal), Reichard’s wing index score place at the Park to reduce fuel loads and restore the (Reichard and Kunz 2009), sex, and age (Brunet- forest to pre-settlement conditions. Between 2002 and Rossinni and Wilkinson 2009) were collected for every individual. Adult females were grouped as non- 123 Landscape Ecol reproductive if no evidence of pregnancy or lactation A spatial point pattern process (SPP) is a stochastic was visible; however, because all of these bats were mechanism that generates a set of points in time and captured in the post-hibernation staging period, many space which describe the locations of observed species likely were reproductively active and would have or events (Law et al. 2009; Baddeley et al. 2015). Early demonstrated to be so if captured later in summer. Bats ecological applications of SPP analysis were mainly to were identified to species and released at the site of characterize spatial trend of points with first-order capture. Myotis bats were banded with 2.9-mm bands statistics for quantifying variations in expected density provided by the Kentucky Department of Fish and (also called intensity) of observed individuals across Wildlife Resources. Adult, female northern long-eared the sample space and to identify spatial interaction bats receiving radio-transmitters were not banded to (i.e., clustering, regularity, and random) among points keep added weight\ 5% of their body mass (Aldridge with second-order statistics such as Ripley’s K func- and Brigham 1988). All handling procedures included tion (Perry et al. 2006; Law et al. 2009). Recent adherence to decontamination protocols laid out by the theoretical developments in SPP have provided a U.S. Fish and Wildlife Service (USFWS 2016). rigorous framework and versatile diagnostic tools to fit Nineteen adult female northern long-eared bats and the observed point data to underlying point processes one juvenile male were captured and fitted with LB- (e.g., Poisson, Cox, Strauss) (Baddeley et al. 2015). 2XT radio-transmitters (Holohil Systems, Ltd., Ontar- While methods for fitting spatial point pattern data are closely related to common regression models, PPMs io, Canada) with surgical glue (Perma-Type Company, Inc., Plainville, CT) between the shoulder blades. have considerable potential in modeling presence- Transmitters mass was B 0.33 g to comply with the only data with various advantages, including (but not 5% rule (Aldridge and Brigham 1988). Bats were limited to) (1) explicit focus on where the points were tracked daily for approximately 8-15 days or until the observed, (2) clarity of model assumptions and tools transmitter battery failed or fell off the bat. A for checking them, and (3) direct handle of spatial 3-element yagi antenna (Wildlife Materials, Inc., dependence between points (Renner et al. 2015). Murphysboro, IL) and an Icom IC-R20 radio-receiver Kernel intensity estimation and Ripley’s K function (Icom America, Inc., Kirkland, WA) were used to were calculated to describe spatial patterns (i.e., track bats. We located 69 roosts used by radio-tagged clustering or regularity) of roosts at the Park (Yang adult, female northern long-eared bats at MACA. For et al. 2007). each roost identified, the coordinates were recorded Inhomogeneous Poisson point process models were with a Garmin GPS unit (Garmin International, Inc., used to fit the observed roost tree location data, which Olathe, KS). assume that expected number of roost trees per unit area varies spatially and roost trees are independent of Modeling roosting habitat each other at the scale of our investigation. It has been shown that Poisson point process model is equivalent Locations of spring and summer roost trees were to the popular entropy-based MAXENT model but geographically referenced using the UTM (Universal with a transparent modeling structure (Renner and Transverse Mercator) Zone 16 N coordinate system. Warton 2013). We examined a variety of spatial Spatial covariates (i.e., roadways, hydrology, and land covariates with transformations in the inhomogeneous cover) were mapped and processed using a geographic Poisson models including elevation, southwestness, information system (ArcGIS 10.4.1, Redlands, CA). distance to water, distance to roads, distance to winter We obtained digital vegetation coverage, data for hibernacula, and proportion of mesic upland decidu- hydrology and roadways (L. Scoggins, MACA, U.S. ous forest. Residual analysis for the spatial point National Park Service), and locations of known bat processes and Akaike’s Information Criterion (AIC) overwintering caves for analyses (R. Toomey, MACA, methods were used to select variables with a back- U.S. National Park Service). We used a point process ward-stepwise model selection to find the best fit modeling (PPM) approach to describe spring and model for the data (Yang et al. 2007). summer roost locations based on an inhomogeneous Spatial covariates were chosen for analysis, in part, Poisson process (Yang et al. 2007; Renner et al. 2015). on the basis of prior research indicating patterns of habitat selection by northern long-eared bats. For 123 Landscape Ecol Results example, the digital vegetation layer contained nine different vegetation classes. The ‘mesic upland decid- The non-parametric kernel density estimation showed uous’ vegetation class was chosen based off prior studies that indicated use of this habitat type by the a high concentration of roosts in the northwest section of the Park, indicating the roost occurrence pattern northern long-eared bat (Foster and Kurta 1999; Menzel et al. 2002; Broders and Forbes 2004; was not completely random (Fig. 2). The minimum distance between any two roosts was 4.24 m, with an Henderson and Broders 2008). We used a moving window analysis (30 9 30 m cell size) to determine average nearest neighbor distance of the proportion of mesic upland deciduous forest within 108 m ± 12.4(SE), and a maximum distance of a neighborhood (i.e., the window) for every location 381 m. The estimated K function was larger than within the Park. The purpose of moving window theoretical complete spatial randomness (CSR), indi- cating the locations of roosts on the landscape analysis was to create a GIS variable that could describe local-scale vegetation composition and trans- exhibited a spatial clustering pattern (Fig. 3). Regard- less, strong spatial dependence could be due to either form the categorical vegetation class GIS variable into a continuous variable. The continuous vegetation bat behavior, i.e., fission–fusion, or to association with clustering of environmental factors (i.e., vegetation variable was then examined in spatial point pattern modeling to quantify vegetation effects on roosting type, elevation, etc.) on the landscape. The inhomogeneous Poisson process model locations. Proximities to road and water were deter- mined by calculating the Euclidian distance from each demonstrated that spatial clustering of roosts could cell (30-m resolution) to the nearest road or water be accounted for by environmental heterogeneity. The source, a function provided by the ArcGIS Spatial null model (homogeneous Poisson) assumes that roost Analyst tool. We used a digital elevation model locations are equally likely across the landscape. The cumulative Pearson residuals were plotted against the (DEM) published by the Kentucky Geological Survey (Kentucky Geological Survey 1998). Slope and aspect seven spatial covariates (i.e., distance to road, distance to water, distance to winter caves, slope, elevation, were calculated from DEM data with the surface analysis provided by the ArcGIS Spatial Analyst tool. southwestness, and proportion of mesic upland decid- uous forest) and the two Cartesian coordinates (x and Calculated aspect azimuths were later transformed into southwestness using the equation (cos(aspect)- y) for the null model. The cumulative Pearson 225) to change the circular aspect to a linear gradient residuals for the predicted random values exceeded for indexing potential incident solar radiation (south- the observed roost occurrence values, suggesting that westness). We used a Euclidian distance function to determine distances from roost locations to the nearest known winter bat caves. A lurking plot variable was used to identify non-linear or spatial trends in the point processes (Baddeley and Turner 2005). First, the cumulative residual is plotted against a select spatial covariate. Then noticeable trends in the lurking variable plot are accounted for and appropriately modified for that spatial covariate. Eventually, selected covariates were plotted in R with a polyno- mial function up to the power of two based on the final model coefficients to model the marginal effects of the variables on roost likelihood (Yang et al. 2015). All the analyses were conducted in the R software environment with the spatstat package (Baddeley and Turner 2005). Fig. 2 Non-parametric density estimation of roosts of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA 123 Landscape Ecol to water, distance to winter caves, elevation, south- westness, slope, and mesic upland deciduous forest. Due to most continuous variables displaying curvilin- ear relationships, the full model also included second order transformations for all covariates except mesic upland deciduous cover type and southwestness. The best fit model possessed an AIC = 2100.3 (Table 1). The second order distance to water, first order distance to roads, and both first and second order distances to winter caves were retained in the best fit model (P \ 0.01). The second order elevation and first order mesic upland deciduous forest cover type were also retained but with a larger P value (P \ 0.1). Slope and southwestness were excluded during the model selec- tion process. The best fit models generated a prediction map of Fig. 3 Estimated K function graph for roosts of female northern likely roosting locations of female northern long-eared long-eared bats at Mammoth Cave National Park, Kentucky, bats at MACA. Dark blue areas on the left top panel of USA the map indicated areas the model predicted to have the highest likelihood of roost occurrence on the the null model underestimated roost likelihood at this landscape (Fig. 5). However, the cumulative sum of scale. raw residuals did not fit within the two-standard- Lurking variables plotted against the null model of deviation error bounds in the northwest portion of the roost occurrence on the Park landscape indicated clear Park (in red), meaning the model did not account for systematic patterns (Fig. 4). Female northern long- all variations in the data. eared bats selected roost locations within approxi- Effects of likelihood of roost occurrence within the mately 500 m of known roadways (Fig. 4a), 800 m of Park were plotted against three variables: elevation, water sources (Fig. 4b), and between approximately distance to water and distance to winter caves (Fig. 6). 2000 and 4000 m away from known winter bat Elevation appears to have a positive association with hibernacula (Fig. 4c). Female bats avoided potential probability of roost location, suggesting higher eleva- roost locations at elevations between 198 and 259 m tion areas are preferred habitats of female northern (Fig. 4d). A lurking plot of the proportion of mesic long-eared bats during staging and the early maternity upland deciduous forest with the 900-m moving season. Distance to water demonstrated a monotoni- window analysis of vegetation cover type revealed cally decreasing pattern indicating that probability of the cumulative residuals of the null hypothesis were roost location decreases as distance to the nearest smaller than expected for areas where the proportion water source increases. The distance to known over- of mesic upland deciduous forest was less than 80% wintering hibernacula within the Park shows an (Fig. 4e). This suggests that female northern long- inflection point at approximately 2000 m. Bats eared bats in MACA had a strong preference towards appeared to select roosts farther away from winter mesic upland deciduous forests. The last two variable caves up to the inflection point. Beyond the inflection plots, slope and southwestness, exhibited empirical point distance, the likelihood of roosts occurring on curves of cumulative Pearson residuals within the two- the landscape dropped significantly. standard-deviation error bounds, suggesting bats did not preferentially choose roost sites by aspect or slope position. Discussion A full range of alternative models were considered that included all possible combinations of the potential Studies have demonstrated that responses of bats to spatial covariates examined. The full model (AIC = spatial structure of habitats is highly dependent on 2113.2) predictors included distance to road, distance focal scale (Gorresen et al. 2005; Perry et al. 2008; 123 Landscape Ecol Fig. 4 Lurking variable plots of a distance to road, b distance to water, c distance to winter caves, d elevation (DEM), e proportion of vegetation code 3 (mesic upland deciduous), f slope, and g southwestness (aspect) for the null model of roost occurrence on the landscape at Mammoth Cave National Park, Kentucky, USA. Solid lines indicate empirical curves of cumulative Pearson residuals. Shaded areas denote two-standard- deviation error bounds 123 Landscape Ecol Table 1 Parameter Variable Parameter Confidence interval estimates of predictor variables for the best fit Estimate SE P value Low High model of location of roosts Intercept - 1.68E ? 01 8.98E-01 ns - 1.86E ? 01 - 1.5E ? 01 of female northern long- eared bats at Mammoth Elevation 2.06E-05 1.04E-05 \ 0.1 1.76E-07 4.1E-05 Cave National Park, 2 Distance to water - 4.29E-06 9.34E-07 \ 0.01 - 6.12E-06 - 2.46E-06 Kentucky, USA Distance to road - 3.26E-03 5.76E-04 \ 0.01 - 4.39E-03 - 2.13E-03 Superscript refers to Vegetation 4.86E-01 2.45E-01 \ 0.1 6.39E-03 9.66E-01 variables included as Distance to caves 2.68E-03 6.78E-04 \ 0.01 1.35E-03 4.01E-03 second order effects. Those Distance to caves - 6.09E-07 1.64E-07 \ 0.01 - 9.31E-07 - 2.88E-07 without the superscript were first order effects Fig. 5 Fit point process model prediction map of roost locations of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA, for the best fit model O’Keefe et al. 2009). Proximity to water sources, et al. 2007). Distance to corridors and mature pine foraging areas, and topography (i.e., slope position, forest was associated with roost selection in Seminole elevation, aspect) can all potentially affect roost bats (L. seminolus; Hein et al. 2008), and tri-colored selection by bats at the landscape scale (Perry et al. bats preferentially selected riparian and upland forests 2008). Multi-scale patterns in roost selection of other over bottomland habitats (Veilleux et al. 2004). bat species in southeastern North America have We observed that during the spring and early demonstrated eastern red bats (Lasiurus borealis)to maternity seasons, roosts of female northern long- favor mature streamside management areas within eared bats were spatially clustered on the landscape, intensively managed pine plantations (Elmore et al. consistent with patterns expected for bats which form 2005), and to select roosting sites near open, urban roost-networks during the summer maternity season land and water compared with random sites (Limpert (Garroway and Broders 2007; Johnson et al. 2012). 123 Landscape Ecol bFig. 6 Likelihood of occurrence of roosts of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA, by a elevation, b distance to water, and c distance to known overwintering caves We identified several environmental factors that served as important determinants of spatial locations for these bats in MACA, with our results corroborating findings that demonstrated female northern long-eared bats to choose roosts in proximity to roads (Perry et al. 2008; Pauli et al. 2015). Roads have been directly associated with flight corridors and improved access to suitable areas for foraging by bats (Limpens and Kapteyn 1991; Walsh and Harris 1996). Our findings also indicated a strong positive correlation of roosts of northern long-eared bats with available sources of water. Empirical evidence has demonstrated the importance of nearby water sources in roost tree selection by several other temperate-zone bat species (Kalcounis-Rueppell et al. 2005; Limpert et al. 2007; Perry et al. 2008). Female northern long-eared bats at MACA had a strong preference toward selection of roosts within the vegetation cover type described as mesic upland deciduous forest. The lurking variable plot of the proportion of mesic upland deciduous forest, com- bined with the moving window analysis, indicated that habitats where these bats chose roost trees at MACA, on average, had up to 80% of habitat patches in the mesic upland deciduous forest cover type. These results are consistent with findings elsewhere across the distribution of the species that demonstrated preference for roosts in deciduous trees within rela- tively contiguous forests (Foster and Kurta 1999; Menzel et al. 2002; Henderson and Broders 2008; Pauli et al. 2015). We also observed northern long- eared bats preferentially choosing roosts in higher elevation habitats that are away from the cold bottomlands, and suggest that roosts situated at higher elevation sites reflected the needs of adult females to inhabit structures possessing warmer microclimates. Warmer roosting microclimates could potentially reduce the cost of maintaining normothermic body temperatures during the early reproductive season, and presumably help facilitate parturition, lactation and the development of young. Landscape-scale selection of roosts at high elevations has also been demonstrated 123 Landscape Ecol for the Indiana bat in southern Appalachian Mountains Assessing the status of a species requires an (Hammond et al. 2016). understanding of the basic biology, ecology, popula- Due to MACA’s karst topography, location of tion size and trends over time (Alberta Sustainable known overwintering hibernacula was a novel land- Resource Development and Alberta Conservation scape feature not previously examined in any other Association 2009). Ultimately, more information landscape scale study on bats. The elevation of the about the basic ecology of bats is needed to effectively water table in MACA, which is roughly the elevation conserve them, with access to shelter, food, and water of the Green River, corresponds with the elevation resources necessary to secure the survival of bat where many cave entrances occur (DiPietro 2013). As populations globally (Fenton and Simmons 2015). Our the Green River cuts downslope into the landscape, research used a point process pattern analysis to active cave formation drops to lower levels, leaving examine landscape-level patterns in roost tree selec- dry caves higher up in elevation. The uppermost tion of adult female northern long-eared bats at passages of Mammoth Cave are located between 174 MACA. We found that during the spring staging and and 210 m in elevation, with the oldest and largest early maternity seasons, roosts of these bats were cave openings occurring at ground level or 227 m spatially clustered on the landscape, with landscape (DiPietro 2013). Female northern long-eared bats features including elevation, and distances to roads, appeared to select roost locations increasingly farther water, and overwintering hibernacula being important determinants of spatial location of these roosts. For at away from known overwintering caves up to 2000 m in distance; however, no female bat chose a roost least MACA, preferred roost tree locations of female location beyond the 2000 m distance threshold from northern long-eared bats are situated within 2000 m of any known winter hibernaculum. We suggest two known winter hibernacula at higher elevation sites possibilities for this pattern. First, the relatively close supporting mesic upland deciduous forests. Manage- proximity to overwintering caves allows for con- ment of habitats at the stand level remains fundamen- specifics to remain in contact and eventually regroup tal in fostering increases in bat colony numbers during after the hibernation period in spring (i.e., staging the maternity season (O’Donnell 2000; Willis and behavior), facilitating formation of local summer Brigham 2004; Garroway and Broders 2008); how- maternity colonies. Second, as hypothesized, by ever, our findings also confirm the importance of minimizing distances moved from hibernacula in larger spatial scales when developing long-term early spring, when temperatures are cooler on average planning efforts for maternity habitat of the northern and availability of insect prey less predictable, adult long-eared bat. female bats are limiting energy expenditures to help Bat populations in eastern North America are maintain a positive energy balance at a time when continually being threatened by anthropogenic forces many are pregnant and allocating energetic resources and, now with the onset of the fungal (Pseudogym- to the developing fetus. noascus destructans) disease white-nose syndrome Maintaining a buffer of at least 2000 m surrounding (WNS), face even greater challenges to survival known overwintering caves of the northern long-eared moving forward (Blehert et al. 2009; USFWS 2017). bat would help to ensure the continued availability of It is presently unclear just how these impacts will suitable roosting sites for the species throughout the interact synergistically to produce population-level Park. The northern long-eared bat has declined effects, or whether declines in bat populations will significantly enough across its range over the past continue and lead to permanent and lasting shifts in decade for the species to be added as threatened under species relative abundance (Moosman et al. 2013; the Endangered Species Act (USDI 2015). It is Reynolds et al. 2016; Thalken et al. 2018). Regardless, presently unknown whether these population trends habitat needs of bats at the landscape scale, especially will lead to permanent and lasting reductions in the maternity habitat, should remain a top conservation abundance of this species. Thus, sustaining maternity priority and our analyses indicate that landscape habitats of the northern long-eared bat at landscape features are important to location of maternity roosts scales in geographic locations where they are still of northern long-eared bats. We encourage further data known to occur is imperative to conservation efforts collection on roost selection of forest-dwelling bats in for the recovery of the species across its distribution. eastern North America to facilitate management and 123 Landscape Ecol management. Johns Hopkins University Press, Baltimore, recovery efforts of bat species, especially those MD, pp 17–59 affected by WNS. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Acknowledgements We thank the National Park Service, the Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat Walt Disney Foundation, and the University of Kentucky, white-nose syndrome: an emerging fungal pathogen? Sci- College of Agriculture, for funding support. We are appreciative ence 323:227 of R. Toomey (Mammoth Cave National Park), S. Thomas Boughey KL, Lake IR, Haysom KA, Dolman PM (2011) Effects (National Park Service), and L. Dodd (Eastern Kentucky of landscape-scale broadleaved woodland configuration University) for assistance during the planning and and extent on roost location for six bat species across the implementation of this study. We are grateful to all the field U.K. Biol Conserv 144:2300–2310 technicians including: E. Stanmyer, B. Daly, T. Walters, M. Broders HG, Forbes G (2004) Interspecific and intersexual Barnes, E. Lee, J. Ayres, H. Dykes, S. Zumdick, Z. Hackworth, variation in roost-site selection of northern long-eared and M. McKenna, E. Kester, S. Fulton, and Z. Fry. All animal little brown bats in the Greater Fundy National Park handling procedures used were approved by the University of ecosystem. J Wildl Manag 68:602–610 Kentucky under IACUC Assurance No.: A3336-01. Data Brunet-Rossinni AK, Wilkinson GS (2009) Methods for age collection was supported through permits from the Kentucky estimation and the study of senescence in bats. In: Kunz Department of Fish and Wildlife Resources (SC1611176; TH, Parsons S (eds) Ecological and behavioral methods for SC1511245) and the U.S. Fish and Wildlife Service the study of bats, 2nd edn. Johns Hopkins University Press, (TE38522A-1). The information reported in this paper (No. Baltimore, MD, pp 315–325 17-09-048) is part of a project of the Kentucky Agricultural Burgar JM, Craig MD, Stokes VL (2015) The importance of Experiment Station and is published with the approval of the mature forest as bat roosting habitat within a production Director. landscape. For Ecol Manag 356:112–123 Caryl FM, Lumsden LF, van der Ree R, Wintle BA (2016) Open Access This article is distributed under the terms of the Functional responses of insectivorous bats to increasing Creative Commons Attribution 4.0 International License (http:// housing density support ‘‘land-sparing’ rather than ‘‘land- creativecommons.org/licenses/by/4.0/), which permits unre- sharing’ urban growth strategies. 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Ecology 76:2446–2459 Park, Kentucky. http://www.usclimatedata.com/climate/ Yang J, He HS, Shifley SR, Gustafson EJ (2007) Spatial patterns mammoth-cave/kentucky/united-states/usky1113. Acces- of modern period human-caused fire occurrence in Mis- sed 1 Sept 2016 souri Ozark highlands. For Sci 53:1–15 US Department of the Interior (2015) Final register for endan- Yang J, Weisberg PJ, Dilts TE, Loudermilk EL, Scheller RM, gered and threatened wildlife and plants; threatened spe- Stanton A, Skinner C (2015) Predicting wildfire occurrence cies status for the northern long-eared bat with 4(d) rule. distribution with spatial point process models and its Fish and Wildlife Service. vol 80. No. 63 uncertainty assessment: a case study in the Lake Tahoe Basin, USA. Int J Wildl Fire 24:38–390 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Landscape Ecology Springer Journals

Landscape-scale distribution of tree roosts of the northern long-eared bat in Mammoth Cave National Park, USA

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Life Sciences; Landscape Ecology; Ecology; Nature Conservation; Landscape/Regional and Urban Planning; Sustainable Development; Environmental Management
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Abstract

Landscape Ecol https://doi.org/10.1007/s10980-018-0659-3 RESEARCH ARTICLE Landscape-scale distribution of tree roosts of the northern long-eared bat in Mammoth Cave National Park, USA . . Marissa M. Thalken Michael J. Lacki Jian Yang Received: 3 August 2017 / Accepted: 26 May 2018 The Author(s) 2018 Abstract Conclusions Our data indicate that a more compre- Context The roosting habits of many temperate zone hensive understanding of habitat requirements which bats are well documented at microhabitat scales, but includes empirically-based, landscape-scale patterns, fewer studies have included multi-scale assessments and not solely considerations at stand or local levels, of landscape patterns in bat roost site selection. could lead to better informed management policies Objectives To identify and assess at the landscape- targeting conservation of maternity habitat of forest- scale the location of spring and early season maternity dwelling bats, including the northern long-eared bat, a roosts of female northern long-eared bats (Myotis species in decline throughout much of its distribution septentrionalis) from 2015 to 2016 at Mammoth Cave in North America. National Park (MACA), Kentucky, USA. Methods We used mist-nets and radiotelemetry to Keywords Bats  Landscape patterns  Maternity catch and track bats to roost trees across the landscape season  Myotis septentrionalis  Roosting habitat of MACA. Data on roosting sites were evaluated using Spatial point pattern  Spring staging  Winter spatial point pattern analysis to examine distributional hibernacula trends of roosts. A variety of spatial covariates were used to model the effect of landscape pattern, includ- ing: forest type, elevation, and proximity to hibernac- ula, water, and road corridors. Introduction Results Data indicate that roost locations of female northern long-eared bats in MACA were typically Bats (Order: Chiroptera) constitute approximately situated within 2000 m of known winter hibernacula, one-fifth of all mammal species (Martin et al. 2011). occurring more often at higher elevations in mesic They are broadly distributed, occupy a variety of upland deciduous forests, and in close proximity to feeding guilds, and may be the most abundant water sources and roads. We present hypotheses to mammals on a local scale, especially in the tropics account for the patterns observed in relation to (Patterson et al. 2003; Gorresen et al. 2005). Anthro- landscape features and habitat resources in the Park. pogenic forces worldwide, such as deforestation and fragmentation (Burgar et al. 2015; Toth et al. 2015; Rocha et al. 2017), urbanization and habitat loss M. M. Thalken  M. J. Lacki (&)  J. Yang (Lintott et al. 2015, 2016; Caryl et al. 2016), agricul- Department of Forestry and Natural Resources, University tural intensification (Azam et al. 2016; Cleary et al. of Kentucky, Lexington, KY 40546-0073, USA e-mail: mlacki@uky.edu 123 Landscape Ecol 2016; Mendes et al. 2017), and alternate energy (i.e., pregnant or lactating) female northern long-eared technologies (Peste et al. 2015; Ferri et al. 2016) are bats, and whether patterns in landscape characteristics elevating the rates of species extinction and the loss of helped explain outcomes for spatial locations of roosts Chiropteran diversity. Globally, deforestation and of this species. Based on known patterns in roosting fragmentation represent the most abrupt form of behavior of northern long-eared bats elsewhere in the landscape change (Millennium Ecosystem Assess- distribution, we hypothesized these bats would roost ment 2005; Boughey et al. 2011). Unfortunately, an within mesic upland deciduous forests (Foster and understanding of species-specific needs of bats at Kurta 1999; Menzel et al. 2002; Broders and Forbes landscape levels, including responses to changes from 2004; Pauli et al. 2015), in close proximity to flyways anthropogenic forces, remains elusive. and corridors such as water sources and roads The majority of studies on summer roosting ecol- (Henderson and Broders 2008; Perry et al. 2008); the ogy of bats in North America has focused on habitat latter presumably to enhance access to foraging sites conditions at the scale of the roost tree or surrounding elsewhere on the landscape. We also hypothesized that forest stand (Lacki and Baker 2003; Kalcounis- topography would influence the likelihood of roosting Ru¨eppell et al. 2005; Barclay and Kurta 2007). occurrences, as topographic features known to be Theoretical and empirical evidence suggests, how- important to female northern long-eared bats else- ever, that animal species rarely follow a linear where include higher elevation sites and upper and association with gradients in habitat characteristics mid-slope positions (Lacki and Schwierjohann 2001; (Wiens 1989; Lord and Norton 1990; With and Crist Lacki et al. 2009; Krynak 2010). Finally, we hypoth- 1995; Gorresen et al. 2005), and criteria that species esized that female northern long-eared bats would use for habitat and resource selection likely vary by roost near known winter hibernacula, especially both landscape and proximal spatial scales. Use of during spring emergence, i.e., staging, when fat multi-scale analyses in examining roost selection of reserves are reduced and availability of insect prey North American bats has been achieved for foliage- remain at seasonal lows. Reproductive female bats are roosting species (Veilleux et al. 2004; Limpert et al. presumably more constrained by energy demands than 2007; Hein et al. 2008) and select Myotis species male bats (Cryan et al. 2000; Willis and Wilcox 2014; (Arnett and Hayes 2009; Lacki et al. 2010; Hammond Wilcox and Willis 2016), so it would be reasonable to et al. 2016; Jachowski et al. 2016), with a range of assume that roost selection of female bats during landscape patterns found to be beneficial depending on staging would be consistent with minimizing move- species and geographic location. Comparative studies ments and energy expenditures during an energetically are limited on landscape-level selection of tree roosts challenging season of the year. by the northern long-eared bat, Myotis septentrionalis (Pauli et al. 2015; Ford et al. 2016); a threatened species experiencing severe population declines Materials and methods across much of its distribution in North America (USDI 2015). Study area Spatial statistics of point patterns provide a rigorous format for describing distributions of species or any The study was located at Mammoth Cave National other spatially-temporally discrete events of interest Park (MACA), situated within the Green River Valley (e.g., earthquake, fire ignition) and testing hypotheses in south central Kentucky, USA (Fig. 1). The Park is about those distributions at larger spatial scales approximately 212 km and is positioned on a karst (Loosmore and Ford 2006; Law et al. 2009; Reiter landscape recognized for the longest known cave and Anderson 2013). We employed spatial point system in the world. The limestone rocks beneath date pattern analysis to quantify patterns of spring and early to 325 million years ago during the Mississippian maternity season roosts of adult, female northern long- Period (Livesay 1953). Much of the landscape on and eared bats at Mammoth Cave National Park, Ken- around the Park is pitted by depressions or sinkholes tucky, USA. Our objectives were to determine what due to the karst topography, resulting in few surface landscape characteristics, if any, were important for streams other than the Green and Nolin Rivers. The roost selection of non-reproductive and reproductive Park ranges in elevation from 128 to 281-m above sea 123 Landscape Ecol Fig. 1 Map of Mammoth Cave National Park (MACA), Kentucky, showing locations of clusters of tree roosts (roosting areas) of female northern long-eared bats recorded in 2015 and 2016 level, has a mean annual temperature of 14.9 C, and 2011, over 25% of the Park was burned with an average annual rainfall of approx. 130 cm (U.S. prescribed fire techniques (Lacki et al. 2014). Climate Data 2016). The Mammoth Cave region is dominated by Capture and telemetry second-growth oak-hickory forest (USNPS 2016). The area is considered to be a transitional zone Northern long-eared bats were captured from April to between open grasslands and oak-hickory forests to July, 2015 and 2016, using mist-nets measuring the west and mesophytic forests to the east. Likewise, 6–18 m in length and stacked 6–9 m high (Avinet, the Park is situated between colder climates to the Dryden, NY). Nets were placed at capture sites that north and sub-tropical climates to the south. The included cave entrances, backcountry roads, and different vegetation types create a mosaic of habitats ephemeral ponds. Upon capture, the mass (g), right across the Park that support a vast array of flora and forearm length (mm), reproductive condition (fe- fauna, including 43 mammal species (USNPS 2016). males: pregnant, lactating or non-reproductive; males: In 2002, a prescribed fire management plan was set in scrotal or non-scrotal), Reichard’s wing index score place at the Park to reduce fuel loads and restore the (Reichard and Kunz 2009), sex, and age (Brunet- forest to pre-settlement conditions. Between 2002 and Rossinni and Wilkinson 2009) were collected for every individual. Adult females were grouped as non- 123 Landscape Ecol reproductive if no evidence of pregnancy or lactation A spatial point pattern process (SPP) is a stochastic was visible; however, because all of these bats were mechanism that generates a set of points in time and captured in the post-hibernation staging period, many space which describe the locations of observed species likely were reproductively active and would have or events (Law et al. 2009; Baddeley et al. 2015). Early demonstrated to be so if captured later in summer. Bats ecological applications of SPP analysis were mainly to were identified to species and released at the site of characterize spatial trend of points with first-order capture. Myotis bats were banded with 2.9-mm bands statistics for quantifying variations in expected density provided by the Kentucky Department of Fish and (also called intensity) of observed individuals across Wildlife Resources. Adult, female northern long-eared the sample space and to identify spatial interaction bats receiving radio-transmitters were not banded to (i.e., clustering, regularity, and random) among points keep added weight\ 5% of their body mass (Aldridge with second-order statistics such as Ripley’s K func- and Brigham 1988). All handling procedures included tion (Perry et al. 2006; Law et al. 2009). Recent adherence to decontamination protocols laid out by the theoretical developments in SPP have provided a U.S. Fish and Wildlife Service (USFWS 2016). rigorous framework and versatile diagnostic tools to fit Nineteen adult female northern long-eared bats and the observed point data to underlying point processes one juvenile male were captured and fitted with LB- (e.g., Poisson, Cox, Strauss) (Baddeley et al. 2015). 2XT radio-transmitters (Holohil Systems, Ltd., Ontar- While methods for fitting spatial point pattern data are closely related to common regression models, PPMs io, Canada) with surgical glue (Perma-Type Company, Inc., Plainville, CT) between the shoulder blades. have considerable potential in modeling presence- Transmitters mass was B 0.33 g to comply with the only data with various advantages, including (but not 5% rule (Aldridge and Brigham 1988). Bats were limited to) (1) explicit focus on where the points were tracked daily for approximately 8-15 days or until the observed, (2) clarity of model assumptions and tools transmitter battery failed or fell off the bat. A for checking them, and (3) direct handle of spatial 3-element yagi antenna (Wildlife Materials, Inc., dependence between points (Renner et al. 2015). Murphysboro, IL) and an Icom IC-R20 radio-receiver Kernel intensity estimation and Ripley’s K function (Icom America, Inc., Kirkland, WA) were used to were calculated to describe spatial patterns (i.e., track bats. We located 69 roosts used by radio-tagged clustering or regularity) of roosts at the Park (Yang adult, female northern long-eared bats at MACA. For et al. 2007). each roost identified, the coordinates were recorded Inhomogeneous Poisson point process models were with a Garmin GPS unit (Garmin International, Inc., used to fit the observed roost tree location data, which Olathe, KS). assume that expected number of roost trees per unit area varies spatially and roost trees are independent of Modeling roosting habitat each other at the scale of our investigation. It has been shown that Poisson point process model is equivalent Locations of spring and summer roost trees were to the popular entropy-based MAXENT model but geographically referenced using the UTM (Universal with a transparent modeling structure (Renner and Transverse Mercator) Zone 16 N coordinate system. Warton 2013). We examined a variety of spatial Spatial covariates (i.e., roadways, hydrology, and land covariates with transformations in the inhomogeneous cover) were mapped and processed using a geographic Poisson models including elevation, southwestness, information system (ArcGIS 10.4.1, Redlands, CA). distance to water, distance to roads, distance to winter We obtained digital vegetation coverage, data for hibernacula, and proportion of mesic upland decidu- hydrology and roadways (L. Scoggins, MACA, U.S. ous forest. Residual analysis for the spatial point National Park Service), and locations of known bat processes and Akaike’s Information Criterion (AIC) overwintering caves for analyses (R. Toomey, MACA, methods were used to select variables with a back- U.S. National Park Service). We used a point process ward-stepwise model selection to find the best fit modeling (PPM) approach to describe spring and model for the data (Yang et al. 2007). summer roost locations based on an inhomogeneous Spatial covariates were chosen for analysis, in part, Poisson process (Yang et al. 2007; Renner et al. 2015). on the basis of prior research indicating patterns of habitat selection by northern long-eared bats. For 123 Landscape Ecol Results example, the digital vegetation layer contained nine different vegetation classes. The ‘mesic upland decid- The non-parametric kernel density estimation showed uous’ vegetation class was chosen based off prior studies that indicated use of this habitat type by the a high concentration of roosts in the northwest section of the Park, indicating the roost occurrence pattern northern long-eared bat (Foster and Kurta 1999; Menzel et al. 2002; Broders and Forbes 2004; was not completely random (Fig. 2). The minimum distance between any two roosts was 4.24 m, with an Henderson and Broders 2008). We used a moving window analysis (30 9 30 m cell size) to determine average nearest neighbor distance of the proportion of mesic upland deciduous forest within 108 m ± 12.4(SE), and a maximum distance of a neighborhood (i.e., the window) for every location 381 m. The estimated K function was larger than within the Park. The purpose of moving window theoretical complete spatial randomness (CSR), indi- cating the locations of roosts on the landscape analysis was to create a GIS variable that could describe local-scale vegetation composition and trans- exhibited a spatial clustering pattern (Fig. 3). Regard- less, strong spatial dependence could be due to either form the categorical vegetation class GIS variable into a continuous variable. The continuous vegetation bat behavior, i.e., fission–fusion, or to association with clustering of environmental factors (i.e., vegetation variable was then examined in spatial point pattern modeling to quantify vegetation effects on roosting type, elevation, etc.) on the landscape. The inhomogeneous Poisson process model locations. Proximities to road and water were deter- mined by calculating the Euclidian distance from each demonstrated that spatial clustering of roosts could cell (30-m resolution) to the nearest road or water be accounted for by environmental heterogeneity. The source, a function provided by the ArcGIS Spatial null model (homogeneous Poisson) assumes that roost Analyst tool. We used a digital elevation model locations are equally likely across the landscape. The cumulative Pearson residuals were plotted against the (DEM) published by the Kentucky Geological Survey (Kentucky Geological Survey 1998). Slope and aspect seven spatial covariates (i.e., distance to road, distance to water, distance to winter caves, slope, elevation, were calculated from DEM data with the surface analysis provided by the ArcGIS Spatial Analyst tool. southwestness, and proportion of mesic upland decid- uous forest) and the two Cartesian coordinates (x and Calculated aspect azimuths were later transformed into southwestness using the equation (cos(aspect)- y) for the null model. The cumulative Pearson 225) to change the circular aspect to a linear gradient residuals for the predicted random values exceeded for indexing potential incident solar radiation (south- the observed roost occurrence values, suggesting that westness). We used a Euclidian distance function to determine distances from roost locations to the nearest known winter bat caves. A lurking plot variable was used to identify non-linear or spatial trends in the point processes (Baddeley and Turner 2005). First, the cumulative residual is plotted against a select spatial covariate. Then noticeable trends in the lurking variable plot are accounted for and appropriately modified for that spatial covariate. Eventually, selected covariates were plotted in R with a polyno- mial function up to the power of two based on the final model coefficients to model the marginal effects of the variables on roost likelihood (Yang et al. 2015). All the analyses were conducted in the R software environment with the spatstat package (Baddeley and Turner 2005). Fig. 2 Non-parametric density estimation of roosts of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA 123 Landscape Ecol to water, distance to winter caves, elevation, south- westness, slope, and mesic upland deciduous forest. Due to most continuous variables displaying curvilin- ear relationships, the full model also included second order transformations for all covariates except mesic upland deciduous cover type and southwestness. The best fit model possessed an AIC = 2100.3 (Table 1). The second order distance to water, first order distance to roads, and both first and second order distances to winter caves were retained in the best fit model (P \ 0.01). The second order elevation and first order mesic upland deciduous forest cover type were also retained but with a larger P value (P \ 0.1). Slope and southwestness were excluded during the model selec- tion process. The best fit models generated a prediction map of Fig. 3 Estimated K function graph for roosts of female northern likely roosting locations of female northern long-eared long-eared bats at Mammoth Cave National Park, Kentucky, bats at MACA. Dark blue areas on the left top panel of USA the map indicated areas the model predicted to have the highest likelihood of roost occurrence on the the null model underestimated roost likelihood at this landscape (Fig. 5). However, the cumulative sum of scale. raw residuals did not fit within the two-standard- Lurking variables plotted against the null model of deviation error bounds in the northwest portion of the roost occurrence on the Park landscape indicated clear Park (in red), meaning the model did not account for systematic patterns (Fig. 4). Female northern long- all variations in the data. eared bats selected roost locations within approxi- Effects of likelihood of roost occurrence within the mately 500 m of known roadways (Fig. 4a), 800 m of Park were plotted against three variables: elevation, water sources (Fig. 4b), and between approximately distance to water and distance to winter caves (Fig. 6). 2000 and 4000 m away from known winter bat Elevation appears to have a positive association with hibernacula (Fig. 4c). Female bats avoided potential probability of roost location, suggesting higher eleva- roost locations at elevations between 198 and 259 m tion areas are preferred habitats of female northern (Fig. 4d). A lurking plot of the proportion of mesic long-eared bats during staging and the early maternity upland deciduous forest with the 900-m moving season. Distance to water demonstrated a monotoni- window analysis of vegetation cover type revealed cally decreasing pattern indicating that probability of the cumulative residuals of the null hypothesis were roost location decreases as distance to the nearest smaller than expected for areas where the proportion water source increases. The distance to known over- of mesic upland deciduous forest was less than 80% wintering hibernacula within the Park shows an (Fig. 4e). This suggests that female northern long- inflection point at approximately 2000 m. Bats eared bats in MACA had a strong preference towards appeared to select roosts farther away from winter mesic upland deciduous forests. The last two variable caves up to the inflection point. Beyond the inflection plots, slope and southwestness, exhibited empirical point distance, the likelihood of roosts occurring on curves of cumulative Pearson residuals within the two- the landscape dropped significantly. standard-deviation error bounds, suggesting bats did not preferentially choose roost sites by aspect or slope position. Discussion A full range of alternative models were considered that included all possible combinations of the potential Studies have demonstrated that responses of bats to spatial covariates examined. The full model (AIC = spatial structure of habitats is highly dependent on 2113.2) predictors included distance to road, distance focal scale (Gorresen et al. 2005; Perry et al. 2008; 123 Landscape Ecol Fig. 4 Lurking variable plots of a distance to road, b distance to water, c distance to winter caves, d elevation (DEM), e proportion of vegetation code 3 (mesic upland deciduous), f slope, and g southwestness (aspect) for the null model of roost occurrence on the landscape at Mammoth Cave National Park, Kentucky, USA. Solid lines indicate empirical curves of cumulative Pearson residuals. Shaded areas denote two-standard- deviation error bounds 123 Landscape Ecol Table 1 Parameter Variable Parameter Confidence interval estimates of predictor variables for the best fit Estimate SE P value Low High model of location of roosts Intercept - 1.68E ? 01 8.98E-01 ns - 1.86E ? 01 - 1.5E ? 01 of female northern long- eared bats at Mammoth Elevation 2.06E-05 1.04E-05 \ 0.1 1.76E-07 4.1E-05 Cave National Park, 2 Distance to water - 4.29E-06 9.34E-07 \ 0.01 - 6.12E-06 - 2.46E-06 Kentucky, USA Distance to road - 3.26E-03 5.76E-04 \ 0.01 - 4.39E-03 - 2.13E-03 Superscript refers to Vegetation 4.86E-01 2.45E-01 \ 0.1 6.39E-03 9.66E-01 variables included as Distance to caves 2.68E-03 6.78E-04 \ 0.01 1.35E-03 4.01E-03 second order effects. Those Distance to caves - 6.09E-07 1.64E-07 \ 0.01 - 9.31E-07 - 2.88E-07 without the superscript were first order effects Fig. 5 Fit point process model prediction map of roost locations of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA, for the best fit model O’Keefe et al. 2009). Proximity to water sources, et al. 2007). Distance to corridors and mature pine foraging areas, and topography (i.e., slope position, forest was associated with roost selection in Seminole elevation, aspect) can all potentially affect roost bats (L. seminolus; Hein et al. 2008), and tri-colored selection by bats at the landscape scale (Perry et al. bats preferentially selected riparian and upland forests 2008). Multi-scale patterns in roost selection of other over bottomland habitats (Veilleux et al. 2004). bat species in southeastern North America have We observed that during the spring and early demonstrated eastern red bats (Lasiurus borealis)to maternity seasons, roosts of female northern long- favor mature streamside management areas within eared bats were spatially clustered on the landscape, intensively managed pine plantations (Elmore et al. consistent with patterns expected for bats which form 2005), and to select roosting sites near open, urban roost-networks during the summer maternity season land and water compared with random sites (Limpert (Garroway and Broders 2007; Johnson et al. 2012). 123 Landscape Ecol bFig. 6 Likelihood of occurrence of roosts of female northern long-eared bats at Mammoth Cave National Park, Kentucky, USA, by a elevation, b distance to water, and c distance to known overwintering caves We identified several environmental factors that served as important determinants of spatial locations for these bats in MACA, with our results corroborating findings that demonstrated female northern long-eared bats to choose roosts in proximity to roads (Perry et al. 2008; Pauli et al. 2015). Roads have been directly associated with flight corridors and improved access to suitable areas for foraging by bats (Limpens and Kapteyn 1991; Walsh and Harris 1996). Our findings also indicated a strong positive correlation of roosts of northern long-eared bats with available sources of water. Empirical evidence has demonstrated the importance of nearby water sources in roost tree selection by several other temperate-zone bat species (Kalcounis-Rueppell et al. 2005; Limpert et al. 2007; Perry et al. 2008). Female northern long-eared bats at MACA had a strong preference toward selection of roosts within the vegetation cover type described as mesic upland deciduous forest. The lurking variable plot of the proportion of mesic upland deciduous forest, com- bined with the moving window analysis, indicated that habitats where these bats chose roost trees at MACA, on average, had up to 80% of habitat patches in the mesic upland deciduous forest cover type. These results are consistent with findings elsewhere across the distribution of the species that demonstrated preference for roosts in deciduous trees within rela- tively contiguous forests (Foster and Kurta 1999; Menzel et al. 2002; Henderson and Broders 2008; Pauli et al. 2015). We also observed northern long- eared bats preferentially choosing roosts in higher elevation habitats that are away from the cold bottomlands, and suggest that roosts situated at higher elevation sites reflected the needs of adult females to inhabit structures possessing warmer microclimates. Warmer roosting microclimates could potentially reduce the cost of maintaining normothermic body temperatures during the early reproductive season, and presumably help facilitate parturition, lactation and the development of young. Landscape-scale selection of roosts at high elevations has also been demonstrated 123 Landscape Ecol for the Indiana bat in southern Appalachian Mountains Assessing the status of a species requires an (Hammond et al. 2016). understanding of the basic biology, ecology, popula- Due to MACA’s karst topography, location of tion size and trends over time (Alberta Sustainable known overwintering hibernacula was a novel land- Resource Development and Alberta Conservation scape feature not previously examined in any other Association 2009). Ultimately, more information landscape scale study on bats. The elevation of the about the basic ecology of bats is needed to effectively water table in MACA, which is roughly the elevation conserve them, with access to shelter, food, and water of the Green River, corresponds with the elevation resources necessary to secure the survival of bat where many cave entrances occur (DiPietro 2013). As populations globally (Fenton and Simmons 2015). Our the Green River cuts downslope into the landscape, research used a point process pattern analysis to active cave formation drops to lower levels, leaving examine landscape-level patterns in roost tree selec- dry caves higher up in elevation. The uppermost tion of adult female northern long-eared bats at passages of Mammoth Cave are located between 174 MACA. We found that during the spring staging and and 210 m in elevation, with the oldest and largest early maternity seasons, roosts of these bats were cave openings occurring at ground level or 227 m spatially clustered on the landscape, with landscape (DiPietro 2013). Female northern long-eared bats features including elevation, and distances to roads, appeared to select roost locations increasingly farther water, and overwintering hibernacula being important determinants of spatial location of these roosts. For at away from known overwintering caves up to 2000 m in distance; however, no female bat chose a roost least MACA, preferred roost tree locations of female location beyond the 2000 m distance threshold from northern long-eared bats are situated within 2000 m of any known winter hibernaculum. We suggest two known winter hibernacula at higher elevation sites possibilities for this pattern. First, the relatively close supporting mesic upland deciduous forests. Manage- proximity to overwintering caves allows for con- ment of habitats at the stand level remains fundamen- specifics to remain in contact and eventually regroup tal in fostering increases in bat colony numbers during after the hibernation period in spring (i.e., staging the maternity season (O’Donnell 2000; Willis and behavior), facilitating formation of local summer Brigham 2004; Garroway and Broders 2008); how- maternity colonies. Second, as hypothesized, by ever, our findings also confirm the importance of minimizing distances moved from hibernacula in larger spatial scales when developing long-term early spring, when temperatures are cooler on average planning efforts for maternity habitat of the northern and availability of insect prey less predictable, adult long-eared bat. female bats are limiting energy expenditures to help Bat populations in eastern North America are maintain a positive energy balance at a time when continually being threatened by anthropogenic forces many are pregnant and allocating energetic resources and, now with the onset of the fungal (Pseudogym- to the developing fetus. noascus destructans) disease white-nose syndrome Maintaining a buffer of at least 2000 m surrounding (WNS), face even greater challenges to survival known overwintering caves of the northern long-eared moving forward (Blehert et al. 2009; USFWS 2017). bat would help to ensure the continued availability of It is presently unclear just how these impacts will suitable roosting sites for the species throughout the interact synergistically to produce population-level Park. The northern long-eared bat has declined effects, or whether declines in bat populations will significantly enough across its range over the past continue and lead to permanent and lasting shifts in decade for the species to be added as threatened under species relative abundance (Moosman et al. 2013; the Endangered Species Act (USDI 2015). It is Reynolds et al. 2016; Thalken et al. 2018). Regardless, presently unknown whether these population trends habitat needs of bats at the landscape scale, especially will lead to permanent and lasting reductions in the maternity habitat, should remain a top conservation abundance of this species. Thus, sustaining maternity priority and our analyses indicate that landscape habitats of the northern long-eared bat at landscape features are important to location of maternity roosts scales in geographic locations where they are still of northern long-eared bats. We encourage further data known to occur is imperative to conservation efforts collection on roost selection of forest-dwelling bats in for the recovery of the species across its distribution. eastern North America to facilitate management and 123 Landscape Ecol management. Johns Hopkins University Press, Baltimore, recovery efforts of bat species, especially those MD, pp 17–59 affected by WNS. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH, Darling SR, Gargas A, Acknowledgements We thank the National Park Service, the Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009) Bat Walt Disney Foundation, and the University of Kentucky, white-nose syndrome: an emerging fungal pathogen? Sci- College of Agriculture, for funding support. We are appreciative ence 323:227 of R. Toomey (Mammoth Cave National Park), S. Thomas Boughey KL, Lake IR, Haysom KA, Dolman PM (2011) Effects (National Park Service), and L. Dodd (Eastern Kentucky of landscape-scale broadleaved woodland configuration University) for assistance during the planning and and extent on roost location for six bat species across the implementation of this study. We are grateful to all the field U.K. Biol Conserv 144:2300–2310 technicians including: E. Stanmyer, B. Daly, T. Walters, M. Broders HG, Forbes G (2004) Interspecific and intersexual Barnes, E. Lee, J. Ayres, H. Dykes, S. Zumdick, Z. Hackworth, variation in roost-site selection of northern long-eared and M. McKenna, E. Kester, S. Fulton, and Z. Fry. All animal little brown bats in the Greater Fundy National Park handling procedures used were approved by the University of ecosystem. J Wildl Manag 68:602–610 Kentucky under IACUC Assurance No.: A3336-01. Data Brunet-Rossinni AK, Wilkinson GS (2009) Methods for age collection was supported through permits from the Kentucky estimation and the study of senescence in bats. In: Kunz Department of Fish and Wildlife Resources (SC1611176; TH, Parsons S (eds) Ecological and behavioral methods for SC1511245) and the U.S. Fish and Wildlife Service the study of bats, 2nd edn. Johns Hopkins University Press, (TE38522A-1). The information reported in this paper (No. Baltimore, MD, pp 315–325 17-09-048) is part of a project of the Kentucky Agricultural Burgar JM, Craig MD, Stokes VL (2015) The importance of Experiment Station and is published with the approval of the mature forest as bat roosting habitat within a production Director. landscape. For Ecol Manag 356:112–123 Caryl FM, Lumsden LF, van der Ree R, Wintle BA (2016) Open Access This article is distributed under the terms of the Functional responses of insectivorous bats to increasing Creative Commons Attribution 4.0 International License (http:// housing density support ‘‘land-sparing’ rather than ‘‘land- creativecommons.org/licenses/by/4.0/), which permits unre- sharing’ urban growth strategies. J Appl Ecol 53:191–201 stricted use, distribution, and reproduction in any medium, Cleary KA, Waits LP, Finegan B (2016) Agricultural intensifi- provided you give appropriate credit to the original cation alters bat assemblage composition and abundance in author(s) and the source, provide a link to the Creative Com- a dynamic Neotropical landscape. Biotropica 48:667–676 mons license, and indicate if changes were made. Cryan PM, Bogan MA, Altenbach JS (2000) Effect on elevation on distribution of female bats in the Black Hills, South Dakota. J Mammal 811:719–725 DiPietro JA (2013) Landscape evolution in the United States: an introduction to the geography, geology, and natural history. 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