Optimizing ultrasonic sampling effort for monitoring forest bats

Landscape‐scale monitoring is a key approach for assessing changes in indicators. However, great care needs to be taken to collect rigorous data and avoid wasting resources in long‐term programmes. Insect‐eating bats are diverse, functionally important and are often proposed as indicator species of environmental health. We used acoustic (ultrasonic) data from pilot bat surveys undertaken in forests and woodlands to optimize sampling effort to produce precise estimates of bat activity and occupancy. We also carried out simulations to evaluate the statistical power of different sampling designs to detect changes in activity and occupancy levels of individual bat species. There was little gain in precision for estimates of bat activity by sampling beyond five to six detector nights. To ensure spatial heterogeneity was sampled around a monitoring point, three detectors for two nights or two detectors for three nights would be required. This level of sampling was also sufficient to be 90% certain of recording occupancy for 11 of 12 taxa. Power simulations revealed that a sampling design using two detectors per monitoring point for two nights could detect a 30% decline within 10 years with 90% power for all species, except the white‐striped free tail bat (Tadarida australis), using either changes in activity levels or occupancy. However, fewer years were required when using occupancy. Setting detectors either on‐flyways or off‐flyways contributed only minor differences to the time taken to reach 90% power for both occupancy and activity levels, though sampling both locations has major implications for interpreting trends in bats. We suggest that bat activity levels are more sensitive for detecting change than occupancy because one pass or 1000 passes can be recorded per night by an acoustic detector, and this is not differentiated by occupancy. Bats can be monitored cost‐effectively and should be included in monitoring programmes.     

Optimizing passive acoustic sampling of bats in forests

Passive acoustic methods are increasingly used in biodiversity research and monitoring programs because they are cost‐effective and permit the collection of large datasets. However, the accuracy of the results depends on the bioacoustic characteristics of the focal taxa and their habitat use. In particular, this applies to bats which exhibit distinct activity patterns in three‐dimensionally structured habitats such as forests. We assessed the performance of 21 acoustic sampling schemes with three temporal sampling patterns and seven sampling designs. Acoustic sampling was performed in 32 forest plots, each containing three microhabitats: forest ground, canopy, and forest gap. We compared bat activity, species richness, and sampling effort using species accumulation curves fitted with the clench equation. In addition, we estimated the sampling costs to undertake the best sampling schemes. We recorded a total of 145,433 echolocation call sequences of 16 bat species. Our results indicated that to generate the best outcome, it was necessary to sample all three microhabitats of a given forest location simultaneously throughout the entire night. Sampling only the forest gaps and the forest ground simultaneously was the second best choice and proved to be a viable alternative when the number of available detectors is limited. When assessing bat species richness at the 1‐km² scale, the implementation of these sampling schemes at three to four forest locations yielded highest labor cost‐benefit ratios but increasing equipment costs. Our study illustrates that multiple passive acoustic sampling schemes require testing based on the target taxa and habitat complexity and should be performed with reference to cost‐benefit ratios. Choosing a standardized and replicated sampling scheme is particularly important to optimize the level of precision in inventories, especially when rare or elusive species are expected.     

Bat point counts: A novel sampling method shines light on flying bat communities

Emerging technologies based on the detection of electro‐magnetic energy offer promising opportunities for sampling biodiversity. We exploit their potential by showing here how they can be used in bat point counts—a novel method to sample flying bats—to overcome shortcomings of traditional sampling methods, and to maximize sampling coverage and taxonomic resolution of this elusive taxon with minimal sampling bias. We conducted bat point counts with a sampling rig combining a thermal scope to detect bats, an ultrasound recorder to obtain echolocation calls, and a near‐infrared camera to capture bat morphology. We identified bats with a dedicated identification key combining acoustic and morphological features, and compared bat point counts with the standard bat sampling methods of mist‐netting and automated ultrasound recording in three oil palm plantation sites in Indonesia, over nine survey nights. Based on rarefaction and extrapolation sampling curves, bat point counts were similarly effective but more time‐efficient than the established methods for sampling the oil palm species pool in our study. Point counts sampled species that tend to avoid nets and those that are not echolocating, and thus cannot be detected acoustically. We identified some bat sonotypes with near‐infrared imagery, and bat point counts revealed strong sampling biases in previous studies using capture‐based methods, suggesting similar biases in other regions might exist. Our method should be tested in a wider range of habitats and regions to assess its performance. However, while capture‐based methods allow to identify bats with absolute and internal morphometry, and unattended ultrasound recorders can effectively sample echolocating bats, bat point counts are a promising, non‐invasive, and potentially competitive new tool for sampling all flying bats without bias and observing their behavior in the wild.     

Ensemble composition and activity levels of insectivorous bats in response to management intensification in coffee agroforestry systems

Shade coffee plantations have received attention for their role in biodiversity conservation. Bats are among the most diverse mammalian taxa in these systems; however, previous studies of bats in coffee plantations have focused on the largely herbivorous leaf-nosed bats (Phyllostomidae). In contrast, we have virtually no information on how ensembles of aerial insectivorous bats--nearly half the Neotropical bat species--change in response to habitat modification. To evaluate the effects of agroecosystem management on insectivorous bats, we studied their diversity and activity in southern Chiapas, Mexico, a landscape dominated by coffee agroforestry. We used acoustic monitoring and live captures to characterize the insectivorous bat ensemble in forest fragments and coffee plantations differing in the structural and taxonomic complexity of shade trees. We captured bats of 12 non-phyllostomid species; acoustic monitoring revealed the presence of at least 12 more species of aerial insectivores. Richness of forest bats was the same across all land-use types; in contrast, species richness of open-space bats increased in low shade, intensively managed coffee plantations. Conversely, only forest bats demonstrated significant differences in ensemble structure (as measured by similarity indices) across land-use types. Both overall activity and feeding activity of forest bats declined significantly with increasing management intensity, while the overall activity, but not feeding activity, of open-space bats increased. We conclude that diverse shade coffee plantations in our study area serve as valuable foraging and commuting habitat for aerial insectivorous bats, and several species also commute through or forage in low shade coffee monocultures.     

Heard but not seen: Comparing bat assemblages and study methods in a mosaic landscape in the Western Ghats of India

We used capture (mist‐netting) and acoustic methods to compare the species richness, abundance, and composition of a bat assemblage in different habitats in the Western Ghats of India. In the tropics, catching bats has been more commonly used as a survey method than acoustic recordings. In our study, acoustic methods based on recording echolocation calls detected greater bat activity and more species than mist‐netting. However, some species were detected more frequently or exclusively by capture. Ideally, the two methods should be used together to compensate for the biases in each. Using combined capture and acoustic data, we found that protected forests, forest fragments, and shade coffee plantations hosted similar and diverse species assemblages, although some species were recorded more frequently in protected forests. Tea plantations contained very few species from the overall bat assemblage. In riparian habitats, a strip of forested habitat on the river bank improved the habitat for bats compared to rivers with tea planted up to each bank. Our results show that shade coffee plantations are better bat habitat than tea plantations in biodiversity hotspots. However, if tea is to be the dominant land use, forest fragments and riparian corridors can improve the landscape considerably for bats. We encourage coffee growers to retain traditional plantations with mature native trees, rather than reverting to sun grown coffee or coffee shaded by a few species of timber trees.     

Neotropical bats in the canopy: diversity,community structure,and implications for conservation

We compare results of parallel ground and canopy netting of bats (Microchiroptera) in three adjacent forest sites near Belém, Brazil, to document possible differences in vertical distribution of species. We caught 1871 individuals representing 49 species of three families (Emballonuridae, Phyllostomidae, Vespertilionidae). Capture effort, totaling 1955.5 mistnet hours in several cycles over a two-year period, was similar for ground and canopy nets. The canopy rigs yielded more species (n = 41) than the ground nets (n = 35), but both samples were characterized by rank abundance curves with similar shape and with a dominance of frugivores (Phyllostomidae). Nearly half (n = 24) of the species were captured in numbers too small (n < 6) to allow firm classification, but differences in capture frequencies of some of the better-sampled species in high and low nets reveal vertical stratification. Species-specific differences in diet, foraging strategies, roost sites, and sampling bias contribute to this pattern. As a result of the differential use of space among bats, alterations of forest structure are likely to result in changes in structure and function of local bat communities, but our limited knowledge of natural history and ecology of many species limits definition of changes. We see a critical need for further research into the extent to which habitat complexity influences species richness and abundance of bats. This information is especially important in view of the need to develop and apply conservation-oriented programs to maintain biodiversity. A review of recent improvements in techniques for inventorying bats shows that a combination of methods, including mistnetting and acoustic monitoring, is mandatory for such studies.     

Do you hear what I see? Vocalization relative to visual detection rates of Hawaiian hoary bats (Lasiurus cinereus semotus)

Bats vocalize during flight as part of the sensory modality called echolocation, but very little is known about whether flying bats consistently call. Occasional vocal silence during flight when bats approach prey or conspecifics has been documented for relatively few species and situations. Bats flying alone in clutter‐free airspace are not known to forgo vocalization, yet prior observations suggested possible silent behavior in certain, unexpected situations. Determining when, why, and where silent behavior occurs in bats will help evaluate major assumptions of a primary monitoring method for bats used in ecological research, management, and conservation. In this study, we recorded flight activity of Hawaiian hoary bats (Lasiurus cinereus semotus) under seminatural conditions using both thermal video cameras and acoustic detectors. Simultaneous video and audio recordings from 20 nights of observation at 10 sites were analyzed for correspondence between detection methods, with a focus on video observations in three distance categories for which accompanying vocalizations were detected. Comparison of video and audio detections revealed that a high proportion of Hawaiian hoary bats “seen” on video were not simultaneously “heard.” On average, only about one in three visual detections within a night had an accompanying call detection, but this varied greatly among nights. Bats flying on curved flight paths and individuals nearer the cameras were more likely to be detected by both methods. Feeding and social calls were detected, but no clear pattern emerged from the small number of observations involving closely interacting bats. These results may indicate that flying Hawaiian hoary bats often forgo echolocation, or do not always vocalize in a way that is detectable with common sampling and monitoring methods. Possible reasons for the low correspondence between visual and acoustic detections range from methodological to biological and include a number of biases associated with the propagation and detection of sound, cryptic foraging strategies, or conspecific presence. Silent flight behavior may be more prevalent in echolocating bats than previously appreciated, has profound implications for ecological research, and deserves further characterization and study.     

Effectiveness of acoustic lures for increasing tropical forest understory bat captures

Bats are the most diverse mammalian order second to rodents, with 1400+ species globally. In the tropics, it is possible to find more than 60 bat species at a single site. However, monitoring bats is challenging due to their small size, ability to fly, cryptic nature, and nocturnal activity. Recently, bioacoustic techniques have been incorporated into survey methods, either through passive acoustic monitoring or acoustic bat lures. Lures have been developed on the premise that broadcasting acoustic stimuli increases the number of captures in harp traps or mist nets. However, this is a relatively new, niche method. This study tested the efficacy of two commonly used acoustic bat lure devices, broadcasting two different acoustic stimuli, to increase forest understory bat captures in the tropics. This is the first time an acoustic bat lure has been systematically tested in a tropical rainforest, and the first study to compare two lure devices (Sussex AutoBat and Apodemus BatLure). Using a paired experimental design, two synthesized acoustic stimuli were broadcasted, a feeding call and a social call, to understand the importance of the call type used on capture rates and genus‐specific responses. Using an acoustic lure significantly increased capture rates, while the type of device did not impact capture rates. The two acoustic stimuli had an almost even distribution of captures, suggesting that the type of call may be less important than previously thought. Results indicate a possible deterrent effect on Rhinolophous sp., while being particularly effective for attracting bats in the genera Murina and Kerivoula. This study highlights the effectiveness of lures, however, also indicates that lure effects can vary across genera. Therefore, lures may bias survey results by altering the species composition of bats caught. Future research should focus on a single species or genus, using synthesized calls of conspecifics, to fully understand the effect of lures.     

Bats probe the aerosphere during landscape‐guided altitudinal flights

As the only mammals capable of powered flight, bats make efficient use of the aerosphere. Yet, our understanding of how bats use the three‐dimensional air column is sketchy. By attaching miniaturised Global Positioning System tags to cave bats near a mountain ridge in Thailand, we show that these bats perform undulating ascending and descending flights in quick succession. Bats repeatedly used mountain slopes to ascend to altitudes of more than 550 m above the ground. We infer that mountain ridges are key habitat features for some open‐space foraging bats, facilitating altitudinal movements which may aid effective foraging and navigation. Therefore, the development of wind farms along mountain ridges might lead to conflicts with the conservation of some open‐space foraging bats.     

Activity levels of bats and katydids in relation to the lunar cycle

Animals are exposed to many conflicting ecological pressures, and the effect of one may often obscure that of another. A likely example of this is the so-called “lunar phobia” or reduced activity of bats during full moon. The main reason for lunar phobia was thought to be that bats adjust their activity to avoid predators. However, bats can be prey, but many are carnivorous and therefore predators themselves. Thus, they are likely to be influenced by prey availability as well as predation risk. We investigated the activity patterns of the perch-hunting Lophostoma silvicolum and one of its main types of prey, katydids, to assess the influence of the former during different phases of the lunar cycle on a gleaning insectivorous bat. To avoid sampling bias, we used sound recordings and two different capture methods for the katydids, as well as video monitoring and radio-telemetry for the bats. Both, bats and katydids were significantly more active during the dark periods associated with new moon compared to bright periods around the full moon. We conclude that foraging activity of L. silvicolum is probably influenced by prey availability to a large extent and argue that generally the causes of lunar phobia are species-specific.     

Does interspecific competition drive patterns of habitat use in desert bat communities?

Bodies of water are a key foraging habitat for insectivorous bats. Since water is a scarce and limiting resource in arid environments, bodies of open water may have a structuring effect on desert bat communities, resulting in temporal or spatial partitioning of bat activity. Using acoustic monitoring, we studied the spatial and temporal activity patterns of insectivorous bats over desert ponds, and hypothesised that sympatric bat species partition the foraging space above ponds based on interspecific competitive interactions. We used indirect measures of competition (niche overlap and competition coefficients from the regression method) and tested for differences in pond habitat selection and peak activity time over ponds. We examined the effect of changes in the activity of bat species on their potential competitors. We found that interspecific competition affects bat community structure and activity patterns. Competing species partitioned their use of ponds spatially, whereby each species was associated with different pond size and hydroperiod (the number of months a pond holds water) categories, as well as temporally, whereby their activity peaked at different hours of the night. The drying out of temporary ponds increased temporal partitioning over permanent ponds. Differences in the activity of species over ponds in response to the presence or absence of their competitors lend further support to the role of interspecific competition in structuring desert bat communities. We suggest that habitat use and night activity pattern of insectivorous bats in arid environments reflect the trade-offs between selection of preferred pond type or activity time and constraints posed by competitive interactions.     

EFFECT OF HABITAT AND FORAGING HEIGHT ON BAT ACTIVITY IN THE COASTAL PLAIN OF SOUTH CAROLINA

Abstract: We compared bat activity levels in the Coastal Plain of South Carolina among 5 habitat types: forested riparian areas, clearcuts, young pine plantations, mature pine plantations, and pine savannas. We used time-expansion radio-microphones and integrated detectors to simultaneously monitor bat activity at 3 heights (30, 10, 2 m) in each habitat type. Variation in vegetative clutter among sampling heights and among habitat types allowed us to examine the differential effect of forest vegetation on the spatial activity patterns of clutter-adapted and open-adapted bat species. Moreover, monitoring activity at 30, 10, and 2 m permitted us to also compare bat activity above and below the forest canopy. We detected calls of 5 species or species groups: eastern red/Seminole bats (Lasiurus borealis/L. seminolus), eastern pipistrelles (Pipistrellus subflavus), evening bats (Nycticeius humeralis), big brown bats (Eptesicus fuscus), and hoary bats (Lasiurus cinerius). At 2 and 10 m, bat activity was concentrated in riparian areas, whereas we detected relatively low levels of bat activity in upland habitats at those heights. Activity was more evenly distributed across the landscape at 30 m. Bat activity levels above the forest canopy were almost 3 times greater than within or below the canopy. We detected significantly greater activity levels of 2 open-adapted species (hoary and big brown bats) above rather than within or below the forest canopy. However, activity levels of 2 clutter-adapted species (eastern red/Seminole bats and eastern pipistrelles) did not differ above, within, or below the forest canopy. Despite classification as a clutter-adapted species, evening bat activity was greater above rather than within or below the forest canopy. We believe our results highlight the importance of riparian areas as foraging habitat for bats in pine-dominated landscapes in the southeastern United States. Although acoustical surveys conducted below forest canopies can provide useful information about species composition and relative activity levels of bats that forage in cluttered environments, our results showing activity above canopy suggest that such data may not accurately reflect relative activity of bats adapted to forage in more open conditions, and therefore may provide an inaccurate picture of bat community assemblage and foraging habitat use.     

Influences of Landscape Features on Bat Activity in North Dakota

Land conversion and modification threatens many wildlife and plant species in the northern Great Plains, including bats. Our objective was to assess the association of bat species with landscape features in the northern Great Plains of North Dakota, USA, taking the first step towards understanding the habitat needs of bats in this region. We examined patterns of bat activity across different landscapes, identified those landscape features associated with high levels of bat activity, and determined which specific land features (i.e., vegetation and water types) were most commonly associated with each bat species. We used passive acoustic monitoring to measure bat activity at sites across North Dakota, and assessed detailed land characteristics at each site. We used nonmetric multidimensional scaling and multivariate regression tree analysis to examine relationships between bat activity and landscape variables. Bat foraging activity was influenced by structural landscape characteristics and the availability of specific water resources. High levels of bat activity were associated with riparian forested areas of varying structural complexity, ponds, and, to a lesser extent, open riparian lands. Individual bat species were influenced by land type and water resources differently. We identified big brown bats (Eptesicus fuscus) and little brown bats (Myotis lucifugus) as indicators of open riparian and pond landscapes, respectively. These results highlight the importance of prairie riparian landscapes and maintaining heterogeneity across the landscape for conservation and management of bat communities. Further, we identified ponds as an important landscape feature for little brown bats, a species of conservation concern, indicating that this specific feature should be a focus of conservation efforts on prairie wetlands. © 2019 The Wildlife Society.     

The Importance of Acacia Trees for Insectivorous Bats and Arthropods in the Arava Desert

Anthropogenic habitat modification often has a profound negative impact on the flora and fauna of an ecosystem. In parts of the Middle East, ephemeral rivers (wadis) are characterised by stands of acacia trees. Green, flourishing assemblages of these trees are in decline in several countries, most likely due to human-induced water stress and habitat changes. We examined the importance of healthy acacia stands for bats and their arthropod prey in comparison to other natural and artificial habitats available in the Arava desert of Israel. We assessed bat activity and species richness through acoustic monitoring for entire nights and concurrently collected arthropods using light and pit traps. Dense green stands of acacia trees were the most important natural desert habitat for insectivorous bats. Irrigated gardens and parks in villages and fields of date palms had high arthropod levels but only village sites rivalled acacia trees in bat activity level. We confirmed up to 13 bat species around a single patch of acacia trees; one of the richest sites in any natural desert habitat in Israel. Some bat species utilised artificial sites; others were found almost exclusively in natural habitats. Two rare species (Barbastella leucomelas and Nycteris thebaica) were identified solely around acacia trees. We provide strong evidence that acacia trees are of unique importance to the community of insectivorous desert-dwelling bats, and that the health of the trees is crucial to their value as a foraging resource. Consequently, conservation efforts for acacia habitats, and in particular for the green more densely packed stands of trees, need to increase to protect this vital habitat for an entire community of protected bats.     

Bats partition activity in space and time in a large,heterogeneous landscape

Diverse species assemblages theoretically partition along multiple resource axes to maintain niche separation between all species. Temporal partitioning has received less attention than spatial or dietary partitioning but may facilitate niche separation when species overlap along other resource axes. We conducted a broad‐scale acoustic study of the diverse and heterogeneous Great Smoky Mountains National Park in the Appalachian Mountains. Between 2015 and 2016, we deployed acoustic bat detectors at 50 sites (for a total of 322 survey nights). We examined spatiotemporal patterns of bat activity (by phonic group: Low, Mid, and Myotis) to test the hypothesis that bats partition both space and time. Myotis and Low bats were the most spatially and temporally dissimilar, while Mid bats were more general in their resource use. Low bats were active in early successional openings or low‐elevation forests, near water, and early in the evening. Mid bats were similarly active in all land cover classes, regardless of distance from water, throughout the night. Myotis avoided early successional openings and were active in forested land cover classes, near water, and throughout the night. Myotis and Mid bats did not alter their spatial activity patterns from 2015 to 2016, while Low bats did. We observed disparate temporal activity peaks between phonic groups that varied between years and by land cover class. The temporal separation between phonic groups relaxed from 2015 to 2016, possibly related to changes in the relative abundance of bats or changes in insect abundance or diversity. Temporal separation was more pronounced in the land cover classes that saw greater overall bat activity. These findings support the hypothesis that niche separation in diverse assemblages may occur along multiple resource axes and adds to the growing body of evidence that bats partition their temporal activity.     

Morphology,Diet and Flower‐visiting by Phyllostomid Bats in Cuba

Pollinator morphology can play an important role in structuring plant–pollinator relationships and a pollinator's morphology may be associated with aspects of its diet. We examined the relationship between morphology and the partitioning of flower‐based food resources for five species of flower‐visiting Cuban bats: Artibeus jamaicensis, Brachyphylla nana, Erophylla sezekorni, Monophyllus redmani and Phyllonycteris poeyi. We analyzed cranial traits and body size to assess differences among species with respect to morphological specializations. We also collected dietary data from guano and used acoustic monitoring to assess bat activity at flowers. We found evidence that bats partition floral resources, but we found no direct evidence that plants were limiting resources for the bats. Morphological similarity among bat species did not predict dietary overlap. Rather it was associated with phylogenic relationships among some species. Species with different morphological specialization for flower‐visiting consumed resources and visited food plants at different frequencies.     

Habitat-associated and temporal patterns of bat activity in a diverse forest landscape of southern New England, USA

The development and use of acoustic recording technology, surveys have revealed the composition, relative levels of activity, and preliminary habitat use of bat communities of various forest locations. However, detailed examinations of acoustic surveys results to investigate temporal patterns of bat activity are rare. Initial active acoustic surveys of bat activity on the Quabbin Reservoir watershed in central Massachusetts recorded high numbers of call sequences by five bat species. The results showed the importance of aquatic and open habitats for bats in this diverse forest landscape. Because the preliminary surveys were restricted in extent (habitats), number (replicates), and duration (active surveys only, limited number of repeated surveys), the authors strongly recommended more comprehensive and extensive surveys of bat activity on the area. This paper reports the results of active (manual) and passive (automated) acoustic bat activity surveys in three replicates of ten habitats, conducted three to four times per year over the course of the study between 2004 and 2006. Over the full study, 2,800 actively-recorded 37,632 passively-recorded call sequences were examined and identified to species when possible. General patterns in activity did not differ by habitat between the two survey methods. Call sequences were recorded more often in open, especially aquatic habitats than in cluttered habitats. The use of passive surveys allowed for the assessment of temporal patterns of activity and an analysis of the relationship between ambient temperature and activity.     

Temporally adaptive acoustic sampling to maximize detection across a suite of focal wildlife species

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Weather conditions determine attenuation and speed of sound: Environmental limitations for monitoring and analyzing bat echolocation

Echolocating bats are regularly studied to investigate auditory‐guided behaviors and as important bioindicators. Bioacoustic monitoring methods based on echolocation calls are increasingly used for risk assessment and to ultimately inform conservation strategies for bats. As echolocation calls transmit through the air at the speed of sound, they undergo changes due to atmospheric and geometric attenuation. Both the speed of sound and atmospheric attenuation, however, are variable and determined by weather conditions, particularly temperature and relative humidity. Changing weather conditions thus cause variation in analyzed call parameters, limiting our ability to detect, and correctly analyze bat calls. Here, I use real‐world weather data to exemplify the effect of varying weather conditions on the acoustic properties of air. I then present atmospheric attenuation and speed of sound for the global range of weather conditions and bat call frequencies to show their relative effects. Atmospheric attenuation is a nonlinear function of call frequency, temperature, relative humidity, and atmospheric pressure. While atmospheric attenuation is strongly positively correlated with call frequency, it is also significantly influenced by temperature and relative humidity in a complex nonlinear fashion. Variable weather conditions thus result in variable and unknown effects on the recorded call, affecting estimates of call frequency and intensity, particularly for high frequencies. Weather‐induced variation in speed of sound reaches up to about ±3%, but is generally much smaller and only relevant for acoustic localization methods of bats. The frequency‐ and weather‐dependent variation in atmospheric attenuation has a threefold effect on bioacoustic monitoring of bats: It limits our capability (1) to monitor bats equally across time, space, and species, (2) to correctly measure frequency parameters of bat echolocation calls, particularly for high frequencies, and (3) to correctly identify bat species in species‐rich assemblies or for sympatric species with similar call designs.     

Winter behavior of bats and the progression of white‐nose syndrome in the southeastern United States

Understanding the winter behavior of bats in temperate North America can provide insight into how bats react to perturbations caused by natural disturbances such as weather, human‐induced disturbances, or the introduction of disease. This study measured the activity patterns of bats outside of their hibernaculum and asked how this winter activity varied by time, temperature, bat species, body condition, and WNS status. Over the course of three winters (2011–2013), we collected acoustic data and captured bats outside of five hibernacula in Tennessee, United States. During this time, Pseudogymnoascus destructans, the causative agent of white‐nose syndrome, became established in hibernacula throughout the region, allowing us to track disease‐related changes in the winter behavior of ten bat species. We determined that bats in the southeastern United States were active during winter regardless of disease. We recorded activity outside of hibernacula at temperatures as low as ?13°C. Although bat activity was best determined by a combination of variables, the strongest factor was mean daily temperature (R ² = .2879, F _1,1450 = 586.2, p  < .0001). Bats that left the hibernacula earlier in evening had lower body condition than those that left 2–4 hr after sunset (F _7,932 = 7.225, p  < .0001, Tukey HSD, p  < .05). The number of daytime emergences from hibernacula, as determined via acoustic detection, increased the longer a site was P. destructans positive (F _{3,17 808} = 124.48, p  < .0001, Tukey HSD, p  < .05). Through the use of passive acoustic monitoring and monthly captures, we determined that winter activity was driven by both ambient temperature and the presence of P. destructans .