Sebaceous Lipid Profiling of Bat Integumentary Tissues: Quantitative Analysis of Free Fatty Acids,Monoacylglycerides, Squalene,and Sterols

White‐nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans and is devastating North American bat populations. Sebaceous lipids secreted from host integumentary tissues are implicated in the initial attachment and recognition of host tissues by pathogenic fungi. We are interested in determining if ratios of lipid classes in sebum can be used as biomarkers to diagnose severity of fungal infection in bats. To first establish lipid compositions in bats, we isolated secreted and integral lipid fractions from the hair and wing tissues of three species: big brown bats (Eptesicus fuscus), Eastern red bats (Lasiurus borealis), and evening bats (Nycticeius humeralis). Sterols, FFAs, MAGs, and squalene were derivatized as trimethylsilyl esters, separated by gas chromatography, and identified by mass spectrometry. Ratios of sterol to squalene in different tissues were determined, and cholesterol as a disease biomarker was assessed. Free sterol was the dominant lipid class of bat integument. Squalene/sterol ratio is highest in wing sebum. Secreted wing lipid contained higher proportions of saturated FFAs and MAGs than integral wing or secreted hair lipid. These compounds are targets for investigating responses of P. destructans to specific host lipid compounds and as biomarkers to diagnose WNS.     

Organization of the primary somatosensory cortex and wing representation in the Big Brown Bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Bats are the only mammals capable of true powered flight. The bat wing exhibits specializations, allowing these animals to perform complicated flight maneuvers like landing upside-down, and hovering. The wing membrane contains various tactile receptors, including hair-associated Merkel receptors that might be involved in stabilizing bat flight. Here, we studied the neuronal representation of the wing membrane in the primary somatosensory cortex (S1) of the anesthetized Big Brown Bat, Eptesicus fuscus, using tactile stimulation with calibrated monofilaments (von Frey hairs) while recording from multi-neuron clusters. We also measured cortical response thresholds to tactile stimulation of the wings.The body surface is mapped topographically across the surface of S1, with the head, foot, and wing being overrepresented. The orientation of the wing representation is rotated compared to the hand representaion of terrestrial mammals, confirming results from other bat species. Although different wing membrane parts derive embryologically from different body parts, including the flank (plagiopatagium), the tactile sensitivity of the entire flight membrane (0.2–1.2 mN) is remarkably close or even higher (dactylopatagium) than the average tactile sensitivity of the human fingertip.     

Target-detection by the echolocating bat,Eptesicus fuscus

Summary The long-range echo-detection capabilities of echolocating bats (Eptesicus fuscus) were studied in a two-choice psychophysical procedure.E. fuscus can detect 4.8 mm diameter spheres at a distance of 2.9 m, and 19.1 mm diameter spheres at a distance of 5.1 m. The threshold of echo-detection corresponds to the distance at which a target returns an echo amplitude in the region of 0 dB SPL. The results demonstrate that the maximum effective range of bat sonar is greater than previously indicated by obstacleavoidance and target-interception tasks.     

Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat

Patterns of offspring development reflect the availability of energy and nutrients, limitations on an individual’s capacity to use available resources, and tradeoffs between the use of nutrients to support current metabolic demands and tissue growth. To determine if the long period of offspring dependency in bats is associated with the need for an advanced state of tissue maturation prior to flight, we examined body composition during postnatal growth in the big brown bat, Eptesicus fuscus. Despite their large size at birth (22% of maternal mass), newborn bats are relatively immature, containing 82% body water in fat-free mass. However, the total body water content of newborn bat pups decreases to near-adult levels in advance of weaning, while concentrations of total body fat and protein exceed adult values. In contrast to many other mammals, postnatal growth of bat pups was characterized by relatively stable concentrations of calcium and phosphorus, but declining concentrations of magnesium. These levels remained stable or rebounded in late postnatal development. This casts doubt on the hypothesis that low rates of mineral transfer necessitate an extended lactation period in bats. However, our finding of near-adult body composition at weaning is consistent with the hypothesis that extended lactation in bats is necessary for the young to achieve sufficient tissue maturity to undertake the active flight necessary for independent feeding. In this respect, bats differ from most other mammals but resemble birds that must engage in active flight to achieve nutritional independence.     

Plasma leptin decreases during lactation in insectivorous bats

We previously demonstrated high leptin levels during late pregnancy in little brown bats (Myotis lucifugus). We now extend these observations to a second species, the big brown bat (Eptesicus fuscus), and also report that leptin increases after the first trimester of pregnancy. Leptin decreased to baseline 1 week following parturition, with a half-time decay of 2 days. During lactation, leptin was significantly correlated with body mass in E. fuscus, but not in M. lucifugus. No circadian pattern of leptin was observed in M. lucifugus. The decrease in post-partum leptin in bats may be partly explained by loss of putative placental leptin. The continued decrease may reflect depletion of body fat during this energy demanding period, at least in Eptesicus. Changes in leptin during lactation appeared to be independent of circadian effects and time of sampling. Our study provides additional evidence that leptin increases during pregnancy and declines during lactation in a free-ranging mammal, supporting the hypothesis that leptin plays important but yet undetermined roles in reproduction. Accepted: 4 October 1998     

Predictive Occurrence Models for Bat Species in California

Abstract: The ability to accurately predict the potential occurrence of species of management concern is useful for wildlife managers, particularly for those whose management activities involve large areas where sampling is difficult due to logistical or financial constraints. During the summers of 2002 and 2003, we used mist nets to capture bats (Myotis yumanensis, M. californicus, M. evotis, M. thysanodes, Eptesicus fuscus, Lasionycteris noctivagans, Tadarida brasiliensis, Antrozous pallidus, Lasiurus borealis, and Lasiurus cinereus) in Whiskeytown National Recreation Area in north-central California, USA. We used landscape-scale variables, logistic regression, and Akaike's Information Criterion (AIC_c) to model species distributions and produce spatially discerning predictive occurrence maps. We developed a priori models that we used to determine which landscape-scale variables best discriminated between capture sites and non-capture sites. The odds of capturing a bat were 3.3 greater when total edge increased by 10,000 m, whereas for Yuma myotis (Myotis yumanensis), the odds of predicting presence were 0.2 greater when distance to lakes and ponds decreased by 2,000 m. Elevation was important in predicting the distribution of silver-haired bats (Lasionycteris noctivagans) and big brown bats (Eptesicus fuscus). Increasing elevation by 400 m decreased the odds of capturing a silver-haired bat by 0.1 and a big brown bat by 0.4. Classification accuracy for our models ranged from 80.9% for all bat species combined to 72.3% for Yuma myotis and silver-haired bats. Predictive occurrence models can be valuable to bat conservation efforts because they provide spatial data important for evaluating the effects of management activities on species distributions.     

Habitat use, diet and roost selection by the Big Brown Bat (Eptesicus fuscus) in North America: a case for conserving an abundant species

Insectivorous bats are integral components of terrestrial ecosystems. Despite this, a growing number of factors causing world‐wide declines in bat populations have been identified. Relatively abundant species are important for bat conservation because of their role in ecosystems and the research opportunities they offer. In addition, species that have been well‐studied present unique opportunities to synthesize information and highlight important areas of focus for conservation and research. This paper focuses on a well‐studied abundant bat, Eptesicus fuscus. I review the relevant literature on habitat use, diet and roost selection by E. fuscus in North America, and highlight important areas of conservation and research for this species, including the effects of roost disturbance, control of economically important insect pests, exposure to pesticides, long‐term monitoring of populations, and the potential consequences of expanding populations. These issues have broad implications for other species and can be used to focus future research and conservation efforts.     

Complex sound analysis in the FM bat Eptesicus fuscus,correlated with structural parameters of frequency modulated signals

Big brown bats, Eptesicus fuscus, were presented with artificial frequency modulated (FM) echoes that simulated an object becoming progressively closer to the bat. A stereotyped approach phase behavioral response of the bat to the virtual approaching target was used to determine the ability of the bat to analyze FM signals for target distance information. The degree to which the bats responded with approach phase behavior to a virtual approaching target was similar when they were presented with either a naturally structured artificial FM echo or an artificial FM echo constructed from a series of brief pure tone steps. The ability of the bats to respond to an FM signal structured from a sequence of pure tone elements depended on the number of pure tone steps in the series; the bats required the presentation of tone-step FM signals containing about 83 or greater pure tone elements. Moreover, the duration of the individual tone steps of the tone-step FM signals could not exceed a specific upper limit of about 0.05 ms. Finally, it appears that the bats were able to independently resolve individual tone steps within the tone-step FM signals that were separated by about 450 Hz or more.Abbreviations CF constant frequency - FM frequency modulation     

Curtailment and acoustic deterrents reduce bat mortality at wind farms

The impacts of wind energy on bat populations is a growing concern because wind turbine blades can strike and kill bats, and wind turbine development is increasing. We tested the effectiveness of 2 management actions at 2 wind-energy facilities for reducing bat fatalities: curtailing turbine operation when wind speeds were <5.0 m/second and combining curtailment with an acoustic bat deterrent developed by NRG Systems. We measured the effectiveness of the management actions using differences in counts of bat carcasses quantified by daily and twice-per-week standardized carcass searches of cleared plots below turbines, and field trials that estimated searcher efficiency and carcass persistence. We studied turbines located at 2 adjacent wind-energy facilities in northeast Illinois, USA, during fall migration (1 Aug–15 Oct) in 2018. We estimated the effectiveness of each management action using a generalized linear mixed-effects model with several covariates. Curtailment alone reduced overall bat mortality by 42.5% but did not reduce silver-haired bat (Lasionycteris noctivagans) mortality. Overall bat fatality rates were 66.9% lower at curtailed turbines with acoustic deterrents compared to turbines that operated at manufacturer cut-in speed. Curtailment and the deterrent reduced bat mortality to varying degrees between species, ranging from 58.1% for eastern red bats (Lasiurus borealis) to 94.4 for big brown bats (Eptesicus fuscus). Hoary (Lasiurus cinereus) and silver-haired bat mortality was reduced by 71.4% and 71.6%, respectively. Our study lacked a deterrent-only treatment group because of the expense of acoustic deterrents. We estimated the additional reduction in mortality with concurrent deployment of the acoustic deterrent and curtailment under the assumption that curtailment and the acoustic deterrent would have reduced mortality by the same percentage at adjacent wind-energy facilities. Acoustic deterrents resulted in 31.6%, 17.4%, and 66.7% additional reductions of bat mortality compared to curtailment alone for eastern red bat, hoary bat, and silver-haired bat, respectively. The effectiveness of acoustic deterrents for reducing bat mortality at turbines with rotor-swept area diameters >110 m is unknown because high frequency sound attenuates quickly, which reduces coverage of rotor-swept areas. Management actions should consider species differences in the ability of curtailment and deterrents to reduce bat mortality and increase energy production.     

Phase evaluation in hypothetical receivers simulating ranging in bats

Echo delay discrimination by the bat Eptesicus fuscus had been investigated in an experiment with simulated targets jittering in range (Simmons 1979). The dip in the resulting psychometric curve was used by Simmons to suggest the neuronal implementation of a coherent cross-correlation receiver in the auditory system of bats. By computer simulation it is shown here that the dip may be even more pronounced and less susceptible to noise with alternative receiver configurations which not necessarily evaluate signal phase information coherently, e.g., a bank of neuronal filters with envelope-processing. New behavioral experiments are suggested to critically test such model hypotheses.     

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.     

Observational learning in three species of insectivorous bats (Chiroptera)

The potential importance of observational learning has been discussed for many orders of animals, but experimental evidence of this phenomenon in undomesticated mammals other than primates is rate. In this study three species of insectivorus vesperilionid bats (Myotis lucifugus, Eptesicus fuscus and Antrozous pallidus) acquired a novel feeding behaviour through interaction with a knowledgeable conspecific or, in some cases, a bat of another species. The response was not acquired through trial-and-error learning, and conditioning the response took significantly longer than acqisition by observing another bat.     

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.     

Disease‐related population declines in bats demonstrate non‐exchangeability in generalist predators

The extent to which persisting species may fill the functional role of extirpated or declining species has profound implications for the structure of biological communities and ecosystem functioning. In North America, arthropodivorous bats are threatened on a continent‐wide scale by the spread of white‐nose syndrome (WNS), a disease caused by the fungus Pseudogymnoascus destructans. We tested whether bat species that display lower mortality from this disease can partially fill the functional role of other bat species experiencing population declines. Specifically, we performed high‐throughput amplicon sequencing of guano from two generalist predators: the little brown bat (Myotis lucifugus) and big brown bat (Eptesicus fuscus). We then compared changes in prey consumption before versus after population declines related to WNS. Dietary niches contracted for both species after large and abrupt declines in little brown bats and smaller declines in big brown bats, but interspecific dietary overlap did not change. Furthermore, the incidence and taxonomic richness of agricultural pest taxa detected in diet samples decreased following bat population declines. Our results suggest that persisting generalist predators do not necessarily expand their dietary niches following population declines in other predators, providing further evidence that the functional roles of different generalist predators are ecologically distinct.     

Discrimination of wingbeat motion by bats,correlated with echolocation sound pattern

Summary Bats of the species Rhinolophus rouxi, Hipposideros lankadiva and Eptesicus fuscus were trained to discriminate between two simultaneously presented artificial insect wingbeat targets moving at different wingbeat rates. During the discrimination trials, R. rouxi, H. lankadiva and E. fuscus emitted long-CF/FM, short-CF/FM and FM echolocation sounds respectively. R. rouxi, H. lankadiva and E. fuscus were able to discriminate a difference in wingbeat rate of 2.7 Hz, 9.2 Hz and 15.8 Hz, respectively, between two simultaneously presented targets at an absolute wingbeat rate of 60 Hz, using a criterion of 75% correct responses.The performance of the different bat species is correlated with the echolocation signal design used by each species, particularly with the presence and relative duration of a narrowband component preceding a broadband FM component. These results provide behavioral evidence supporting the hypothesis that bats that use CF/FM echolocation sounds have adaptations for the perception of insect wingbeat motion and that long-CF/FM species are more specialized for this task than short-CF/FM species.Abbreviations CF constant frequency - FM frequency modulation     

Bat Response to Woodland Restoration within Urban Forest Fragments

In urban environments, woodland areas are typically fragmented and subject to invasive species encroachment, woody overgrowth, and natural succession. In response to negative impacts, conservationists and land managers have implemented restoration strategies to enhance the integrity of woodlands. Because woodland habitat is important for bats (Order Chiroptera), alterations to forest structures may affect how bats utilize forest fragments in urban environments. We evaluated relationships among restoration efforts, microhabitat characteristics and overall bat activity, and interspecific variation among bats in response to woodland characteristics. We monitored bats in nine woodland forest preserves representing various stages of restoration within the Chicago metropolitan area in 2004 and 2005. Overall bat activity was positively related to prescribed burning, invasive species removal, and small tree density (7.7‐20 cm dbh) and inversely related to shrub density and clutter at 0‐6 m heights. There was interspecific variation in response to alterations in woodland structure, with Lasiurus borealis (L. borealis) positively associated with small and medium (20.1‐33 cm) tree densities and inversely related to clutter at 0‐9 m; Myotis spp. positively associated with canopy cover, clutter at 6‐9 m, and small and medium tree densities; and Lasionycteris noctivagans (L. noctivagans) positively associated with more open forests. Eptesicus fuscus (E. fuscus) activity was not strongly associated with any measured vegetation variable. Our results demonstrate bats positively respond to some forms of woodland restoration in urban landscapes. However, species‐specific responses to vegetation differed and should be taken into consideration when developing management plans.     

Separating the effects of water quality and urbanization on temperate insectivorous bats at the landscape scale

Many local scale studies have shown that bats respond to water quality degradation or urbanization in a species‐specific manner. However, few have separated the effects of urbanization versus water quality degradation on bats, in single city or single watershed case studies. Across North Carolina, USA, we used the standardized North American Bat Monitoring Program mobile transect protocol to survey bat activity in 2015 and 2016 at 41 sites. We collected statewide water quality and urban land cover data to disentangle the effects of urbanization and water quality degradation on bats at the landscape scale. We found that statewide, water quality degradation and urbanization were not correlated. We found that bats responded to water quality degradation and urbanization independently at the landscape scale. Eptesicus fuscus and Lasiurus cinereus negatively responded to water quality degradation. Lasiurus borealis and Perimyotis subflavus positively responded to water quality degradation. Lasionycteris noctivagans did not respond to water quality degradation but was more active in more urbanized areas. Tadarida brasiliensis positively responded to urbanization and was less active in areas with degraded water quality. We show that bat–water quality relationships found at the local scale are evident at a landscape scale. We confirm that bats are useful bioindicators for both urbanization and water quality degradation. We suggest that water quality can be used to predict the presence of bat species of conservation concern, such as P. subflavus, in areas where it has not been studied locally.     

Habitat associations of bats in a working rangeland landscape

Land‐use change has resulted in rangeland loss and degradation globally. These changes include conversion of native grasslands for row‐crop agriculture as well as degradation of remaining rangeland due to fragmentation and changing disturbance regimes. Understanding how these and other factors influence wildlife use of rangelands is important for conservation and management of wildlife populations. We investigated bat habitat associations in a working rangeland in southeastern North Dakota. We used Petterson d500x acoustic detectors to systematically sample bat activity across the study area on a 1‐km point grid. We identified calls using Sonobat autoclassification software. We detected five species using this working rangeland, which included Lasionycteris noctivagans (2,722 detections), Lasiurus cinereus (2,055 detections), Eptesicus fuscus (749 detections), Lasiurus borealis (62 detections), and Myotis lucifugus (1 detection). We developed generalized linear mixed‐effects models for the four most frequently detected species based on their ecology. The activity of three bat species increased with higher tree cover. While the scale of selection varied between the four species, all three investigated scales were explanatory for at least one bat species. The broad importance of trees to bats in rangelands may put their conservation needs at odds with those of obligate grassland species. Focusing rangeland bat conservation on areas that were treed prior to European settlement, such as riparian forests, can provide important areas for bat conservation while minimizing negative impacts on grassland species.     

GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse–echo pairs

When insectivorous bats such as Eptesicus fuscus emit ultrasonic signals and analyze the returning echoes to hunt insects, duration selectivity of auditory neurons plays an important role in echo recognition. The success of prey capture indicates that they can effectively encode progressively shortened echo duration throughout the hunting process. The present study examines the echo duration selectivity of neurons in the central nucleus of the bat inferior colliculus (IC) under stimulation conditions of single pulses and pulse–echo (P–E) pairs. This study also examines the role of gamma-aminobutyric acid (GABA)ergic inhibition in shaping echo duration selectivity of IC neurons. The data obtained show that the echo duration selectivity of IC neurons is sharper when determined with P–E pairs than with single pulses. Echo duration selectivity also sharpens with shortening of pulse duration and P–E gap. Bicuculline application decreases and GABA application increases echo duration selectivity of IC neurons. The degree of change in echo duration selectivity progressively increases with shortening of pulse duration and P–E gap during bicuculline application while the opposite is observed during the GABA application. These data indicate that the GABAergic inhibition contributes to sharpening of echo duration selectivity of IC neurons and facilitates echo recognition by bats throughout different phases of hunting.