Publications

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comparative metabolomics of aging in a long-lived bat: insights into the physiology of extreme longevity.vespertilionid bats (mammalia: order chiroptera) live 3-10 times longer than other mammals of an equivalent body size. at present, nothing is known of how bat fecal metabolic profiles shift with age in any taxa. this study established the feasibility of using a non-invasive, fecal metabolomics approach to examine age-related differences in the fecal metabolome of young and elderly adult big brown bats (eptesicus fuscus) as an initial investigation into using metabolomics for age determination. s ...201829715267
smart bats click twice.the acoustic representation of the outside world in the midbrain of a bat becomes more precise as it uses double clicks to locate closer objects.201829651985
dynamic representation of 3d auditory space in the midbrain of the free-flying echolocating bat.essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. despite the importance of 3d spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2d, artificial stimuli. here, we show for the first time that sensory neurons in the midbrain superior colliculus (sc) of the free-flying echo ...201829633711
ddt poisoning of big brown bats, eptesicus fuscus, in hamilton, montana.dichlorodiphenyltrichloroethane (ddt) is an insecticidal organochlorine pesticide with; known potential for neurotoxic effects in wildlife. the united states environmental protection agency (us epa) registration for this pesticide has been cancelled and there are currently no federally active products that contain this ingredient in the u.s. we present a case of a colony of big brown bats (e. fuscus) found dead in the attic roost of an administrative building; in the city of hamilton, montana fr ...201829505918
spike train similarity space (ssims) method detects effects of obstacle proximity and experience on temporal patterning of bat biosonar.bats emit biosonar pulses in complex temporal patterns that change to accommodate dynamic surroundings. efforts to quantify these patterns have included analyses of inter-pulse intervals, sonar sound groups, and changes in individual signal parameters such as duration or frequency. here, the similarity in temporal structure between trains of biosonar pulses is assessed. the spike train similarity space (ssims) algorithm, originally designed for neural activity pattern analysis, was applied to de ...201829472848
spatial variation of mercury bioaccumulation in bats of canada linked to atmospheric mercury deposition.wildlife are exposed to neurotoxic mercury at locations distant from anthropogenic emission sources because of long-range atmospheric transport of this metal. in this study, mercury bioaccumulation in insectivorous bat species (mammalia: chiroptera) was investigated on a broad geographic scale in canada. fur was analyzed (n=1178) for total mercury from 43 locations spanning 20° latitude and 77° longitude. total mercury and methylmercury concentrations in fur were positively correlated with conce ...201829396333
from individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions.in most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. this is because individ ...201829395101
need for multiscale planning for conservation of urban bats.for over a century there have been continual efforts to incorporate nature into urban planning. these efforts (i.e., urban reconciliation) aim to manage and create habitats that support biodiversity within cities. given that species select habitat at different spatial scales, understanding the scale at which urban species respond to their environment is critical to the success of urban reconciliation efforts. we assessed species-habitat relationships for common bat species at 50-m, 500-m, and 1 ...201829124788
bat rabies in washington state: temporal-spatial trends and risk factors for zoonotic transmission (2000-2017).rabies is a zoonotic viral disease that can affect all mammals. in the united states, the majority of human rabies cases are caused by bats, which are the only known reservoirs for rabies virus (rabv) in washington state. we sought to characterize bat rabv epidemiology in washington among bats submitted by the public for rabv testing.201830300384
isolation, characterization and prevalence of a novel gammaherpesvirus in eptesicus fuscus, the north american big brown bat.little is known about the relationship of gammaherpesviruses with their bat hosts. gammaherpesviruses are of interest because of their long-term infection of lymphoid cells and their potential to cause cancer. here, we report the characterization of a novel bat herpesvirus isolated from a big brown bat (eptesicus fuscus) in canada. the genome of the virus, tentatively named eptesicus fuscus herpesvirus (efhv), is 166,748 base pairs. phylogenetically efhv is a member of gammaherpesvirinae, in whi ...201829407381
active acoustic interference elicits echolocation changes in heterospecific bats.echolocating bats often forage in the presence of both conspecific and heterospecific individuals, which have the potential to produce acoustic interference. recent studies have shown that at least one bat species, the brazilian free-tailed bat (tadarida brasiliensis), produces specialized social signals that disrupt the sonar of conspecific competitors. we herein discuss the differences between passive and active jamming signals and test whether heterospecific jamming occurs in species overlapp ...201829950451
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 cov ...201829321903
survey of parasitic bacteria in bat bugs, colorado.bat bugs (cimex adjunctus barber) (hemiptera: cimicidae) collected from big brown bats (eptesicus fuscus palisot de beauvoir) in colorado, united states were assessed for the presence of bartonella, brucella, and yersinia spp. using molecular techniques. no evidence of brucella or yersinia infection was found in the 55 specimens collected; however, 4/55 (7.3%) of the specimens were positive for bartonella dna. multi-locus characterization of bartonella dna shows that sequences in bat bugs are ph ...201829329460
interferon regulatory factor 3-mediated signaling limits middle-east respiratory syndrome (mers) coronavirus propagation in cells from an insectivorous bat.insectivorous bats are speculated to be ancestral hosts of middle-east respiratory syndrome (mers) coronavirus (cov). mers-cov causes disease in humans with thirty-five percent fatality, and has evolved proteins that counteract human antiviral responses. since bats experimentally infected with mers-cov do not develop signs of disease, we tested the hypothesis that mers-cov would replicate less efficiently in bat cells than in human cells because of its inability to subvert antiviral responses in ...201930781790
arousal from hibernation and reactivation of eptesicus fuscus gammaherpesvirus (efhv) in big brown bats.many viruses that cause serious and often fatal disease in humans have spilled over from bats. recent evidence suggests that stress may enhance virus shedding by bats increasing the possibility of transmission to other species. to understand the reasons for spillover is therefore important to determine the molecular pathways that link stress to virus reactivation and shedding in bats. we recently isolated and characterized a gammaherpesvirus (eptesicus fuscus herpesvirus, efhv) autochthonous to ...201930554475
lipolytic activity and the utilization of fatty acids associated with bat sebum by pseudogymnoascus destructans.pseudogymnoascus destructans is the causative agent of a fungal infection of bats known as white-nose syndrome (wns). since its discovery in 2006, it has been responsible for precipitous declines of several species of cave-dwelling north american bats. while numerous advancements in the understanding of the disease processes underlying wns have been made in recent years, there are still many aspects of wns, particularly with respect to pathogen virulence, that remain unknown. in this preliminary ...201931529298
a smart curtailment approach for reducing bat fatalities and curtailment time at wind energy facilities.the development and expansion of wind energy is considered a key global threat to bat populations. bat carcasses are being found underneath wind turbines across north and south america, eurasia, africa, and the austro-pacific. however, relatively little is known about the comparative impacts of techniques designed to modify turbine operations in ways that reduce bat fatalities associated with wind energy facilities. this study tests a novel approach for reducing bat fatalities and curtailment ti ...201930939226
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 u ...201930680140
incomer, a dd36e family of tc1/mariner transposons newly discovered in animals.the tc1/mariner superfamily might represent the most diverse and widely distributed group of dna transposons. several families have been identified; however, exploring the diversity of this superfamily and updating its classification is still ongoing in the life sciences.201931788035
winter habitats of bats in texas.few studies have described winter microclimate selection by bats in the southern united states. this is of particular importance as the cold-adapted fungus, pseudogymnoascus destructans, which causes the fatal bat disease white-nose syndrome (wns), continues to spread into southern united states. to better understand the suitability of winter bat habitats for the growth of p. destructans in this region, we collected roost temperature and vapor pressure deficit from 97 hibernacula in six ecoregio ...201931393965
frequency-modulated up-chirps produce larger evoked responses than down-chirps in the big brown bat auditory brainstem.in many mammals, upward-sweeping frequency-modulated (fm) sounds (up-chirps) evoke larger auditory brainstem responses than downward-sweeping sounds (down-chirps). to determine if similar effects occur in fm echolocating bats, auditory evoked responses (aers) in big brown bats in response to up-chirps and down-chirps at different chirp durations and levels were recorded. even though down-chirps are the biologically relevant stimulus for big brown bats, up-chirps typically evoked larger peaks in ...201931590554
rapid increases in bat activity and diversity after wetland construction in an urban ecosystem.wetland construction can mitigate the biodiversity and water quality losses associated with reduced natural wetland coverage. while beneficial effects of wetland construction for bats have been observed in natural and rural settings, the effects of wetland construction on bats in an urban ecosystem are less understood. we used passive acoustic monitoring to measure bat activity levels and diversity at two constructed wetlands and two control sites on the university of north carolina greensboro c ...201931564763
sonar strobe groups and buzzes are produced before powered flight is achieved in the juvenile big brown bat, eptesicus fuscus.laryngeally echolocating bats produce a rapid succession of echolocation calls just before landing. these landing buzzes exhibit an increase in call rate and a decrease in call peak frequency and duration relative to pre-buzz calls, and resemble the terminal buzz phase calls of an aerial hawking bat's echolocation attack sequence. sonar strobe groups (ssgs) are clustered sequences of non-buzz calls whose pulse intervals (pis) are fairly regular and shorter than the pis both before and after the ...201931548288
hypsugopoxvirus: a novel poxvirus isolated from hypsugo savii in italy.interest in bat-related viruses has increased considerably during the last decade, leading to the discovery of a rising number of new viruses in several bat species. poxviridae are a large, diverse family of dna viruses that can infect a wide range of vertebrates and invertebrates. to date, only a few documented detections of poxviruses have been described in bat populations on three different continents (america, africa, and australia). these viruses are phylogenetically dissimilar and have div ...201931248065
echolocating bats perceive natural-size targets as a unitary class using micro-spectral ripples in echoes.echolocating big brown bats emit frequency-modulated (fm) sounds covering ultrasonic frequencies in two harmonic sweeps (fm1 from 50-60 khz sweeping down to 20-25 khz, fm2 from 100-110 khz sweeping down to 45 khz). using a complex interplay of acoustic cues, the bats perceive object distance from echo delay and object shape from echo spectra. typical natural targets-flying insects-return discrete reflections, called glints, from prominent body parts (e.g., head, wings). insect sizes are mostly 0 ...201931021108
effect of sound pressure level on contralateral inhibition underlying duration-tuned neurons in the mammalian inferior colliculus.duration tuning in the mammalian inferior colliculus (ic) is created by the interaction of excitatory and inhibitory synaptic inputs. we used extracellular recordings and paired tone stimulation to measure the strength and time course of the contralateral inhibition underlying duration-tuned neurons (dtns) in the ic of the awake bat. the onset time of a short, best duration (bd), excitatory probe tone set to +10 db (re threshold) was varied relative to the onset of a longer-duration, nonexcitato ...201931017836
echolocating bats inspect and discriminate landmark features to guide navigation.landmark-guided navigation is a common behavioral strategy for way-finding, yet prior studies have not examined how animals collect sensory information to discriminate landmark features. we investigated this question in animals that rely on active sensing to guide navigation. four echolocating bats (eptesicus fuscus) were trained to use an acoustic landmark to find and navigate through a net opening for a food reward. in experimental trials, an object serving as a landmark was placed adjacent to ...201930936268
biosonar interpulse intervals and pulse-echo ambiguity in four species of echolocating bats.in complex biosonar scenes, the delay of echoes represents the spatial distribution of objects in depth. to avoid overlap of echo streams from successive broadcasts, individual echolocation sounds should only be emitted after all echoes of previous sounds have returned. however, close proximity of obstacles demands rapid pulse updates for steering to avoid collisions, which often means emitting a new sound before all of the previous echoes have returned. when two echo streams overlap, there is a ...201930877230
rabies outbreak in captive big brown bats (eptesicus fuscus) used in a white-nose syndrome vaccine trial.an outbreak of rabies occurred in a captive colony of wild-caught big brown bats (eptesicus fuscus). five of 27 bats exhibited signs of rabies virus infection 22-51 d after capture or 18-22 d after contact with the index case. rabid bats showed weight loss, aggression, increased vocalization, hypersalivation, and refusal of food. antigenic typing and virus sequencing confirmed that all five bats were infected with an identical rabies virus variant that circulates in e. fuscus in the us. two bats ...202031295082
novel and diverse non-rabies rhabdoviruses identified in bats with human exposure, south dakota, usa.bats are a host and reservoir for a large number of viruses, many of which are zoonotic. in north america, the big brown bat (eptesicus fuscus) is widely distributed and common. big brown bats are a known reservoir for rabies virus, which, combined with their propensity to roost in human structures, necessitates testing for rabies virus following human exposure. the current pandemic caused by severe acute respiratory syndrome coronavirus 2, likely of bat origin, illustrates the need for continue ...202033302422
seasonal transfer and quantification of urinary estradiol in the big brown bat (eptesicus fuscus).growing evidence shows that sex steroids not only act within the individual whose glands produce them; they can also act on proximate conspecifics. previous studies show that exogenous 17β-estradiol (e2) can be absorbed both nasally and percutaneously, arriving in blood, neural, reproductive, and peripheral tissues. when male bats were injected with radiolabeled e2 (3h-e2) and housed with females during the mating season, radioactivity was reliably measured in the females' tissues. the present s ...202031733210
estimation of spatiotemporal trends in bat abundance from mortality data collected at wind turbines.renewable energy sources, such as wind energy, are essential tools for reducing the causes of climate change, but wind turbines can pose a collision risk for bats. to date, the population-level effects of wind-related mortality have been estimated for only 1 bat species. to estimate temporal trends in bat abundance, we considered wind turbines as opportunistic sampling tools for flying bats (analogous to fishing nets), where catch per unit effort (carcass abundance per monitored turbine) is a pr ...202032424911
echolocating bats accumulate information from acoustic snapshots to predict auditory object motion.unlike other predators that use vision as their primary sensory system, bats compute the three-dimensional (3d) position of flying insects from discrete echo snapshots, which raises questions about the strategies they employ to track and intercept erratically moving prey from interrupted sensory information. here, we devised an ethologically inspired behavioral paradigm to directly test the hypothesis that echolocating bats build internal prediction models from dynamic acoustic stimuli to antici ...202033139550
north american big brown bats (eptesicus fuscus) harbor an exogenous deltaretrovirus.bats are the reservoir for a large number of zoonotic viruses, including members of coronaviridae (severe acute respiratory syndrome coronavirus [sars-cov] and sars-cov-2), paramyxoviridae (hendra and nipah viruses), rhabdoviridae (rabies virus), and filoviridae (ebola virus) as exemplars. many retroviruses, such as human immunodeficiency virus, are similarly zoonotic; however, only infectious exogenous gammaretroviruses have recently been identified in bats. here, viral metagenomic sequencing o ...202032968009
antifungal potential of the skin microbiota of hibernating big brown bats (eptesicus fuscus) infected with the causal agent of white-nose syndrome.little is known about skin microbiota in the context of the disease white-nose syndrome (wns), caused by the fungus pseudogymnoascus destructans (pd), that has caused enormous declines of hibernating north american bats over the past decade. interestingly, some hibernating species, such as the big brown bat (eptesicus fuscus), appear resistant to the disease and their skin microbiota could play a role. however, a comprehensive analysis of the skin microbiota of e. fuscus in the context of pd has ...202032793178
dolphin echo-delay resolution measured with a jittered-echo paradigm.biosonar echo delay resolution was investigated in four bottlenose dolphins (tursiops truncatus) using a "jittered" echo paradigm, where dolphins discriminated between electronic echoes with fixed delay and those whose delay alternated (jittered) on successive presentations. the dolphins performed an echo-change detection task and produced a conditioned acoustic response when detecting a change from non-jittering echoes to jittering echoes. jitter delay values ranged from 0 to 20 μs. a passive l ...202032752735
how frequency hopping suppresses pulse-echo ambiguity in bat biosonar.big brown bats transmit wideband fm biosonar sounds that sweep from 55 to 25 khz (first harmonic, fm1) and from 110 to 50 khz (second harmonic, fm2). fm1 is required to perceive echo delay for target ranging; fm2 contributes only if corresponding fm1 frequencies are present. we show that echoes need only the lowest fm1 broadcast frequencies of 25 to 30 khz for delay perception. if these frequencies are removed, no delay is perceived. bats begin echo processing at the lowest frequencies and accum ...202032632013
transcriptional host-pathogen responses of pseudogymnoascus destructans and three species of bats with white-nose syndrome.understanding how context (e.g., host species, environmental conditions) drives disease susceptibility is an essential goal of disease ecology. we hypothesized that in bat white-nose syndrome (wns), species-specific host-pathogen interactions may partly explain varying disease outcomes among host species. we characterized bat and pathogen transcriptomes in paired samples of lesion-positive and lesion-negative wing tissue from bats infected with pseudogymnoascus destructans in three parallel expe ...202032552222
selection of viral variants during persistent infection of insectivorous bat cells with middle east respiratory syndrome coronavirus.coronaviruses that cause severe acute respiratory syndrome (sars) and middle east respiratory syndrome (mers) are speculated to have originated in bats. the mechanisms by which these viruses are maintained in individuals or populations of reservoir bats remain an enigma. mathematical models have predicted long-term persistent infection with low levels of periodic shedding as a likely route for virus maintenance and spillover from bats. in this study, we tested the hypothesis that bat cells and m ...202032350357
serological survey of lyssaviruses in polish bats in the frame of passive rabies surveillance using an enzyme-linked immunosorbent assay.background: bats are known to host a number of nonpathogenic viruses, as well as highly pathogenic viruses causing fatal diseases like rabies. serological surveys as part of active and passive bat rabies surveillance mainly use seroneutralization assays, demonstrating the presence of lyssavirus-specific antibodies in a variety of european bats, particularly against european bat lyssaviruses type 1 (eblv-1). here, we present the first serological survey in european bats of this kind during which ...202032121200
neural response selectivity to natural sounds in the bat midbrain.little is known about the neural mechanisms that mediate differential action-selection responses to communication and echolocation calls in bats. for example, in the big brown bat, frequency modulated (fm) food-claiming communication calls closely resemble fm echolocation calls, which guide social and orienting behaviors, respectively. using advanced signal processing methods, we identified fine differences in temporal structure of these natural sounds that appear key to auditory discrimination ...202031918008
safety, immunogenicity, and efficacy of intramuscular and oral delivery of era-g333 recombinant rabies virus vaccine to big brown bats (eptesicus fuscus).attenuated strains of rabies virus (rabv) have been used for oral vaccination of wild carnivores in europe and north america. however, some rabv vaccines caused clinical rabies in target animals. to improve the safety of attenuated rabv as an oral vaccine for field use, strategies using selection of escape mutants under monoclonal antibody neutralization pressure and reverse genetics-defined mutations have been used. we tested the safety, immunogenicity, and efficacy of one rabv construct, era-g ...202031895645
binaural response properties and sensitivity to interaural difference of neurons in the auditory cortex of the big brown bat, eptesicus fuscus.this study examines binaural response properties and sensitivity to interaural level difference of single neurons in the primary auditory cortex (ac) of the big brown bat, eptesicus fuscus under earphone stimulation conditions. contralateral sound stimulation always evoked response from all 306 ac neurons recorded but ipsilateral sound stimulation either excited, inhibited or did not affect their responses. high best frequency (bf) neurons typically had high minimum threshold (mt) and low bf neu ...202031785358
first record of carios kelleyi (acari: ixodida: argasidae) in new jersey, united states and implications for public health.the soft tick carios kelleyi (cooley and kohls), a parasite of bats known to occur in at least 29 of the 48 conterminous u.s. states, is here reported from new jersey for the first time, based on larvae collected from big brown bats, eptesicus fuscus. although thought to be widespread in north america, the ecology of c. kelleyi is not well understood, despite reports of this species feeding on humans and its consequent potential as a disease vector. the association of c. kelleyi with bat species ...202032901802
seroprevalence in bats and detection of borrelia burgdorferi in bat ectoparasites.the role of bats in the enzootic cycle of lyme disease and relapsing fever-causing bacteria is a matter of speculation. in canada, borrelia burgdorferi sensu stricto (ss) is the genospecies that is responsible for most cases of lyme disease in humans. in this study, we determined if big brown bats, eptesicus fuscus, have been exposed to spirochetes from the genus borrelia. we collected serum from 31 bats and tested them for the presence of anti-borrelia burgdorferi antibodies using a commercial ...202032244986
using deuterium oxide as a non-invasive, non-lethal tool for assessing body composition and water consumption in mammals.body condition scoring systems and body condition indices are common techniques used for assessing the health status or fitness of a species. body condition scoring systems are evaluator dependent and have the potential to be highly subjective. body condition indices can be confounded by foraging, the effects of body weight, as well as statistical and inferential problems. an alternative to body condition scoring systems and body condition indices is using a stable isotope such as deuterium oxid ...202032150166
big brown bats are challenged by acoustically-guided flights through a circular tunnel of hoops.mines and caves provide essential roosting places for bats, but often they are obstructed to prevent entry by humans. to allow bats to access their roosts, metal corrugated culvert pipes are sometimes installed. wildlife surveys indicate, however, that bats may abandon caves having corrugated culvert entrances. culverts may be confusing to bats due to the complex patterns of echoes returned by the regular, ring-like corrugations. we tested the hypothesis that a circular tunnel composed of succes ...202031964933
do bats use guano and urine stains to find new roosts? tests with three group-living bats.many animals use social cues to find refuges. bats can find roosts using the echolocation and social calls of conspecifics, but they might also use scent cues, a possibility which is less studied. the entrances of bat roosts are often marked by guano and urine, providing possible scent cues. we conducted eight experiments to test whether bats use the scent of guano and urine to find potential roosts. in field experiments, we tested if molossus molossus (velvety free-tailed bats) in panama and ep ...202033047058
biological characteristics and permissiveness to viruses of diploid kidney cells strain from the bat nathusius' pipistrelle (pipistrellus nathusii keyserling & blasius, 1839; chiroptera: microchiroptera: vespertilionidae).bats are an epidemiologically important natural reservoir of viruses of various taxonomic groups, including causative agents of especially dangerous infections of humans and animals. considering the relevance of arbovirus infections, it seems advisable to study the spectrum of the sensitivity of cells derived from bats inhabiting and migrating on the territory of the russian federation to causative agents of vector-borne diseases of animals.the study aimed to obtain a diploid strain of cells fro ...202133683063
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