Volatile antimicrobial compounds in the pelage of the Mexican free-tailed bat, Tadarida brasiliensis mexicana

Gas chromatography–mass spectrometry (GC–MS) showed that CH₂Cl₂ extracts of the pelage from the Mexican free-tailed bats, Tadarida brasiliensis mexicana, contained only seven volatile compounds. They include two hydrocarbons, 1-octene and octane; three aldehydes, heptanal, octanal and nonanal; a carboxylic acid, nonanoic acid; and urea. It is likely that nonanal, at an average concentration 0.62 μg/mg hair, and the two homologues, heptanal and octanal found at 0.059 and 0.066 μg/mg hair, respectively, function as antimicrobial agents against mammalian skin bacteria and fungi. These three aldehydes may also act as a chemical protection against bat ectoparasites.     

Echolocation by free-tailed bats (Tadarida)

Summary The echolocation of bats in the genusTadarida is highly adaptive to different acoustic conditions. These bats use different types of sonar signals with a diversity usually observed in comparisons across families of bats.Tadarida brasiliensis andT. macrotis search for airborne prey in open, uncluttered spaces using narrow-band, short CF signals with no FM components. They add broadband FM components while dropping the CF components when approaching or capturing prey. Only one harmonic is present in these insect-pursuit signals. When flying in cluttered situations or echolocating in a laboratory room,T. brasiliensis uses multiple-harmonic FM signals. Stationary bats tend to use linear frequency sweeps and moving bats tend to use curvilinear frequency sweeps or linear period sweeps. When emerging from a roost they initially use a short-CF/FM signal, changing to an FM signal as they fly away. The acuity of perception of target range inT. brasiliensis is about 1.0 to 1.5 cm and is determined by the bandwidth of the target-ranging sonar signals as represented by their autocorrelation functions. Many less adaptable species of bats use signals corresponding to part of the sonar repertoire ofTadarida. The functions of short CF or narrowband signals for detection and FM or broadband signals for resolution and acoustic imaging identified from comparisons among such species are confirmed by observations of echolocation byTadarida. The differences observed in echolocation among many species and families of bats appear to be evolutionary adaptations to some of the same features of the acoustic environment to whichTadarida responds behaviorally.Abbreviations CF frequency modulated - FM constant frequency - LPM linear period modulation - LFM linear-frequency modulation We thank Prof. T.T. Sandel, Prof. D.R. Griffin, Dr. George Pollak, and P.H. Dolkart for their advice and assistance. This research was supported by Grant No. BMS 72-02351-A01 from the National Science Foundation and by Biomedical Research Support Grant No. RR-07054 from the Division of Research Resources, National Institutes of Health.     

Individual variation in the isolation calls of Mexican free-tailed bat pups (Tadarida brasiliensis mexicana)

Near-term pregnant females and female-pup nursing pairs of Mexican free-tailed bats (Tadarida brasiliensis mexicana) were captured from large maternity colonies in central Texas. A total of 337 isolation calls from 20 pups were recorded and nine call parameters were measured from each call either sonagraphically or with a spectrum analyser. Univariate and multivariate analyses of the call parameters show that the calls of different pups are structurally distinct. Discriminant function analysis using a random subset of calls correctly categorized 60·4% to the pup emitting them. These results suggest that the pups have individual vocal signatures. Calls also possess qualities which suggest that they are attractive in nature and easy to locate. Regression analyses show that several call parameters increase in frequency as pups age.     

Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation

Stomach content analysis of 20 pregnant (x body mass=13.4 g) and 18 lactating (x body mass=11.5 g) female Tadarida brasiliensis revealed that the diet, expressed as percent volume, consists largely of lepidopterans, coleopterans, hymenopterans, and dipterans, in decreasing order of importance. We found no significant difference in the diet of pregnant and lactating females when expressed as percent volume. However, when expressed as percent frequency, proportionately more pregnant females fed on lepidopterans, coleopterans, and dipterans than did lactating bats, and proportionately more lactating females fed on hymenopterans. We found no significant differences in the percentages of water, lean dry mass, fat, and energy density in the stomach contents of pregnant and lactating females. Water in stomach contents averaged 62.7% and fat and lean dry mass averaged 22.2% and 15.2%, respectively (expressed as percentage of wet mass); energy density averaged 31.2 kJ g^–1 dry mass. This relatively high energy density of stomach contents, as compared to whole insects, can be attributed to the consumption of insects high in fat (especially flying ants) and the abdomens only of moths and beetles (other body parts being discarded). Estimates of nightly food intake increased markedly from mid- to late pregnancy, stabilized or decreased during late pregnancy, and increased again during early to mid-lactation. Average nightly feeding rate doubled from pregnancy to lactation and increased threefold during the first half of lactation. By adjusting our gravimetric estimates of nightly feeding rate upwards by 40% (based on estimates of field metabolic rate), we estimate that the average nightly energy intake of female T. brasiliensis ranges from 57 kJ day^–1 in early lactation to 104 kJ day^–1 in mid-lactation. These estimates represent nightly feeding rates averaging 39% and 73% of a female's body mass in the period from early to mid-lactation, respectively.     

Evidence for prenatal transfer of rabies virus in the Mexican free-tailed bat (Tadarida brasiliensis Mexicana)

Fetuses were collected from four Mexican free-tailed bats (Tadarida brasiliensis mexicana) and a fetal bat cell (FBC) line was established and tested for its ability to support the replication of the ERA vaccine strain of rabies virus. Cytopathic effects were detected in ERA virus-inoculated as well as uninoculated FBC's. Immunofluorescent antibody testing of uninoculated FBC's provided no evidence for the presence of rabies virus. However, mice inoculated intracranially with supernatant fluid from uninoculated FBC's died. Enzyme-linked immunosorbent assay and immunofluorescent antibody testing revealed rabies virus in the brains of these mice. Tests with a panel of monoclonal antibodies indicated that the isolate was the same as that isolated from Mexican free-tailed bats from the southwestern United States. We conclude that the fetuses from which the FBC line was derived had been infected in utero with rabies virus. We believe this may represent the first observation of prenatal transfer of rabies virus in naturally infected bats.     

Reproduction of Angola free-tailed bats (Tadarida condylura) and little free-tailed bats (Tadarida pumila) in Malawi (Central Africa) and elsewhere in Africa

Angola free-tailed bats and little free-tailed bats occur in diverse habitats throughout most of Africa south of the Sahara. This study investigated the reproductive strategies and related biology of these species in Malawi where they were sympatric, and analysed data from elsewhere in Africa to show how the strategies varied along a gradient of habitats from approximately 12 degrees N to 25 degrees S. Both the Angola free-tailed bat and the little free-tailed bat were normally monotocous. Angola free-tailed bats invariably had 2 births/year, and the interval between consecutive births decreased with increasing latitude. When the interval was shortest (approximately 90 days) a post-partum oestrus occurred. Little free-tailed bats differed by having a shorter gestation (approximately 60 days), and the ability to have up to 5 births/year with a postpartum oestrus after each birth. The extent to which this potential is achieved varies with latitude and rainfall, mainly so that lactation can coincide with peaks in the abundance of food. The interaction between rainfall and reproductive characteristics results in the two species having patterns of reproduction which are sometimes similar, but more often different. Competition between the species is unlikely to be affected by differences in their reproduction.     

Histological assessment of cellular immune response to the phytohemagglutinin skin test in Brazilian free-tailed bats (Tadarida brasiliensis)

Bats are known reservoirs for numerous emerging infectious diseases, occupy unique ecological niches, and occur globally except for Antarctica. Given their impact on human and agricultural health, it is critical to understand the mechanisms underlying immunocompetence in this reservoir host. To date, few studies have examined immune function in the Order Chiroptera, particularly among natural colonies of bats. The phytohemagglutinin (PHA) skin test has been widely used to measure delayed-type cellular immune response in a wide variety of vertebrates, and has been routinely employed in immunoecological studies. Although this test is frequently described as a measure of T cell proliferation, recent studies indicate it may represent a combination of immune responses. In mammals, the immune response is differentially, temporally and spatially regulated, therefore, we characterized the infiltrating leukocyte response to the PHA skin test in bats by examining a time-series of histological sections from PHA and saline injection areas in 41 Brazilian free-tailed bats (Tadarida brasiliensis). Results suggest that bats exhibit diverse leukocyte traffic within 6 h, and up to 24 h following subcutaneous PHA injection. There was a significant presence of lymphocytes and neutrophils, as well as eosinophils, basophils, and macrophages observed in the PHA-injected tissues, compared with saline-injected control tissues. We observed a highly significant negative correlation between the number of lymphocytes and neutrophils in PHA-injected tissue, with peak lymphocyte response at 12 h, and peak neutrophil response at 24 h post-injection. These results indicate substantial variation in the immune response of individuals, and may aid our understanding of disease emergence in natural populations of bats.     

Thermoregulation during flight: body temperature and sensible heat transfer in free-ranging Brazilian free-tailed bats (Tadarida brasiliensis)

Bat wings are important for thermoregulation, but their role in heat balance during flight is largely unknown. More than 80% of the energy consumed during flight generates heat as a by-product, and thus it is expected that bat wings should dissipate large amounts of heat to prevent hyperthermia. We measured rectal (T(r)) and surface (T(s)) temperatures of Brazilian free-tailed bats (Tadarida brasiliensis) as they emerged from and returned to their daytime roosts and calculated sensible heat transfer for different body regions (head, body, wings, and tail membrane). Bats' T(r) decreased from 36.8°C during emergence flights to 34.4°C during returns, and T(s) scaled positively with ambient temperature (T(a)). Total radiative heat loss from bats was significantly greater for a radiative sink to the night sky than for a sink with temperature equal to T(a). We found that free-ranging Brazilian free-tailed bats, on average, do not dissipate heat from their wings by convection but instead dissipate radiative heat (L) to the cloudless night sky during flight ([Formula: see text] W). However, within the range of T(a) measured in this study, T. brasiliensis experienced net heat loss between evening emergence and return flights. Regional hypothermia reduces heat loss from wings that are exposed to potentially high convective fluxes. Additional research is needed to establish the role of wings in evaporative cooling during flight in bats.     

Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: links to migratory insect populations

Existing information on the activity of bats in the aerosphereis restricted almost exclusively to altitudes that are withina few tens of meters above the ground. We report a total of50.2 h of ultrasonic recordings made using radio microphonicbat detectors suspended from free-floating helium balloons andfrom kites. The data include a total of 22 353 echolocativecalls from ground-level to 1118 m above ground level (AGL).These calls are attributed to Brazilian free-tailed bats basedon acoustic features and the large numbers and high-altitudeaerial dispersion of these bats over the local landscape. Batactivity varied significantly throughout the air column andwas greatest at 400–500 m AGL and near ground level. Feedingbuzzes, indicating feeding on aerial prey, were most abundantnear ground level and at 400–500 m, and were detectedto altitudes of 900 m AGL. The peak activity of bats at 400–500m AGL is concordant with the altitude of the atmospheric boundarylayer and the seasonal formation of the low-elevation southerlywind jet that has been identified as a major aeroecologicalcorridor for the nocturnal dispersal of noctuid moths and otherinsects.     

Seasonal variation in age,sex, and reproductive status of Mexican free-tailed bats

In North America, Mexican free-tailed bats (Tadarida brasiliensis mexicana) consume vast numbers of insects contributing to the economic well-being of society. Mexican free-tailed bats have declined due to historic guano mining, roost destruction, and bioaccumulation of organochlorine pesticides. Long-distance migrations and dense congregations at roosts exacerbate these declines. Wind energy development further threatens bat communities worldwide and presents emerging challenges to bat conservation. Effective mitigation of bat mortality at wind energy facilities requires baseline data on the biology of affected populations. We collected data on age, sex, and reproductive condition of Mexican free-tailed bats at a cave roost in eastern Nevada located 6 km from a 152-MW industrial wind energy facility. Over 5 years, we captured 46,353 Mexican free-tailed bats. Although just over half of the caught individuals were nonreproductive adult males (53.6%), 826 pregnant, 892 lactating, 10,101 post-lactating, and 4327 nonreproductive adult females were captured. Juveniles comprised 11.5% of captures. Female reproductive phenology was delayed relative to conspecific roosts at lower latitudes, likely due to cooler temperatures. Roost use by reproductive females and juvenile bats demonstrates this site is a maternity roost, with significant ecological and conservation value. To our knowledge, no other industrial scale wind energy facilities exist in such proximity to a heavily used bat roost in North America. Given the susceptibility of Mexican free-tailed bats to wind turbine mortality and the proximity of this roost to a wind energy facility, these data provide a foundation from which differential impacts on demographic groups can be assessed.     

Analyzing NEXRAD doppler radar images to assess nightly dispersal patterns and population trends in Brazilian free-tailed bats (Tadarida brasiliensis)

Operators of early weather-surveillance radars often observedechoes on their displays that did not behave like weather pattern,including expanding ring-like shapes they called angels. Theseechoes were caused by high-flying insects, migrating birds,and large colonies of bats emerging from roosts to feed. Modernweather-surveillance radar stations in the United States (NEXt-generationRADar or NEXRAD) provide detailed images that clearly show eveningbat emergences from large colonies. These images can be usedto investigate the flight behavior of groups of bats and populationtrends in large colonies of Brazilian free-tailed bats (Tadaridabrasiliensis) in south-central Texas which are clearly imagedby local NEXRAD radar stations. In this study, we used radarreflectivity data from the New Braunfels, Texas NEXRAD stationto examine relative colony size, direction of movement, speedof dispersion, and altitude gradients of bats from these coloniesfollowing evening emergence. Base reflectivity clear-air-modeLevel-II images were geo-referenced and compiled in a GIS alongwith locations of colonies and features on the landscape. Temporalsequences of images were filtered for the activity of bats,and from this, the relative size of bat colonies, and the speedand heading of bat emergences were calculated. Our results indicatecyclical changes in colony size from year to year and that initialheadings taken by bats during emergence flights are highly directional.We found that NEXRAD data can be an effective tool for monitoringthe nightly behavior and seasonal changes in these large colonies.Understanding the distribution of a large regional bat populationon a landscape scale has important implications for agriculturalpest management and conservation efforts.     

Prevalence of rabies specific antibodies in the Mexican free-tailed bat (Tadarida brasiliensis mexicana) at Lava Cave, New Mexico

Adult female and juvenile Mexican free-tailed bats (Tadarida brasiliensis mexicana) were collected bimonthly at Lava Cave, New Mexico from May through September. The purpose of this study was to examine the prevalence of active rabies infection as well as to determine individual immune status in these hosts. All bats were bled and examined for rabies antibody (total antibody versus IgM) utilizing a modified serum neutralization test. The brains were removed and examined by the fluorescent rabies antibody (FRA) test. No significant difference was observed in the number of adults with rabies neutralizing antibody (total) over the study period. Significant differences in rabies neutralizing antibody (total) were observed among the juveniles sampled during July and August. The number of adults with IgM specific antibody was low (15 of 750, 2%) and did not fluctuate significantly. However, the number of juveniles with IgM antibody did show increased levels in August and September. The number of adults positive by the FRA was low (4 of 750, less than 1%) and did not appear to fluctuate significantly over the study period. The number of juveniles positive by the FRA was three and one-half times higher than observed for the adults (14 of 600, 2%). These results indicate that the Mexican free-tailed bat appears to be exposed to rabies virus shortly after birth as evident by its immune status. The low prevalence (4 of 750, less than 1%) of active infection as determined by the FRA and mouse inoculation and the high prevalence (514 of 750, 69%) of IgG antibody in the adult females indicate that the Mexican free-tailed bat recovers from rabies virus infection.     

Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis

We examined patterns of variation in the mineral content of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. We ashed humeri, radii, metacarpals II-V, and phalanges of digit III, and quantified mineralization differences among elements at specific ages, and ontogenetically for each element. The most mineralized elements are the humerus and the radius, followed by the metacarpals, of which the third and fifth are the most mineralized. The proximal and middle phalanges of the third digit exhibit the lowest mineral content, and the distal phalanges have no mineral content according to our ashing protocol. Histological examination shows a thin (< 10 μm) shell of unmineralized osteoid surrounding a cartilaginous core in distal phalanges. Mineral content of each bone increases linearly with age during post-natal development, but there are differences in the rate and extent of this increase among the different elements.
The mineralizaton differences we observed parallel substantially different bone loading patterns found in different parts of the wing in other studies. The humerus and radius are subjected to large torsional loads during flight, while the metacarpals and phalanges experience dorsoventral bending. The high mineral content of the humerus and radius and the low mineral content of the metacarpals and phalanges may resist torsion proximally and promote bending distally. Furthermore, the decrease in mineral content along the wing's proximodistal axis decreases bone mass disproportionately at the wing tips, where the energetic cost of accelerating and decelerating limb mass is greatest.     

Molecular diet analysis of two african free-tailed bats (molossidae) using high throughput sequencing

Given the diversity of prey consumed by insectivorous bats, it is difficult to discern the composition of their diet using morphological or conventional PCR-based analyses of their faeces. We demonstrate the use of a powerful alternate tool, the use of the Roche FLX sequencing platform to deep-sequence uniquely 5' tagged insect-generic barcode cytochrome c oxidase I (COI) fragments, that were PCR amplified from faecal pellets of two free-tailed bat species Chaerephon pumilus and Mops condylurus (family: Molossidae). Although the analyses were challenged by the paucity of southern African insect COI sequences in the GenBank and BOLD databases, similarity to existing collections allowed the preliminary identification of 25 prey families from six orders of insects within the diet of C. pumilus, and 24 families from seven orders within the diet of M. condylurus. Insects identified to families within the orders Lepidoptera and Diptera were widely present among the faecal samples analysed. The two families that were observed most frequently were Noctuidae and Nymphalidae (Lepidoptera). Species-level analysis of the data was accomplished using novel bioinformatics techniques for the identification of molecular operational taxonomic units (MOTU). Based on these analyses, our data provide little evidence of resource partitioning between sympatric M. condylurus and C. pumilus in the Simunye region of Swaziland at the time of year when the samples were collected, although as more complete databases against which to compare the sequences are generated this may have to be re-evaluated.