Search

info:eu-repo/semantics/publishedVersion

In multifunctional landscapes, diverse communities of flying vertebrate predators provide vital services of insect pest control. In such landscapes, conservation biocontrol should benefit service-providing species to enhance the flow, stability and resilience of pest control services supporting the production of food and fiber. However, this would require identifying key service providers, which may be challenging when multiple predators interact with multiple pests. Here we provide a framework to identify the functional role of individual species to pest control in multifunctional landscapes. First, we used DNA metabarcoding to provide detailed data on pest species predation by diverse predator communities. Then, these data were fed into an extensive network analysis, in which information relevant for conservation biocontrol is gained from parameters describing network structure (e.g., modularity) and species roles in such network (e.g., centrality, specialization). We applied our framework to a Mediterranean landscape, where 19 bat species were found to feed on 132 insect pest species. Metabarcoding data revealed potentially important bats that consumed insect pest species in high frequency and/or diversity. Network analysis showed a modular structure, indicating sets of bat species that are required to regulate specific sets of insect pests. A few generalist bats had particularly important roles, either at network or module levels. Extinction simulations highlighted six bats, including species of conservation concern, which were sufficient to ensure that over three-quarters of the pest species had at least one bat predator. Combining DNA metabarcoding and ecological network analysis provides a valuable framework to identify individual species within diverse predator communities that might have a disproportionate contribution to pest control services in multifunctional landscapes. These species can be regarded as candidate targets for conservation biocontrol, although additional information is needed to evaluate their actual effectiveness in pest regulation.

Temperate bat species use extended torpor to conserve energy when ambient temperatures are low and food resources are scarce. Previous research suggests that migratory bat species and species known to roost in thermally unstable locations, such as those that roost in trees, are more likely to remain active during winter. However, hibernating colonies of cave roosting bats in the southeastern United States may also be active and emerge from caves throughout the hibernation period. We report what bats are eating during these bouts of winter activity. We captured 2,044 bats of 10 species that emerged from six hibernacula over the course of 5 winters (October–April 2012/2013, 2013/2014, 2015/2016, 2016/2017, and 2017/2018). Using Next Generation sequencing of DNA from 284 fecal samples, we determined bats consumed at least 14 Orders of insect prey while active. Dietary composition did not vary among bat species; however, we did record variation in the dominant prey items represented in species’ diets. We recorded Lepidoptera in the diet of 72.2% of individual Corynorhinus rafinesquii and 67.4% of individual Lasiurus borealis. Diptera were recorded in 32.4% of Myotis leibii, 37.4% of M. lucifugus, 35.5% of M. sodalis and 68.8% of Perimyotis subflavus. Our study is the first to use molecular genetic techniques to identify the winter diet of North American hibernating bats. The information from this study is integral to managing the landscape around bat hibernacula for insect prey, particularly in areas where hibernating bat populations are threatened by white-nose syndrome.

The diverse functional roles of over 6,000 species of extant mammals that range in body size across eight orders of magnitude, from blue whales (Balaenoptera musculus) to tiny Etruscan shrews (Suncus etruscus), contribute to shaping Earth's ecosystems. Large mammalian herbivores (e.g., African elephants [Loxodonta africana], American bison [Bison bison], hippopotamuses [Hippopotamus amphibius]) and carnivores (e.g., wolves [Canis lupus], pumas [Puma concolor], sea otters [Enhydra lutris]) often have significant effects on primary producers in terrestrial, aquatic, and marine systems through nutrient cycling, energy flow, and the exertion of bottom-up and top-down processes. Small mammals, like bats, are important pollinators, dispersers of fruits, and consumers of arthropods, and others, especially rodents and primates, are important predators and dispersers of seeds. Many of these mammal-mediated processes occur simultaneously in the same ecosystem, and have significant effects on community structure of primary producers that in turn alter communities of other vertebrates and invertebrates. Many mammals also are ecosystem engineers (e.g., elephants, American beavers [Castor canadensis], porcupines [Erithezon dorsatum], prairie dogs [Cynomys spp.]) that create, significantly modify, or destroy habitat, and by doing so, they alter ecosystem structure and function and increase habitat heterogeneity and biodiversity. The extensive influence mammals have on ecosystems results in important services that contribute to human well-being, such as pollination, insect pest control, and bioturbation of soils. The rapid declines in abundance of many mammal populations and the associated increase in extinction risk raise conservation concerns for mammals. To maintain mammalian diversity and the critical ecosystem processes they provide, scientists need to mobilize concern for their status and strive for more effective and comprehensive conservation action. We provide insights and synthesis on the ecological role of mammals and highlight key research questions and future directions for their conservation.

Bats are assumed not to use vision for communication, despite recent evidence of their capacity for color vision. The possibility that bats use color traits as signals has thus been overlooked. Some tent-roosting bats have a potential for visual signaling because they exhibit bright yellow skin, a trait that in birds often acts as a sexual signal. We searched for evidence of sexual dichromatism in the yellow bare skin of Honduran white bats Ectophylla alba, the first reported mammal with a capacity to deposit significant amounts of carotenoid pigments in the skin. We found that skin yellow chroma, a measure that reflects carotenoid content, increases in the ears and nose-leaf during development probably due to an increase in dietary carotenoid accumulation. Once in the adulthood, the yellow color of the nose-leaf becomes brighter in males, representing the first evidence of sexual dichromatism in a bat. The nose-leaf brightness tends to covary positively with the body condition of males. We also found that the skin shows a reflectance peak at 530 nm that virtually coincides with the main reflectance peak (540 nm) of the back side of Heliconia leaves used as roosts. This suggests that these leaves were selected because of camouflage benefits, and the rich lighting conditions of these roosting places then favored the use of skin coloration as a sexual signal. These findings open a new perspective in the physiological and behavioral ecology of bats in which vision has a more relevant role than previously thought.

At the second North American Symposium on Bat Research the first reported use of radar to study flight behavior in bats confirmed that Mexican free-tailed bats (Tadarida brasiliensis mexicana) fly at altitudes over 3000 m above the ground. The reasons for these high-altitude flights were unclear, and it was assumed that the bats flew this high to commute to favorable foraging sites. Large numbers of insects now are known to utilize favorable winds at altitudes of hundreds to thousands of meters aloft to assist their long-distance movements. Dietary analyses and deployment of bat detectors to altitudes up to 1100 m confirm that Mexican free-tailed bats alter their behavior to feed heavily on these insects, many of which are major agricultural pests. Next generation radars confirm the movements and high-altitude intersection of bats and insects. Doppler weather radars continuously monitor and archive information on the emergence and dispersal of bats, providing long-term data on the bats’ ecology, behavior, and estimates of population sizes. Bat species regularly fly to high altitudes on all continents where they occur, and many of these bats are confirmed or suspected of feeding on migratory insects. The high-altitude habitat remains poorly known, as are the physiological adaptations, behaviors, and sensory cues that bats use to meet the challenges and opportunities of flying at high altitudes. Advancing technologies should continue to aid future research to investigate the high-altitude frontier and make discoveries about the ecology and behavior of bats aloft.

During the day, flying animals exploit the environmental energy landscape by seeking out thermal or orographic uplift, or extracting energy from wind gradients.1-6 However, most of these energy sources are not thought to be available at night because of the lower thermal potential in the nocturnal atmosphere, as well as the difficulty of locating features that generate uplift. Despite this, several bat species have been observed hundreds to thousands of meters above the ground.7-9 Individuals make repeated, energetically costly high-altitude ascents,10-13 and others fly at some of the fastest speeds observed for powered vertebrate flight.14 We hypothesized that bats use orographic uplift to reach high altitudes,9,15-17 and that both this uplift and bat high-altitude ascents would be highly predictable.18 By superimposing detailed three-dimensional GPS tracking of European free-tailed bats (Tadarida teniotis) on high-resolution regional wind data, we show that bats do indeed use the energy of orographic uplift to climb to over 1,600 m, and also that they reach maximum sustained self-powered airspeeds of 135 km h-1. We show that wind and topography can predict areas of the landscape able to support high-altitude ascents, and that bats use these locations to reach high altitudes while reducing airspeeds. Bats then integrate wind conditions to guide high-altitude ascents, deftly exploiting vertical wind energy in the nocturnal landscape. published

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-g333, developed with reverse genetics by intramuscular (IM) or oral (PO) routes in big brown bats (

Insect migrations represent large movements of resources across a landscape, which are attractive to predators capable of detecting and catching them. Brazilian free-tailed bats (Tadarida brasiliensis (I. Geoffroy, 1824)) consume migratory noctuid moths, which concentrate in favourable winds resulting in aggregations of prey that attract bats hundreds of metres above ground. Although T. brasiliensis are known to feed on these aggregations of migratory moths, changes in their foraging behaviours have not been linked to moth migration events. We investigated possible shifts in the bats’ foraging behaviours when moths are migrating with respect to altitude and moth abundance. We recorded 1104 echolocation call passes of T. brasiliensis at ground level and at altitudes of ∼100 and ∼200 m above ground level. We found proportionally more bat activity at higher altitudes when migratory moth abundance was high. We also found that bats decreased call frequency and bandwidth and increased call duration at higher altitudes and behaved similarly with increasing moth abundance even at ground level. Our results support predictions that bats change foraging behaviour in response to seasonal availability of migratory moths and document alterations in echolocation call parameters that are consistent with optimizing prey detection.

Brazilian free-tailed bats (Tadarida brasiliensis) are one of the most widely distributed bat species in the Americas, often engaging in rapid, long-distance dispersals. Here, we document that, since ca. 2007, these bats have expanded their range into western North Carolina, eastern Tennessee, and Virginia. Reports from wildlife control professionals, wildlife rehabilitators, regional submissions of bats for rabies testing, acoustic monitoring, and the presence of T. brasiliensis in buildings and bat houses indicate that these bats are now established in year-round colonies in areas previously thought outside their range limits. The geographic distributions of many organisms are currently shifting to higher latitudes in response to changing climate. We hypothesize that a coldtolerant thermal physiology that allows these largely tropical bats to enter extended torpor contributes to the ability of T. brasiliensis to establish populations in formerly cooler regions, and propose that their rapid northward expansion is facilitated by climate change and their tendency to explore new habitats and use a wide diversity of roost sites. Because of their abundance and use of man-made structures, we anticipate that the range expansion of T. brasiliensis will have implications for public health, ecosystem services, and bat conservation.

In 2014, the Fish and Wildlife Service (FWS) and National Marine Fisheries Service announced a new policy interpretation for the U.S. Endangered Species Act (ESA). According to the act, a species must be listed as threatened or endangered if it is determined to be threatened or endangered in a significant portion of its range (SPR). The 2014 policy seeks to provide consistency by establishing that a portion of the range should be considered significant if the associated individuals' "removal would cause the entire species to become endangered or threatened." We reviewed 20 quantitative techniques used to assess whether a portion of a species' range is significant according to the new guidance. Our assessments are based on the 3R criteria-redundancy (i.e., buffering from catastrophe), resiliency (i.e., ability to withstand stochasticity), and representation (i.e., ability to evolve)-that the FWS uses to determine if a species merits listing. We identified data needs for each quantitative technique and considered which methods could be implemented given the data limitations typical of rare species. We also identified proxies for the 3Rs that may be used with limited data. To assess potential data availability, we evaluated 7 example species by accessing data in their species status assessments, which document all the information used during a listing decision. In all species, an SPR could be evaluated with at least one metric for each of the 3Rs robustly or with substantial assumptions. Resiliency assessments appeared most constrained by limited data, and many species lacked information on connectivity between subpopulations, genetic variation, and spatial variability in vital rates. These data gaps will likely make SPR assessments for species with complex life histories or that cross national boundaries difficult. Although we reviewed techniques for the ESA, other countries require identification of significant areas and could benefit from this research.

Background Emerging infectious diseases in wildlife are an increasing threat to global biodiversity. White-nose syndrome (WNS) in bats is one of the most recently emerged infectious diseases in North America, causing massive declines in eastern bat populations. In the Northeast, winter behavior of bats during the hibernation period, such as flying during the day or in cold weather, has been attributed to WNS. However, winter emergence of bats in the southeastern United States, where winters are warmer, has received little attention. The goals of this study were to determine if winter emergence results from infection by Pseudogymnoascus destructans, the causative pathogen of WNS, and to investigate how pathogen load and prevalence vary by species, site, and over time. Results We collected epidermal swab samples from 871 active bats of 10 species captured outside of hibernacula in Tennessee during winters 2012–2013 and 2013–2014. Deoxyribonucleic acid (DNA) from P. destructans was not detected on 54% of these bats, suggesting that winter emergence occurs regardless of fungal infection. Among infected bats, Perimyotis subflavus (tri-colored bats) had the highest mean fungal load, whereas Myotis lucifugus (little brown bats) had the highest infection prevalence of all individuals captured. Less than 18% (n = 59 of 345 individuals sampled) of all M. grisescens (gray bats) captured had detectible P. destructans DNA on their forearms and muzzle. Hibernacula with large M. grisescens populations had lower fungal loads than sites used by other species; however, mean load per species did not significantly differ between M. grisescens and non-M. grisescens sites. Conclusions We found that pathogen load and prevalence were higher on bats captured during winter 2012–2013 than in the following winter, indicating that fungal loads on bats did not increase the longer a site was presumably contaminated. Repeated low-dose exposure, mild temperatures, and availability of prey during winter in the Southeast may provide a regional refuge for surviving bat populations.

The common vampire bat, Desmodus rotundus, ranges from South America into northern Mexico in North America. This sanguivorous species of bat feeds primarily on medium to large‐sized mammals and is known to rely on livestock as primary prey. Each year, there are hotspot areas of D. rotundus‐specific rabies virus outbreaks that lead to the deaths of livestock and economic losses. Based on incidental captures in our study area, which is an area of high cattle mortality from D. rotundus transmitted rabies, it appears that D. rotundus are being caught regularly in areas and elevations where they previously were thought to be uncommon. Our goal was to investigate demographic processes and genetic diversity at the north eastern edge of the range of D. rotundus in Mexico. We generated control region sequences (441 bp) and 12‐locus microsatellite genotypes for 602 individuals of D. rotundus. These data were analyzed using network analyses, Bayesian clustering approaches, and standard population genetic statistical analyses. Our results demonstrate panmixia across our sampling area with low genetic diversity, low population differentiation, loss of intermediate frequency alleles at microsatellite loci, and very low mtDNA haplotype diversity with all haplotypes being very closely related. Our study also revealed strong signals of population expansion. These results follow predictions from the leading‐edge model of expanding populations and supports conclusions from another study that climate change may allow this species to find suitable habitat within the U.S. border.

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

Native predators provide undervalued pest suppression services to agriculture. Studies of pest consumption by insectivorous bats tend to focus upon single species in large, centralized colonies, while bats dispersed in small groups within the agricultural matrix often go unnoticed. Pecan trees, Carya illinoinensis, and the destructive pecan nut casebearer (PNC) moth, Acrobasis nuxvorella, comprise a tightly linked host&ndash, parasite system in a widespread agroecosystem native to North America. Here we use a quantitative polymerase chain reaction (qPCR) assay of fecal DNA to document predation on PNC moths by an assemblage of sympatric bat species across episodic peaks in PNC abundance. Although five species of bats consume PNC moths, greater predation by a solitary tree-roosting bat (eastern red bat, Lasiurus borealis) than other species is suggested by a higher frequency of PNC occurrence and quantity of PNC gene copies in fecal samples. Consumption of PNC by bats during all documented peaks in moth activity suggests that predation pressure occurs throughout the PNC season. Our results highlight the need to consider multi-species assemblages and different foraging strategies when assessing pest suppression services, particularly in agroforestry or tree crops. Assessing the diet of only common or easily captured species limits our ability to accurately document pest consumption by bats.

The spread of white nose syndrome raises serious concerns about the long-term viability of affected bat species. Here we examine the geographic distribution of genetic variation, levels of population connectivity that may influence the spatial spread of WNS, and the likelihood that recent population declines in regions affected by WNS have led to the loss of unique genetic variation for the endangered Indiana bat (Myotis sodalis). We amplified a fragment of the mitochondrial control region for 375 individuals and genotyped 445 individuals at 10 microsatellite loci from 18 sampling sites distributed across the majority of the species' range. Analysis of mitochondrial DNA indicated the presence of at least five distinct matrilineal clusters, with the most pronounced differences between northeastern sites and those in the rest of the range. The majority of individuals in the Ozark- Central, Midwest, and Appalachian recovery units fell into a single cluster. Significant differentiation also was observed between one Appalachian and one Midwestern site and the majority of other sites. However, using nuclear microsatellites we observed the absence of differentiation and widespread gene flow among all hibernacula, suggesting the occurrence of extensive gene flow through dispersal and mating. The absence of genetically distinct populations within the range of Indiana bats indicates a lack of barriers to WNS transmission, and it is unlikely that significant portions of the hibernating population of Indiana bats will remain disease free into the future. Further, while matrilineal gene flow was restricted among some sites and regions, we found no genetic evidence to support the division of Indiana bats into separate recovery units.

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 a...

DNA metabarcoding is increasingly used in dietary studies to estimate diversity, composition and frequency of occurrence of prey items. However, few studies have assessed how technical and biological replication affect the accuracy of diet estimates. This study addresses these issues using the European free‐tailed bat Tadarida teniotis, involving high‐throughput sequencing of a small fragment of the COI gene in 15 separate faecal pellets and a 15‐pellet pool per each of 20 bats. We investigated how diet descriptors were affected by variability among (a) individuals, (b) pellets of each individual and (c) PCRs of each pellet. In addition, we investigated the impact of (d) analysing separate pellets vs. pellet pools. We found that diet diversity estimates increased steadily with the number of pellets analysed per individual, with seven pellets required to detect ~80% of prey species. Most variation in diet composition was associated with differences among individual bats, followed by pellets per individual and PCRs per pellet. The accuracy of frequency of occurrence estimates increased with the number of pellets analysed per bat, with the highest error rates recorded for prey consumed infrequently by many individuals. Pools provided poor estimates of diet diversity and frequency of occurrence, which were comparable to analysing a single pellet per individual, and consistently missed the less common prey items. Overall, our results stress that maximizing biological replication is critical in dietary metabarcoding studies and emphasize that analysing several samples per individual rather than pooled samples produce more accurate results.

The conversion of natural lands to agriculture is a leading cause of the worldwide loss of biodiversity. In particular, cropland monocultures alter insect abundance and diversity compared to adjacent natural habitats. While agricultural lands can provide large numbers of insect pests as prey items to predators such as bats, insect pest population size vary greatly throughout growing seasons. This study assesses the importance of land use and corn earworm moth availability as spatial and temporal drivers of bat activity. We quantified spatial variation in land use patterns at fifteen sites located within the Winter Garden region in south central Texas and used bat detectors and insect pheromone traps to monitor nightly bat activity and corn earworm moth abundance across the landscape and throughout most of the year. Our temporal analyses show that bat activity was positively correlated with moth abundance, but only early in the growing season when moth abundance is at its peak. The key result from this study is a positive relationship between bat activity and natural habitat cover during late summer months, corresponding to periods of low moth abundance and a peak in bat activity. During the late summer period, bats were more active at sites containing a larger percentage of natural habitats than those containing a larger percentage of agricultural land. Our results strongly suggest that intensive agricultural practices create systems providing bats with inconsistent resource supply, but the persistence of natural habitats provides consistency in food supply though time. Taken together, these findings illustrate the importance of protecting and restoring natural habitats for the conservation for bats and the pest-suppression services they provide in agricultural ecosystems.

Pseudogymnoascus destructans, the causal agent of white-nose syndrome (WNS), is responsible for widespread mortality of hibernating bats across eastern North America. To document P. destructans exposure and infections on bats active during winter in the southeastern US, we collected epidermal swabs from bats captured during winters 2012–13 and 2013–14 in mist nets set outside of hibernacula in Tennessee. Epidermal swab samples were collected from eight Rafinesque's big-eared bats (Corynorhinus rafinesquii), six eastern red bats (Lasiurus borealis), and three silver-hair bats (Lasionycteris noctivagans). Using real-time PCR methods, we identified DNA sequences of P. destructans from skin swabs of two Rafinesque's big-eared bats, two eastern red bats, and one silver-haired bat. This is the first detection of the WNS fungus on Rafinesque's big-eared bats and eastern red bats and the second record of the presence of the fungus on silver-haired bats.

Bats are generalist predators of night flying insects, including many crop pests. Attracting bats to agricultural areas using bat houses may reduce the numbers of these pests and, consequently, their economic impact. We use real time polymerase chain reaction of mitochondrial DNA found in the guano of bats living in bat houses on organic pecan orchards to document the consumption of pest moth species: pecan nut casebearer, Acrobasis nuxvorella Neunzig (Lepidoptera: Pyralidae), hickory shuckworm, Cydia caryana Fitch (Lepidoptera: Torticidae), and corn earworm, Helicoverpa zea Boddie (Lepidoptera: Noctuidae). We also use direct sequencing of insect remains in bat fecal pellets to identify stink bugs consumed by bats in bat houses. Evidence that bats prey upon crop pests is the first step in showing that bats are beneficial to pecan farmers and provides incentives for bat conservation.

We estimated U.S. and Mexican citizens' willingness to pay (WTP) for protecting habitat for a transborder migratory species, the Mexican free-tailed bat (Tadarida brasiliensis mexicana), using the contingent valuation method. Few contingent valuation surveys have evaluated whether households in one country would pay to protect habitat in another country. This study addresses that gap. In our study, Mexican respondents were asked about their WTP for conservation of Mexican free-tailed bat habitat in Mexico and in the United States. Similarly, U.S. respondents were asked about their WTP for conservation in the United States and in Mexico. U.S. households would pay $30 annually to protect habitat in the United States and $24 annually to protect habitat in Mexico. Mexican households would pay $8 annually to protect habitat in Mexico and $5 annually to protect habitat in the United States. In both countries, these WTP amounts rose significantly for increasing the size of the bat population rather than simply stabilizing the current bat population. The ratio of Mexican household WTP relative to U.S. household WTP is nearly identical to that of Mexican household income relative to U.S. household income. This suggests that the perceived economic benefits received from the bats is similar in Mexico and the United States, and that scaling WTP by relative income in international benefit transfer may be plausible.

Different second-generation sequencing technologies may have taxon-specific biases when DNA metabarcoding prey in predator faeces. Our major objective was to examine differences in prey recovery from bat guano across two different sequencing workflows using the same faecal DNA extracts. We compared results between the Ion Torrent PGM and the Illumina MiSeq with similar library preparations and the same analysis pipeline. We focus on repeatability and provide an R Notebook in an effort towards transparency for future methodological improvements. Full documentation of each step enhances the accessibility of our analysis pipeline. We tagged DNA from insectivorous bat faecal samples, targeted the arthropod cytochrome c oxidase I minibarcode region and sequenced the product on both second-generation sequencing platforms. We developed an analysis pipeline with a high operational taxonomic unit (OTU) clustering threshold (i.e., ≥98.5%) followed by copy number filtering to avoid merging rare but genetically similar prey into the same OTUs. With this workflow, we detected 297 unique prey taxa, of which 74% were identified at the species level. Of these, 104 (35%) prey OTUs were detected by both platforms, 176 (59%) OTUs were detected by the Illumina MiSeq system only, and 17 (6%) OTUs were detected using the Ion Torrent system only. Costs were similar between platforms but the Illumina MiSeq recovered six times more reads and four additional insect orders than did Ion Torrent. The considerations we outline are particularly important for long-term ecological monitoring; a more standardized approach will facilitate comparisons between studies and allow faster recognition of changes within ecological communities.

High-altitude nocturnal insect migrations are ubiquitous and represent significant pulses of biomass, which impact large areas and multiple trophic levels, yet are difficult to study and poorly understood. Predation on migratory insects by high-flying bats provides potential for investigating flows of migratory insects across a landscape. Brazilian free-tailed bats, Tadarida brasiliensis, provide valuable ecosystem services by consuming migratory pests, and research suggests migratory insects are an important resource to bats in autumn. We sequenced insect DNA from bat feces collected during the 2010–2012 autumn migrations of insects over southern Texas, and tested the utility of predator–prey interactions for monitoring migratory insect populations by asking: 1) how extensively do bats consume migratory insects during autumn? (2) does the prey community reflect known drivers of insect migrations, e.g. cold fronts? and (3) are migratory insects increasingly important to bats when local food resources decline in autumn? Bats consumed at least 21 species of migratory insects and 44 species of agricultural pests. Prey community richness increased with cold front passage. Bats consumed migratory moths over the entire autumn season, and the proportion of migratory moths in the bat diet increased over the course of the autumn season in all 3 years. This study confirms extensive consumption of migratory insects by bats, links patterns in prey communities to mechanisms driving insect migration, and documents a novel approach to tracking patterns of migratory insect movement. As an important resource for T. brasiliensis in autumn, migratory insects provide stabilizing effects to the local animal community.

Drivers of environmental change in one location can have profound effects on ecosystem services and human well-being in distant locations, often across international borders. The telecoupling provides a conceptual framework for describing these interactions - for example, locations can be defined as sending areas (sources of flows of ecosystem services, energy, or information) or receiving areas (recipients of flows). However, the ability to quantify feedbacks between ecosystem change in one area and societal benefits in other areas requires analytical approaches. We use spatial subsidies - an approach developed to measure the degree to which a migratory species' ability to provide services in one location depends on habitat in another location - as an example of how telecoupling can be operationalized. Using the cotton pest control and ecotourism services of Mexican free-tailed bats as an example, we determined that of the 16 states in the United States and Mexico where the species resides, three states (Texas, New Mexico, and Colorado) are receiving areas, while the rest of the states are sending areas. In addition, the magnitude of spatial subsidy can be used as an indicator of the degree to which different locations are telecoupled to other locations. In this example, the Mexican free-tailed bat ecosystem services to cotton production and ecotourism in Texas and New Mexico are heavily dependent on winter habitat in four states in central and southern Mexico. In sum, spatial subsidies can be used to operationalize the telecoupling conceptual framework by identifying sending and receiving areas, and by indicating the degree to which locations are telecoupled to other locations.

Conservation planning can be challenging due to the need to balance biological concerns about population viability with social concerns about the benefits biodiversity provide to society, often while operating under a limited budget. Methods and tools that help prioritize conservation actions are critical for the management of at-risk species. Here, we use a multi-attribute utility function to assess the optimal maternity roosts to conserve for maintaining the population viability and the ecosystem services of a single species, the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Mexican free-tailed bats provide ecosystem services such as insect pest-suppression in agricultural areas and recreational viewing opportunities, and may be threatened by climate change and development of wind energy. We evaluated each roost based on five attributes: the maternity roost’s contribution to population viability, the pest suppression ecosystem services to the surrounding area provided by the bats residing in the roost, the ecotourism value of the roost, the risks posed to each roost structure, and the risks posed to the population of bats residing in each roost. We compared several scenarios that prioritized these attributes differently, hypothesizing that the set of roosts with the highest rankings would vary according to the conservation scenario. Our results indicate that placing higher values on different roost attributes (e.g. population importance over ecosystem service value) altered the roost rankings. We determined that the values placed on various conservation objectives are an important determinant of habitat planning.

The performance capabilities of flying animals reflect the interplay of biomechanical and physiological constraints and evolutionary innovation. Of the two extant groups of vertebrates that are capable of powered flight, birds are thought to fly more efficiently and faster than bats. However, fast-flying bat species that are adapted for flight in open airspace are similar in wing shape and appear to be similar in flight dynamics to fast-flying birds that exploit the same aerial niche. Here, we investigate flight behaviour in seven free-flying Brazilian free-tailed bats (Tadarida brasiliensis) and report that the maximum ground speeds achieved exceed speeds previously documented for any bat. Regional wind modelling indicates that bats adjusted flight speeds in response to winds by flying more slowly as wind support increased and flying faster when confronted with crosswinds, as demonstrated for insects, birds and other bats. Increased frequency of pauses in wing beats at faster speeds suggests that flap-gliding assists the bats' rapid flight. Our results suggest that flight performance in bats has been underappreciated and that functional differences in the flight abilities of birds and bats require re-evaluation.

Widespread animals at the extremes of the species' distribution experience ecological constraints different than individuals in the core of the distribution. For example, small endotherms at very high latitudes face short summers with cool temperatures and a lack of true darkness. In particular, insectivorous bats at high latitudes may experience constraints because of their unique life history traits, and may have different energy requirements than bats at lower latitudes. To evaluate the extent of these differences, we estimated an energy budget and refueling rates for reproductively active female little brown bats ( Myotis lucifugus ) roosting in buildings in eastern Alaska (~ 63°N). Physiological parameters (torpor use and metabolic rates) and daily energy expenditures (25.7 ± 5.3 kJ d − 1 ) were similar to, or slightly lower than, conspecifics at lower latitudes. Northern little brown bats foraged for less time than southerly conspecifics, but measurements of plasma β-hydroxybutyrate concentrations suggest that northern bats refuel at a rate considerably higher than those to the south. It appears that high refueling rates (and therefore foraging intensity) involve a dietary shift to orb-weaver spiders, which are abundant and likely offer higher energetic benefit than the small, flying insects consumed by individuals in other parts of the distribution. Environmental factors may limit species' distributions, but our results provide an example of a population at the limit of their geographic range that has compensated for environmental challenges by adopting unique behavioral strategies while the underlying physiology (including daily energy expenditure) remains similar to populations at the core of the species' range.

Given rapid changes in agricultural practice, it is critical to understand how alterations in ecological, technological, and economic conditions over time and space impact ecosystem services in agroecosystems. Here, we present a benefit transfer approach to quantify cotton pest-control services provided by a generalist predator, the Mexican free-tailed bat (Tadarida brasiliensis mexicana), in the southwestern United States. We show that pest-control estimates derived using (1) a compound spatial–temporal model – which incorporates spatial and temporal variability in crop pest-control service values – are likely to exhibit less error than those derived using (2) a simple-spatial model (i.e., a model that extrapolates values derived for one area directly, without adjustment, to other areas) or (3) a simple-temporal model (i.e., a model that extrapolates data from a few points in time over longer time periods). Using our compound spatial–temporal approach, the annualized pest-control value was $12.2 million, in contrast to an estimate of $70.1 million (5.7 times greater), obtained from the simple-spatial approach. Using estimates from one year (simple-temporal approach) revealed large value differences (0.4 times smaller to 2 times greater). Finally, we present a detailed protocol for valuing pest-control services, which can be used to develop robust pest-control transfer functions for generalist predators in agroecosystems.EDITED BY Neville Crossman EDITED BY Neville Crossman

This study examines effects of simulated echolocation calls of bats in a field setting on the flight activity and pheromone-tracking behavior of the male corn earworm moth, Helicoverpa zea (Lepidoptera: Noctuidae), an insect that responds evasively to echolocation calls of bats. Simulated echolocation was broadcast over crop fields in an area where moths were abundant during summer. Field collections of free-flying moths and pheromone trapping of male moths were conducted in the presence and absence of simulated calls. Numbers of moths captured were not affected in either experiment by presence of simulated echolocation calls. Contrary to previous evidence, these data suggest that moths are not dissuaded from tracking pheromones under a perceived high risk of predation. Exhibiting a continual anti-predator response under a sustained risk of predation could have negative impacts on reproductive success, leading males to take higher risks compared to situations in which predators are sporadically p...

The Mariana flying fox (Pteropus mariannus) has suffered substantial decline in recent years. Taxonomic classification of P. mariannus has been inconsistent, with subspecies designations based mainly on geography and morphological variation within small sample sizes. In this study, we examine relationships of P. mariannus across two island groups in the western Pacific Ocean. Microsatellite data and mitochondrial sequences, from D-loop, cytochrome oxidase I, and cytochrome b, suggest that the population on the islands of Palau is genetically isolated from the populations in the Mariana Islands. Our data confirm that the bats of Palau should be considered a separate conservation unit from the bats of the Mariana Islands, supporting the current subspecies separation of these two populations. Our results also suggest that there is gene flow among islands within the Mariana archipelago and that the bats on these islands, currently classified as two subspecies, should be managed as a single conservation unit, although we refrain from suggesting taxonomic revisions until genetic and morphological data become available from geographically intermediate populations.

The probability of persistence of many species of hibernating bats in the United States is greatly reduced by an emerging infectious disease, white-nose syndrome (WNS). In the United States WNS is rapidly spreading and is associated with a psychrophilic fungus, Geomyces destructans. WNS has caused massive mortality of bats that hibernate. Efforts to control the disease have been ineffective. The culling of bats in hibernacula has been proposed as a way to break the transmission cycle or slow the spread of WNS. We formulated a disease model to examine the efficacy of culling to abate WNS in bat populations. We based the model dynamics on disease transmission in maternity roosts, swarms, and hibernacula, which are the arenas of contact among bats. Our simulations indicated culling will not control WNS in bats primarily because contact rates are high among colonial bats, contact occurs in multiple arenas, and periodic movement between arenas occurs. In general, culling is ineffective in the control of animal diseases in the wild.

Brazilian free-tailed bats (Tadarida brasiliensis) emerge from cave roosts in dense columns in which adjacent bats are separated by only small distances. We describe and quantify variation in the structure of echolocation calls produced by these emerging bats and determine if call structure changes in relation to the rate of emergence measured using thermal infrared imaging. We recorded emergence calls at 2 roosts, 1 housing approximately 200,000 bats and the other approximately 17,000 bats. We found that Brazilian free-tailed bats emit distinct frequency-modulated (FMstart) and constant frequency (CFstart) calls during emergence that are significantly different from echolocation calls they emit while foraging. We propose that these calls provide different information for orientation within the emergence column. CFstart calls are very similar to social calls used by Brazilian free-tailed bats, suggesting 2 potential functions for this call type. The structure of both the FMstart and CFstart calls were not related to the number of bats emerging from a roost, although significant structural differences existed between sites. The differences between sites could be associated with the spacing of bats during emergence, because bats appeared to form tighter columns at the larger roost colony compared to the smaller colony. DOI: 10.1644/09-MAMM-A-302.1.

Threats to and from Bats Bats appear to be able to host an assortment of alarming pathogens, which, if they do not extirpate the bats, have implications for human health (see the Perspective by Daszak ). For example, exposure to bats is the main source of human rabies in the Americas. But rabies is not generally transmitted among people; humans are a dead end for the virus. Streicker et al. (p. 676 , see the cover) show that rabies virus lineages tend to be specific for bat lineages. It seems that although rabies viruses have the potential for rapid evolution, this property alone is not enough to overcome genetic barriers, which inhibit the onward transmission of rabies virus into a new species. White-nose syndrome, an exotic fungal infection of bats, has, over the past 3 years, spread from upstate New York to West Virginia, killing on average 70% of the animals in a hibernating colony. The infection makes bats restless over winter when they should be dormant, which makes them exhaust their fat reserves, resulting in the death of over a million bats. Frick et al. (p. 679 ) have analyzed population data collected on bats in the northeastern United States for the past 30 years and show that, mainly owing to white-nose syndrome, the once abundant little brown bat is heading for regional extinction in the next 16 years or so. This scale of loss of an insectivorous mammal is expected to have repercussions for ecosystem integrity and for the economic costs of agricultural pest control.

The nursing behavior of Mexican free-tailed bats (Tadarida brasiliensis mexicana) was examined in two large maternity cave roosts during six nursing seasons. After depositing pups in large creches, adults return to these creches two or more times daily to nurse. Densities, movements, and roosting associations of pups in creches were documented, and a night-vision device and infrared-sensitive video system were used to observe female-pup reunions and nursing affiliations. Densities of young (< 15 d) pups in creches averaged 4000 pups/m2. Pups moved independently of one another between milk meals. Stable roosting associations among pups were absent, and females evidently could not predict where a given pup would be relocated. Upon returning to the creche, females searched for and relocated pups using vocal and olfactory cues. Experiments with marked individuals demonstrated that females nursed the same pups on subsequent nights. These same experiments indicated that female/pup recognition was mutual and that the pup participated in reunions by moving toward its putative mother. However, pups also attempted to suckle from other females and 35 instances of apparently successful milk “theft” were observed. Observed milk theft was insufficient to account for the frequency of alloparental nursing that was estimated independently using genotype tests. The high densities of bats within roosts and the lack of stable roosting associations among individuals argue against selection for shared nursing via kin selection and/or reciprocity. Errors in pup recognition, milk-dumping by females, and adoption by mothers whose own pup had died may occur, but high pup survival to weaning suggests that adoption is rare. The estimate of alloparental nursing obtained from genotype tests may be inflated as a result of increased opportunities for milk theft caused by our disturbance of adults. Current evidence suggests that energetic costs to females of alloparental nursing and searching for pups are compensated by mutualistic benefits obtained from aggregative roosting.

and Summary Saccopteryx leptura and S. bilineata are closely related, sympacric species of neotropical bats that exhibit marked differences in social organization and dispersion patterns. S. leptura is monogamous and roosts in small groups of 1 to 5 (Y = 2.6) individuals that are finely dispersed. S. bilineata is harem-polygamous and roosts in larger groups of 1 to 42 (Y = 8.1) individuals that are more coarsely dispersed. Allozyme genetic studies of individuals from Trinidad, W I. demonstrate that both species carry similar, high levels of polymorphism and heterozygosity. Although significant genetic heterogeneity was observed among geographical populations of S. leptura, there is no evidence for either species that social structuring leads to inbreeding and the loss of heterozygosity, or that it promotes the development of genetic heterogeneity among social units that could accelerate the evolutionary diversification of these taxa. These results do not support a recently proposed hypothesis that social structuring in mammals has these effects. Observed intercolony genetic heterogeneity among adult males resident in multimale groups of S. bilineata is greater than intercolony heterogeneity of adult females. This is an apparent result of female dispersal and the recruitment of males into their parental groups. These results suggest that the adult males within large colonies may be kin-related.

Previous studies have investigated rabies virus (RABV) epizootiology in Brazilian free-tailed bats (Tadarida brasiliensis) in natural cave roosts. However, little is known about geographic variation in RABV exposure, or if the use of man-made roosts by this species affects enzootic RABV infection dynamics within colonies. We sampled rabies viral neutralizing antibodies in bats at three bridge and three cave roosts at multiple time points during the reproductive season to investigate temporal and roost variation in RABV exposure. We report seropositive bats in all age and sex classes with minimal geographic variation in RABV seroprevalence among Brazilian free-tailed bat colonies in south-central Texas. While roost type was not a significant predictor of RABV seroprevalence, it was significantly associated with seasonal fluctuations, suggesting patterns of exposure that differ between roosts. Temporal patterns suggest increased RABV seroprevalence after parturition in cave colonies, potentially related to an influx of susceptible young, in contrast to more uniform seroprevalence in bridge colonies. This study highlights the importance of life history and roost ecology in understanding patterns of RABV seroprevalence in colonies of the Brazilian free-tailed bat.

Bats are natural reservoirs for the majority of lyssaviruses globally, and are unique among mammals in having exceptional sociality and longevity. Given these facets, and the recognized status of bats as reservoirs for rabies viruses (RABVs) in the Americas, individual bats may experience repeated exposure to RABV during their lifetime. Nevertheless, little information exists with regard to within-host infection dynamics and the role of immunological memory that may result from abortive RABV infection in bats. In this study, a cohort of big brown bats (Eptesicus fuscus) was infected intramuscularly in the left and right masseter muscles with varying doses [10(-0.1)-10(4.9) median mouse intracerebral lethal doses (MICLD(50))] of an E. fuscus RABV variant isolated from a naturally infected big brown bat. Surviving bats were infected a second time at 175 days post-(primary) infection with a dose (10(3.9)-10(4.9) MICLD(50)) of the same RABV variant. Surviving bats were infected a third time at either 175 or 305 days post-(secondary) infection with a dose (10(4.9) MICLD(50)) of the same RABV variant. When correcting for dose, similar mortality was observed following primary and secondary infection, but reduced mortality was observed following the third and last RABV challenge, despite infection with a high viral dose. Inducible RABV-neutralizing antibody titres post-infection were ephemeral among infected individuals, and dropped below levels of detection in several bats between subsequent infections. These results suggest that long-term repeated infection of bats may confer significant immunological memory and reduced susceptibility to RABV infection.

As the human population continues to expand, increased encroachment on natural landscapes and wildlife habitats is expected. Organisms able to acclimate to human-altered environments should have a selective advantage over those unable to do so. Over the past two decades, bats have increasingly begun to roost and raise offspring in spaces beneath pre-cast concrete bridges. Few studies have examined the health or fitness of individuals living in these anthropogenic sites. In the present study, we examined birth size and postnatal growth, as surrogates of reproductive success, in Brazilian free-tailed bat pups born at a natural and a human-made roost. Based on putative stress-related conditions (noise from vehicular traffic, chemical pollutants and a modified social environment) present at bridges, we predicted that bats at these sites would have reduced reproductive success. Contrary to our prediction, pups born at a bridge site were on average heavier and larger at birth and grew faster than those born at a cave site. Also, both birth size and growth rates of pups differ between years. We attribute observed differences to a combination of roost-related conditions (i.e. roost temperature and proximity to foraging areas), climate and maternal effects with larger mothers raising larger pups. Thus, some bridge roosts, at least in the short term, are suitable, and in some cases may provide better conditions, for raising young bat pups than cave roosts.

Bats alter their echolocation in response to changes in ecological and behavioral conditions, but little is known about how they adjust call structure in response to changes in altitude. We examined altitudinal variation in the echolocation of Brazilian free-tailed bats, Tadarida brasiliensis, a species known to fly to altitudes of 3,000 m above the ground. From 50.2 h of recordings, we analyzed 113 high-quality echolocation call sequences recorded from 0 to 862 m above ground level. Bats flying near the ground used shorter, higher-frequency, broader-bandwidth calls compared to bats at higher altitudes, an effect likely due to the greater levels of echo-producing clutter (i.e., vegetation, buildings) found near the ground. When ground-level recordings are excluded, bats continue to shift towards the use of longer-duration, lower-frequency, narrower-bandwidth calls with increasing altitude. We propose that the observed high-altitude changes in call structure are a response to changing acoustic attenuation rates and/or decreasing insect densities at higher altitudes.

During a Myotis sodalis telemetry project in Pennsylvania, USA, in 2000, road-killed M. lucifugus were recorded and a highway survey was initiated. The purpose of this study was to assess the level of mortality from road kills on this colony, verify which species were being killed in traffic and examine the influence of canopy height and structure on flight behavior. On 10 evenings between 15 May and 26 July 2001, bats were counted as they emerged from day roosts and crossed a heavily trafficked highway en route to foraging areas. A total of 26 442 bats were observed cross- ing this highway over 9.29 h of observation. Bats used canopy cover when approaching the highway from roosts. Where canopy cover was lacking adjacent to the highway, fewer bats were counted crossing; where adjacent canopy was low (≤6 m), bats crossed lower and closer to traffic. Motivated by a planned highway upgrade that would extend deforestation of the highway verge, we monitored the flight behavior of M. lucifugus as they crossed a 55 m mowed field. Observations of more than 1700 bats revealed that a vast majority of commuting individuals fly less than 2 m above the ground in the open field. Between 15 May and 14 September 2001, searches for road-killed bats were con- ducted along a section of highway crossed by large numbers of bats. We collected 27 road-killed M. lucifugus, 1 suspected M. sodalis and 1 unidentifiable Myotis sp. Subsequent genetic analyses of mitochondrial DNA sequences confirmed the suspect bat as a federally endangered M. sodalis.

Many emerging and reemerging viruses, such as rabies, SARS, Marburg, and Ebola have bat populations as disease reservoirs. Understanding the spillover from bats to humans and other animals, and the associated health risks requires an analysis of the disease dynamics in bat populations. Traditional compartmental epizootic models, which are relatively easy to implement and analyze, usually impose unrealistic aggregation assumptions about disease-related structure and depend on parameters that frequently are not measurable in field conditions. We propose a novel combination of computational and adaptive modeling approaches that address the maintenance of emerging diseases in bat colonies through individual (intra-host) models of the response of the host to a viral challenge. The dynamics of the individual models are used to define survival, susceptibility and transmission conditions relevant to epizootics as well as to develop and parametrize models of the disease evolution into uniform and diverse populations. Applications of the proposed approach to modeling the effects of immunological heterogeneity on the dynamics of bat rabies are presented.

During the past 12 000 years agricultural systems have transitioned from natural habitats to conventional agricultural regions and recently to large areas of genetically engineered (GE) croplands. This GE revolution occurred for cotton in a span of slightly more than a decade during which a switch occurred in major cotton production areas from growing 100% conventional cotton to an environment in which 95% transgenics are grown. Ecological interactions between GE targeted insects and other insectivorous insects have been investigated. However, the relationships between ecological functions (such as herbivory and ecosystem transport) and agronomic benefits of avian or mammalian insectivores in the transgenic environment generally remain unclear, although the importance of some agricultural pest management services provided by insectivorous species such as the Brazilian free-tailed bat, Tadarida brasiliensis, have been recognized. We developed a dynamic model to predict regional-scale ecological functions in agricultural food webs by using the indicators of insect pest herbivory measured by cotton boll damage and insect emigration from cotton. In the south-central Texas Winter Garden agricultural region we find that the process of insectivory by bats has a considerable impact on both the ecology and valuation of harvest in Bacillus thuringiensis (Bt) transgenic and non- transgenic cotton crops. Predation on agricultural pests by insectivorous bats may enhance the economic value of agricultural systems by reducing the frequency of required spraying and delaying the ultimate need for new pesticides. In the Winter Garden region, the presence of large numbers of insectivorous bats yields a regional summer dispersion of adult pest insects from Bt cotton that is considerably reduced from the moth emigration when bats are absent in either transgenic or non-transgenic crops. This regional decrease of pest numbers impacts insect herbivory on a transcontinental scale. With a few exceptions, we find that the agronomics of both Bt and conventional cotton production is more profitable when large numbers of insectivorous bats are present.

Using data collected with thermal imaging technology, we found a major reduction in population estimates of colony size in the Brazilian free-tailed bat (Tadarida brasiliensis) from 54 million, obtained in 1957 without this technology, to 4 million in 6 major cave colonies in the southwestern United States. The 1957 census was based on human visual observations of cave emergence flights that were subject to potentially high errors. The recent census was produced using an accurate, reproducible counting method and based on complete temporal records of colony emergences. Analysis of emergence flights from dusk through darkness also revealed patterns in group behavior that would be difficult to capture without thermal infrared technology. Flow patterns of bats during emergence flights exhibited characteristic single, double, or triple episodes, with the peak flow during the 1st episode. A consistent rhythmic pattern of flow episodes and pauses was revealed across colonies and was independent of emergence tempo.