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1.  Mercury in bats from the northeastern United States 
This study examines mercury exposure in bats across the northeast U.S. from 2005 to 2009. We collected 1,481 fur and 681 blood samples from 8 states and analyzed them for total Hg. A subset (n = 20) are also analyzed for methylmercury (MeHg). Ten species of bats from the northeast U.S. are represented in this study of which two are protected by the Endangered Species Act (ESA 1973) and two other species are pending review. There are four objectives in this paper: (1) to examine correlates to differences in fur–Hg levels among all of the sampling sites, including age, sex, species, and presence of a Hg point source; (2) define the relationship between blood and fur–Hg levels and the factors that influence that relationship including age, sex, species, reproductive status, and energetic condition; (3) determine the relationships between total Hg and MeHg in five common eastern bat species; and (4) assess the distribution of Hg across bat populations in the northeast. We found total blood and fur mercury was eight times higher in bats captured near point sources compared to nonpoint sources. Blood–Hg and fur–Hg were well correlated with females on average accumulating two times more Hg in fur than males. On average fur MeHg accounted for 86 % (range 71–95 %) of the total Hg in bat fur. Considering that females had high Hg concentrations, beyond that of established levels of concern, suggests there could be negative implications for bat populations from high Hg exposure since Hg is readily transferred to pups via breast milk. Bats provide an integral part of the ecosystem and their protection is considered to be of high priority. More research is needed to determine if Hg is a stressor that is negatively impacting bat populations.
PMCID: PMC3884133  PMID: 24271419
Mercury; Hg; Methylmercury; MeHg; Bats; Northeast United States
2.  Correction: Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome 
PLoS ONE  2013;8(10):10.1371/annotation/2296467f-c10a-4677-8520-490a614ce355.
PMCID: PMC3797215
3.  Hibernating Little Brown Myotis (Myotis lucifugus) Show Variable Immunological Responses to White-Nose Syndrome 
PLoS ONE  2013;8(3):e58976.
White-nose syndrome (WNS) is an emerging infectious disease devastating hibernating North American bat populations that is caused by the psychrophilic fungus Geomyces destructans. Previous histopathological analysis demonstrated little evidence of inflammatory responses in infected bats, however few studies have compared other aspects of immune function between WNS-affected and unaffected bats. We collected bats from confirmed WNS-affected and unaffected sites during the winter of 2008–2009 and compared estimates of their circulating levels of total leukocytes, total immunoglobulins, cytokines and total antioxidants. Bats from affected and unaffected sites did not differ in their total circulating immunoglobulin levels, but significantly higher leukocyte counts were observed in bats from affected sites and particularly in affected bats with elevated body temperatures (above 20°C). Bats from WNS-affected sites exhibited significantly lower antioxidant activity and levels of interleukin-4 (IL-4), a cytokine that induces T cell differentiation. Within affected sites only, bats exhibiting visible fungal infections had significantly lower antioxidant activity and levels of IL-4 compared to bats without visible fungal infections. Overall, bats hibernating in WNS-affected sites showed immunological changes that may be evident of attempted defense against G. destructans. Observed changes, specifically elevated circulating leukocytes, may also be related to the documented changes in thermoregulatory behaviors of affected bats (i.e. increased frequencies in arousal from torpor). Alterations in immune function may reflect expensive energetic costs associated with these processes and intrinsic qualities of the immunocapability of hibernating bats to clear fungal infections. Additionally, lowered antioxidant activity indicates a possible imbalance in the pro- versus antioxidant system, may reflect oxidative tissue damage, and should be investigated as a contributor to WNS-associated morbidity and mortality.
PMCID: PMC3604015  PMID: 23527062
4.  Effects of sunlight on behavior and 25-hydroxyvitamin D levels in two species of Old World fruit bats 
Dermato-endocrinology  2013;5(1):192-198.
It has long been accepted that most vertebrate animals meet their vitamin D requirements from exposure of skin to UV-B (UV-B) radiation. Many factors affect this endogenous synthesis of vitamin D, including season, latitude, time of day, age, presence of hair, and degree of skin pigmentation. Most bats roost in dark places by day and forage at night, and thus have little or no potential for sunlight exposure. Notwithstanding, some tropical species are diurnal and are known to roost in the canopy of trees where they may be exposed to sunlight for up to 12 h each day. In this study, two species of captive tropical bats (both species are active at night but one, Rousettus aegyptiacus, roosts in caves, tombs, and buildings, whereas the other, Pteropus hypomelanus, roosts in trees) were evaluated for their ability to endogenously synthesize vitamin D. Following timed periods of sunlight exposure, blood plasma was analyzed using a competitive protein binding assay (CPBA) to determine concentrations of 25-hydroxyvitamin D [25(OH)D], the major circulating vitamin D metabolite. The ability to photoconvert provitamin D (7-dehydrocholesterol, 7-DHC) in the sub-tropical winter was determined using sunlight exposed borosilicate samples of 7-DHC in hourly increments. Finally, both species were evaluated in their preference for a roost site by the release of individuals into sunlight or shade in timed trials.
Our results support the hypotheses: (1) when exposed to natural sunlight, both species exhibited an ability to endogenously synthesize vitamin D, although significant differences were found between the two, (2) photoconversion of 7-DHC to previtamin D3 is possible during the mid-day hours of a sub-tropical winter day and (3) captive, cave roosting R. aegyptiacus will choose shaded roost sites while captive P. hypomelanus will show no preference for either shade or sun.
PMCID: PMC3897589  PMID: 24494054
bats; calcium; Chiroptera; sunlight; UV-B radiation; vitamin D
5.  Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies 
Biology Letters  2011;7(6):950-953.
White-nose syndrome (WNS) is a disease responsible for unprecedented mortality in hibernating bats. First observed in a New York cave in 2006, mortality associated with WNS rapidly appeared in hibernacula across the northeastern United States. We used yearly presence–absence data on WNS-related mortality among hibernating bat colonies in the Northeast to determine factors influencing its spread. We evaluated hazard models to test hypotheses about the association between the timing of mortality and colony-level covariates, such as distance from the first WNS-affected site, colony size, species diversity, species composition and type of hibernaculum (cave or mine). Distance to origin and colony size had the greatest effects on WNS hazard over the range of observations; the type of hibernaculum and species composition had weaker effects. The distance effect showed a temporal decrease in magnitude, consistent with the pattern of an expanding epizootic. Large, cave-dwelling bat colonies with high proportions of Myotis lucifugus or other species that seek humid microclimates tended to experience early mortality. Our results suggest that the timing of mortality from WNS is largely dependent on colony location, and large colonies tend to be first in an area to experience high mortality associated with WNS.
PMCID: PMC3210657  PMID: 21632616
bat; colony size; Cox proportional hazards model; epizootic; hibernacula; white-nose syndrome
6.  Bats Track and Exploit Changes in Insect Pest Populations 
PLoS ONE  2012;7(8):e43839.
The role of bats or any generalist predator in suppressing prey populations depends on the predator's ability to track and exploit available prey. Using a qPCR fecal DNA assay, we document significant association between numbers of Brazilian free-tailed bats (Tadarida brasiliensis) consuming corn earworm (CEW) moths (Helicoverpa zea) and seasonal fluctuations in CEW populations. This result is consistent with earlier research linking the bats' diet to patterns of migration, abundance, and crop infestation by important insect pests. Here we confirm opportunistic feeding on one of the world's most destructive insects and support model estimates of the bats' ecosystem services. Regression analysis of CEW consumption versus the moth's abundance at four insect trapping sites further indicates that bats track local abundance of CEW within the regional landscape. Estimates of CEW gene copies in the feces of bats are not associated with seasonal or local patterns of CEW abundance, and results of captive feeding experiments indicate that our qPCR assay does not provide a direct measure of numbers or biomass of prey consumed. Our results support growing evidence for the role of generalist predators, and bats specifically, as agents for biological control and speak to the value of conserving indigenous generalist predators.
PMCID: PMC3432057  PMID: 22952782
7.  Climate and Weather Impact Timing of Emergence of Bats 
PLoS ONE  2012;7(8):e42737.
Interest in forecasting impacts of climate change have heightened attention in recent decades to how animals respond to variation in climate and weather patterns. One difficulty in determining animal response to climate variation is lack of long-term datasets that record animal behaviors over decadal scales. We used radar observations from the national NEXRAD network of Doppler weather radars to measure how group behavior in a colonially-roosting bat species responded to annual variation in climate and daily variation in weather over the past 11 years. Brazilian free-tailed bats (Tadarida brasiliensis) form dense aggregations in cave roosts in Texas. These bats emerge from caves daily to forage at high altitudes, which makes them detectable with Doppler weather radars. Timing of emergence in bats is often viewed as an adaptive trade-off between emerging early and risking predation or increased competition and emerging late which restricts foraging opportunities. We used timing of emergence from five maternity colonies of Brazilian free-tailed bats in south-central Texas during the peak lactation period (15 June–15 July) to determine whether emergence behavior was associated with summer drought conditions and daily temperatures. Bats emerged significantly earlier during years with extreme drought conditions than during moist years. Bats emerged later on days with high surface temperatures in both dry and moist years, but there was no relationship between surface temperatures and timing of emergence in summers with normal moisture levels. We conclude that emergence behavior is a flexible animal response to climate and weather conditions and may be a useful indicator for monitoring animal response to long-term shifts in climate.
PMCID: PMC3411708  PMID: 22876331
8.  Possible cross-species transmission of circoviruses and cycloviruses among farm animals 
The Journal of General Virology  2011;92(Pt 4):768-772.
Circoviruses consist of highly prevalent and genetically diverse porcine and avian pathogens. The genomes of cycloviruses, a proposed new genus in the family Circoviridae, were recently identified in human and chimpanzee faeces. Here, six cyclovirus and four circovirus genomes from the tissues of chickens, goats, cows, and a bat were amplified and sequenced using rolling-circle amplification and inverse PCR. A goat cyclovirus was nearly identical to a cyclovirus from a cow. USA beef contained circoviruses with >99 % similarity to porcine circovirus 2b. Circoviruses in chicken were related to those of pigeons. The close genetic similarity of a subset of cycloviruses and circoviruses replicating in distinct animal species may reflect recent cross-species transmissions. Further studies will be required to determine the impact of these highly prevalent infections on the health of farm animals.
PMCID: PMC3133700  PMID: 21177928
9.  Response of a Specialist Bat to the Loss of a Critical Resource 
PLoS ONE  2011;6(12):e28821.
Human activities have negatively impacted many species, particularly those with unique traits that restrict their use of resources and conditions to specific habitats. Unfortunately, few studies have been able to isolate the individual and combined effects of different threats on population persistence in a natural setting, since not all organisms can be associated with discrete habitat features occurring over limited spatial scales. We present the results of a field study that examines the short-term effects of roost loss in a specialist bat using a conspicuous, easily modified resource. We mimicked roost loss in the natural habitat and monitored individuals before and after the perturbation to determine patterns of resource use, spatial movements, and group stability. Our study focused on the disc-winged bat Thyroptera tricolor, a species highly morphologically specialized for roosting in the developing furled leaves of members of the order Zingiberales. We found that the number of species used for roosting increased, that home range size increased (before: mean 0.14±SD 0.08 ha; after: 0.73±0.68 ha), and that mean association indices decreased (before: 0.95±0.10; after: 0.77±0.18) once the roosting habitat was removed. These results demonstrate that the removal of roosting resources is associated with a decrease in roost-site preferences or selectivity, an increase in mobility of individuals, and a decrease in social cohesion. These responses may reduce fitness by potentially increasing energetic expenditure, predator exposure, and a decrease in cooperative interactions. Despite these potential risks, individuals never used roost-sites other than developing furled leaves, suggesting an extreme specialization that could ultimately jeopardize the long-term persistence of this species' local populations.
PMCID: PMC3244425  PMID: 22216118
10.  Specific Alterations in Complement Protein Activity of Little Brown Myotis (Myotis lucifugus) Hibernating in White-Nose Syndrome Affected Sites 
PLoS ONE  2011;6(11):e27430.
White-nose syndrome (WNS) is the most devastating condition ever reported for hibernating bats, causing widespread mortality in the northeastern United States. The syndrome is characterized by cutaneous lesions caused by a recently identified psychrophilic and keratinophylic fungus (Geomyces destructans), depleted fat reserves, atypical behavior, and damage to wings; however, the proximate cause of mortality is still uncertain. To assess relative levels of immunocompetence in bats hibernating in WNS-affected sites compared with levels in unaffected bats, we describe blood plasma complement protein activity in hibernating little brown myotis (Myotis lucifugus) based on microbicidal competence assays using Escherichia coli, Staphylococcus aureus and Candida albicans. Blood plasma from bats collected during mid-hibernation at WNS-affected sites had higher bactericidal ability against E. coli and S. aureus, but lower fungicidal ability against C. albicans when compared with blood plasma from bats collected at unaffected sites. Within affected sites during mid-hibernation, we observed no difference in microbicidal ability between bats displaying obvious fungal infections compared to those without. Bactericidal ability against E. coli decreased significantly as hibernation progressed in bats collected from an affected site. Bactericidal ability against E. coli and fungicidal ability against C. albicans were positively correlated with body mass index (BMI) during late hibernation. We also compared complement activity against the three microbes within individuals and found that the ability of blood plasma from hibernating M. lucifugus to lyse microbial cells differed as follows: E. coli>S. aureus>C. albicans. Overall, bats affected by WNS experience both relatively elevated and reduced innate immune responses depending on the microbe tested, although the cause of observed immunological changes remains unknown. Additionally, considerable trade-offs may exist between energy conservation and immunological responses. Relationships between immune activity and torpor, including associated energy expenditure, are likely critical components in the development of WNS.
PMCID: PMC3227581  PMID: 22140440
11.  Thermal Windows on Brazilian Free-tailed Bats Facilitate Thermoregulation during Prolonged Flight 
The Brazilian free-tailed bat (Tadarida brasiliensis) experiences challenging thermal conditions while roosting in hot caves, flying during warm daylight conditions, and foraging at cool high altitudes. Using thermal infrared cameras, we identified hot spots along the flanks of free-ranging Brazilian free-tailed bats, ventral to the extended wings. These hot spots are absent in syntopic cave myotis (Myotis velifer), a species that forages over relatively short distances, and does not engage in long-distance migration. We hypothesized that the hot spots, or “radiators,” on Brazilian free-tailed bats may be adaptations for migration, particularly in this long-distance, high-flying species. We examined the vasculature of radiators on Brazilian free-tailed bats with transillumination to characterize the unique arrangements of arteries and veins that are positioned perpendicular to the body in the proximal region of the wing. We hypothesized that these radiators aid in maintaining heat balance by flushing the uninsulated thermal window with warm blood, thereby dissipating heat while bats are flying under warm conditions, but shunting blood away and conserving heat when they are flying in cooler air at high altitudes. We also examined fluid-preserved specimens representing 122 species from 15 of 18 chiropteran families and radiators appeared present only in species in the family Molossidae, including both sedentary and migratory species and subspecies. Thus, the radiator appears to be a unique trait that may facilitate energy balance and water balance during sustained dispersal, foraging, and long-distance migration.
PMCID: PMC2931312  PMID: 20811514
12.  Win-Win for Wind and Wildlife: A Vision to Facilitate Sustainable Development 
PLoS ONE  2011;6(4):e17566.
Wind energy offers the potential to reduce carbon emissions while increasing energy independence and bolstering economic development. However, wind energy has a larger land footprint per Gigawatt (GW) than most other forms of energy production, making appropriate siting and mitigation particularly important. Species that require large unfragmented habitats and those known to avoid vertical structures are particularly at risk from wind development. Developing energy on disturbed lands rather than placing new developments within large and intact habitats would reduce cumulative impacts to wildlife. The U.S. Department of Energy estimates that it will take 241 GW of terrestrial based wind development on approximately 5 million hectares to reach 20% electricity production for the U.S. by 2030. We estimate there are ∼7,700 GW of potential wind energy available across the U.S., with ∼3,500 GW on disturbed lands. In addition, a disturbance-focused development strategy would avert the development of ∼2.3 million hectares of undisturbed lands while generating the same amount of energy as development based solely on maximizing wind potential. Wind subsidies targeted at favoring low-impact developments and creating avoidance and mitigation requirements that raise the costs for projects impacting sensitive lands could improve public value for both wind energy and biodiversity conservation.
PMCID: PMC3076357  PMID: 21533285
13.  Ecology of Rabies Virus Exposure in Colonies of Brazilian Free-Tailed Bats (Tadarida brasiliensis) at Natural and Man-Made Roosts in Texas 
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.
PMCID: PMC2944840  PMID: 19492942
Brazilian free-tailed bat; Epizootiology; Rabies virus; Roost ecology
14.  Bat Guano Virome: Predominance of Dietary Viruses from Insects and Plants plus Novel Mammalian Viruses▿  
Journal of Virology  2010;84(14):6955-6965.
Bats are hosts to a variety of viruses capable of zoonotic transmissions. Because of increased contact between bats, humans, and other animal species, the possibility exists for further cross-species transmissions and ensuing disease outbreaks. We describe here full and partial viral genomes identified using metagenomics in the guano of bats from California and Texas. A total of 34% and 58% of 390,000 sequence reads from bat guano in California and Texas, respectively, were related to eukaryotic viruses, and the largest proportion of those infect insects, reflecting the diet of these insectivorous bats, including members of the viral families Dicistroviridae, Iflaviridae, Tetraviridae, and Nodaviridae and the subfamily Densovirinae. The second largest proportion of virus-related sequences infects plants and fungi, likely reflecting the diet of ingested insects, including members of the viral families Luteoviridae, Secoviridae, Tymoviridae, and Partitiviridae and the genus Sobemovirus. Bat guano viruses related to those infecting mammals comprised the third largest group, including members of the viral families Parvoviridae, Circoviridae, Picornaviridae, Adenoviridae, Poxviridae, Astroviridae, and Coronaviridae. No close relative of known human viral pathogens was identified in these bat populations. Phylogenetic analysis was used to clarify the relationship to known viral taxa of novel sequences detected in bat guano samples, showing that some guano viral sequences fall outside existing taxonomic groups. This initial characterization of the bat guano virome, the first metagenomic analysis of viruses in wild mammals using second-generation sequencing, therefore showed the presence of previously unidentified viral species, genera, and possibly families. Viral metagenomics is a useful tool for genetically characterizing viruses present in animals with the known capability of direct or indirect viral zoonosis to humans.
PMCID: PMC2898246  PMID: 20463061
15.  Global Conservation Significance of Ecuador's Yasuní National Park 
PLoS ONE  2010;5(1):e8767.
The threats facing Ecuador's Yasuní National Park are emblematic of those confronting the greater western Amazon, one of the world's last high-biodiversity wilderness areas. Notably, the country's second largest untapped oil reserves—called “ITT”—lie beneath an intact, remote section of the park. The conservation significance of Yasuní may weigh heavily in upcoming state-level and international decisions, including whether to develop the oil or invest in alternatives.
Methodology/Principal Findings
We conducted the first comprehensive synthesis of biodiversity data for Yasuní. Mapping amphibian, bird, mammal, and plant distributions, we found eastern Ecuador and northern Peru to be the only regions in South America where species richness centers for all four taxonomic groups overlap. This quadruple richness center has only one viable strict protected area (IUCN levels I–IV): Yasuní. The park covers just 14% of the quadruple richness center's area, whereas active or proposed oil concessions cover 79%. Using field inventory data, we compared Yasuní's local (alpha) and landscape (gamma) diversity to other sites, in the western Amazon and globally. These analyses further suggest that Yasuní is among the most biodiverse places on Earth, with apparent world richness records for amphibians, reptiles, bats, and trees. Yasuní also protects a considerable number of threatened species and regional endemics.
Yasuní has outstanding global conservation significance due to its extraordinary biodiversity and potential to sustain this biodiversity in the long term because of its 1) large size and wilderness character, 2) intact large-vertebrate assemblage, 3) IUCN level-II protection status in a region lacking other strict protected areas, and 4) likelihood of maintaining wet, rainforest conditions while anticipated climate change-induced drought intensifies in the eastern Amazon. However, further oil development in Yasuní jeopardizes its conservation values. These findings form the scientific basis for policy recommendations, including stopping any new oil activities and road construction in Yasuní and creating areas off-limits to large-scale development in adjacent northern Peru.
PMCID: PMC2808245  PMID: 20098736
16.  Nutrition or Detoxification: Why Bats Visit Mineral Licks of the Amazonian Rainforest 
PLoS ONE  2008;3(4):e2011.
Many animals in the tropics of Africa, Asia and South America regularly visit so-called salt or mineral licks to consume clay or drink clay-saturated water. Whether this behavior is used to supplement diets with locally limited nutrients or to buffer the effects of toxic secondary plant compounds remains unclear. In the Amazonian rainforest, pregnant and lactating bats are frequently observed and captured at mineral licks. We measured the nitrogen isotope ratio in wing tissue of omnivorous short-tailed fruit bats, Carollia perspicillata, and in an obligate fruit-eating bat, Artibeus obscurus, captured at mineral licks and at control sites in the rainforest. Carollia perspicillata with a plant-dominated diet were more often captured at mineral licks than individuals with an insect-dominated diet, although insects were more mineral depleted than fruits. In contrast, nitrogen isotope ratios of A. obscurus did not differ between individuals captured at mineral lick versus control sites. We conclude that pregnant and lactating fruit-eating bats do not visit mineral licks principally for minerals, but instead to buffer the effects of secondary plant compounds that they ingest in large quantities during periods of high energy demand. These findings have potential implications for the role of mineral licks for mammals in general, including humans.
PMCID: PMC2292638  PMID: 18431492

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