U.S. National Park visitor perceptions and behavioral intentions towards actions to prevent white-nose syndrome.

In the United States, the discovery and spread of white-nose syndrome (WNS) has drastically changed how bats and caves are managed. The U.S. National Park Service has been instrumental in the national response to WNS, as it manages extensive cave resources and has a close relationship with the public. However, managers lack information on visitor support for disease prevention measures designed to slow the spread of WNS and minimize human disturbance of vulnerable bat populations. This study utilized the Theory of Planned Behavior to determine how visitor attitudes, subjective norms, and perceived behavioral controls influenced their behavior regarding WNS preventive actions, including participation in educational programming on bats, wearing clothes or shoes in caves that have not been contaminated with the fungus that causes WNS, walking over decontamination mats, and complying with cave closures. During summer of 2019, data were collected using an on-site survey of 1365 visitors to eight U.S. national park units: Oregon Caves, Lava Beds, Carlsbad Caverns, El Malpais, Wind Cave, Jewel Cave, Mammoth Cave, and Cumberland Gap. Visitors were willing to participate in all preventative actions addressed in the survey (77.7%-96.7%). Visitors expressed that engaging in these actions was very desirable (36.0%-65.6%), and their decision to engage in these actions was most strongly influenced by park staff (39.2%-68.8%) or signage (35.5%-61.9%). Attitudes and subjective norms were positive predictors of behavioral intentions for all measures. Perceived behavioral control was not a direct predictor for behavioral intent, but its interaction with attitudes and subjective norms had a moderating influence on intention to comply with multiple WNS preventive actions. With the continued spread of WNS and emergence of other threats to bats, understanding visitor behavioral intent and underlying factors will facilitate successful implementation of preventive actions that are publicly supported and promote conservation of bat populations in U.S. national parks.

Emergence activity at hibernacula differs among four bat species affected by white-nose syndrome.

Prior to the introduction of white-nose syndrome (WNS) to North America, temperate bats were thought to remain within hibernacula throughout most of the winter. However, recent research has shown that bats in the southeastern United States emerge regularly from hibernation and are active on the landscape, regardless of their WNS status. The relationship between winter activity and susceptibility to WNS has yet to be explored but warrants attention, as it may enable managers to implement targeted management for WNS-affected species. We investigated this relationship by implanting 1346 passive integrated transponder (PIT) tags in four species that vary in their susceptibility to WNS. Based on PIT-tag detections, three species entered hibernation from late October to early November. Bats were active at hibernacula entrances on days when midpoint temperatures ranged from -1.94 to 22.78°C (mean midpoint temperature = 8.70 ± 0.33°C). Eastern small-footed bats (Myotis leibii), a species with low susceptibility to WNS, were active throughout winter, with a significant decrease in activity in mid-hibernation (December 16 to February 15). Tricolored bats (Perimyotis subflavus), a species that is highly susceptible to WNS, exhibited an increase in activity beginning in mid-hibernation and extending through late hibernation (February 16 to March 31). Indiana bats (M. sodalis), a species determined to have a medium-high susceptibility to WNS, remained on the landscape into early hibernation (November 1 to December 15), after which we did not record any again until the latter portion of mid-hibernation. Finally, gray bats (M. grisescens), another species with low susceptibility to WNS, maintained low but regular levels of activity throughout winter. Given these results, we determined that emergence activity from hibernacula during winter is highly variable among bat species and our data will assist wildlife managers to make informed decisions regarding the timing of implementation of species-specific conservation actions.

Winter torpor expression varies in four bat species with differential susceptibility to white-nose syndrome.

Studies examining the overwintering behaviors of North American hibernating bats are limited to a handful of species. We deployed temperature-sensitive transmitters on four species of bat that exhibit differences in their susceptibility to white nose syndrome (WNS; Myotis grisescens, M. leibii, M. sodalis, and Perimyotis subflavus) to determine if these differences are correlated with behavior exhibited during hibernation (i.e., torpor expression and arousal frequency). Mean torpor skin temperature (Tsk) and torpor bout duration varied significantly among species (P ≤ 0.024), but arousal Tsk and duration did not (P ≥ 0.057). One of the species with low susceptibility to WNS, M. leibii, had significantly shorter torpor bout durations (37.67 ± 26.89 h) than M. sodalis (260.67 ± 41.33 h), the species with medium susceptibility to WNS. Myotis leibii also had significantly higher torpor Tsk (18.57 °C ± 0.20) than M. grisescens (13.33 °C ± 0.60), a second species with low WNS susceptibility. The high susceptibility species, Perimyotis subflavus, exhibited low torpor Tsk (14.42 °C ± 0.36) but short torpor bouts (72.36 ± 32.16 h). We demonstrate that the four cavernicolous species examined exhibit a wide range in torpid skin temperature and torpor bout duration. Information from this study may improve WNS management in multispecies hibernacula or individual species management by providing insight into how some species may differ in their techniques for overwinter survival.

Contaminant exposure as an additional stressor to bats affected by white-nose syndrome: current evidence and knowledge gaps.

Bats are exposed to numerous threats including pollution and emerging diseases. In North America, the fungal disease white-nose syndrome (WNS) has caused declines in many bat species. While the mechanisms of WNS have received considerable research attention, possible influences of contaminants have not. Herein, we review what is known about contaminant exposure and toxicity for four species whose populations have been severely affected by WNS (Myotis sodalis, M. septentrionalis, M. lucifugus, and Perimyotis subflavus) and identify temporal and spatial data gaps. We determine that there is limited information about the effects of contaminants on bats, and many compounds that have been detected in these bat species have yet to be evaluated for toxicity. The four species examined were exposed to a wide variety of contaminants; however, large spatial and knowledge gaps limit our ability to evaluate if contaminants contribute to species-level declines and if contaminant exposure exacerbates infection by WNS.

Feasting, not fasting: winter diets of cave hibernating bats in the United States.

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.

Molecular Detection of Candidatus Bartonella mayotimonensis in North American Bats.

Candidatus Bartonella mayotimonensis was detected in 2010 from an aortic valve sample of a patient with endocarditis from Iowa, the United States of America. The environmental source of the potentially new endocarditis-causing Bartonella remained elusive. We set out to study the prevalence and diversity of bat-associated Bartonella in North America. During 2015, mist nets and harp traps were used to capture 92 bats belonging to two species: little brown myotis (Myotis lucifugus Le Conte 1831, n = 73) and the gray myotis (M. grisescens A.H. Howell 1909, n = 19) in Kentucky, Michigan, Pennsylvania, and Tennessee. DNA preparations of peripheral blood samples from bats were subjected to a three-marker (gltA, rpoB, and intergenic spacer region [ISR]) multilocus sequence analysis. Sequence-verified gltA-positive PCR amplicons were obtained from nine samples. Three sequences were 99.7-100% identical with the gltA sequence of the Iowa endocarditis patient strain. Analysis of rpoB and ISR sequences demonstrated that one little brown myotis sample from the Upper Peninsula of Michigan contained Bartonella DNA, with 100% sequence identity with the Iowa endocarditis patient strain DNA. It appears possible that bats are a reservoir of Candidatus Bartonella mayotimonensis in North America.

Detection of Pseudogymnoascus destructans on Free-flying Male Bats Captured During Summer in the Southeastern USA.

Pseudogymnoascus destructans, the causal agent of white-nose syndrome (WNS), is commonly found on bats captured both inside and outside caves during hibernation, a time when bats are most vulnerable to infection. It has not been documented in the southeast US on bats captured outside caves or on the landscape in summer. We collected 136 skin swabs from 10 species of bats captured at 20 sites on the Tennessee side of Great Smoky Mountains National Park, 12 May-16 August 2015. Three swabs were found positive for P. destructans, one from a male tricolored bat ( Perimyotis subflavus ) and two from male big brown bats ( Eptesicus fuscus ). This detection of P. destructans on free-flying male bats in the southeast US during summer has potential repercussions for the spread of the fungus to novel bat species and environments. Our finding emphasizes the need to maintain rigorous year-round decontamination of field clothing and equipment until more is understood about the viability of P. destructans found on bats captured outside hibernacula during summer, about the potential for males to act as reservoirs of the fungus, and the risk of fungal transmission and spread.

Molecular detection of the causative agent of white-nose syndrome on Rafinesque's big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the southeastern USA.

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.