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"Johnson, Joseph S."
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The White-Nose Syndrome Transcriptome: Activation of Anti-fungal Host Responses in Wing Tissue of Hibernating Little Brown Myotis
by
Field, Kenneth A.
,
Rogers, Elizabeth J.
,
Behr, Melissa J.
in
Animals
,
Ascomycota - pathogenicity
,
Bats
2015
White-nose syndrome (WNS) in North American bats is caused by an invasive cutaneous infection by the psychrophilic fungus Pseudogymnoascus destructans (Pd). We compared transcriptome-wide changes in gene expression using RNA-Seq on wing skin tissue from hibernating little brown myotis (Myotis lucifugus) with WNS to bats without Pd exposure. We found that WNS caused significant changes in gene expression in hibernating bats including pathways involved in inflammation, wound healing, and metabolism. Local acute inflammatory responses were initiated by fungal invasion. Gene expression was increased for inflammatory cytokines, including interleukins (IL) IL-1β, IL-6, IL-17C, IL-20, IL-23A, IL-24, and G-CSF and chemokines, such as Ccl2 and Ccl20. This pattern of gene expression changes demonstrates that WNS is accompanied by an innate anti-fungal host response similar to that caused by cutaneous Candida albicans infections. However, despite the apparent production of appropriate chemokines, immune cells such as neutrophils and T cells do not appear to be recruited. We observed upregulation of acute inflammatory genes, including prostaglandin G/H synthase 2 (cyclooxygenase-2), that generate eicosanoids and other nociception mediators. We also observed differences in Pd gene expression that suggest host-pathogen interactions that might determine WNS progression. We identified several classes of potential virulence factors that are expressed in Pd during WNS, including secreted proteases that may mediate tissue invasion. These results demonstrate that hibernation does not prevent a local inflammatory response to Pd infection but that recruitment of leukocytes to the site of infection does not occur. The putative virulence factors may provide novel targets for treatment or prevention of WNS. These observations support a dual role for inflammation during WNS; inflammatory responses provide protection but excessive inflammation may contribute to mortality, either by affecting torpor behavior or causing damage upon emergence in the spring.
Journal Article
Seasonal roost selection and activity of a remnant population of northern myotis in Pennsylvania
by
Turner, Gregory G.
,
Johnson, Joseph S.
,
Lewis, Mattea A.
in
Acoustic tracking
,
Analysis
,
Animal diseases
2022
The decline in northern myotis ( Myotis septentrionalis ) populations due to the disease white-nose syndrome (WNS) has led to the species receiving federal protection in the United States and Canada, requiring conservation of critical habitats. However, considerably more is known about summer habitat preferences of northern myotis compared to late summer through winter. Our goal was to describe the seasonal presence and habitat use of a remnant colony of northern myotis in central Pennsylvania. We radio-tagged 31 northern myotis and established 6 acoustic monitoring stations to document activity from 2017–2021. We found that roost trees used during the maternity season by reproductive females were occupied by bats during both summer (21 June–14 August) and autumn (15 August–31 October), indicating similar habitat use patterns between seasons. During this time, both males and females preferred to roost in dead and declining trees. No other variable influenced male use, but females also preferred trees located close to water and in forest stands with higher basal area than randomly located trees. Northern myotis with active transmitters never left the study area and were tracked to roosts until early November. During October and November, a female and male were tracked to an underground network of air-filled voids (the Milieu Souterrain Superficiel) we presume to be a hibernaculum. Northern myotis calls were recorded outside this roost between March and October, and bats were observed emerging from this roost during spring and autumn but not summer. Acoustic activity at this site exhibited a seasonal pattern that differed from acoustic activity near roost trees and foraging areas, with a peak of activity during late summer when northern myotis are known to swarm. These data show that northern myotis maternity roosts are used extensively outside of summer and may be vulnerable to forestry practices that occur even outside of the pup-rearing season. These data also support the growing evidence that some northern myotis hibernate outside of caves and mines.
Journal Article
Winter habitats of bats in Texas
by
Meierhofer, Melissa B.
,
Pierce, Brian L.
,
Morrison, Michael L.
in
Air temperature
,
Animal behavior
,
Animal diseases
2019
Few studies have described winter microclimate selection by bats in the southern United States. This is of particular importance as the cold-adapted fungus, Pseudogymnoascus destructans, which causes the fatal bat disease white-nose syndrome (WNS), continues to spread into southern United States. To better understand the suitability of winter bat habitats for the growth of P. destructans in this region, we collected roost temperature and vapor pressure deficit from 97 hibernacula in six ecoregions in Texas during winter 2016-17 and 2017-18. We also measured skin temperature of Rafinesque's big-eared bats (Corynorhinus townsendii), Townsend's big-eared bats (C. townsendii), big-brown bats (Eptesicus fuscus), southeastern myotis (Myotis austroriparius), cave myotis (M. velifer), tri-colored bats (Perimyotis subflavus), and Mexican free-tailed bats (Tadarida brasiliensis) during hibernation to study their use of torpor in these habitats. We found that temperatures within hibernacula were strongly correlated with external air temperatures and were often within the optimal range of temperatures for P. destructans growth. Hibernacula and skin temperatures differed among species, with Rafinesque's big-eared bats, southeastern myotis, and Mexican free-tailed bats occupying warmer microclimates and having higher torpid skin temperatures. For species that were broadly distributed throughout Texas, hibernacula and skin temperatures differed within species by ecoregion; Tri-colored bats and cave myotis in colder, northern regions occupied colder microclimates within hibernacula and exhibited colder skin temperatures, than individuals of the same species in warmer, southern regions. These data illustrate the variability in microclimates used as hibernacula by bats in Texas and suggest similar variation in susceptibility to WNS in the state. Thus, monitoring microclimates at winter roosts may help predict where WNS may develop, and where management efforts would be most effective.
Journal Article
Summer day-roost selection by eastern red bats varies between areas with different land-use histories
by
Monarchino, Maria N.
,
Behan, Marnie L.
,
Johnson, Joseph S.
in
Animal behavior
,
Bats
,
Bats (Animals)
2020
The eastern red bat (Lasiurus borealis) is widely considered to be in decline, inspiring interest in identifying important habitats for conservation in the eastern United States. Unfortunately, knowledge of important day-roosting habitats is lacking for much of the species' range. We examined patterns of day-roost selection by male and female eastern red bats at two study sites in southeastern Ohio, U. S. A, to help fill this information gap. We radio-tagged 28 male and 25 female bats during the summers of 2016-2019 and located 53 male and 74 female roosts. Day-roost selection differed between sexes and study areas. In a mostly even-aged forest with significant historical disturbance, we found males and females roosting in trees located at higher elevations, with no clear selection based on tree or stand characteristics. Specifically, males selected trees with larger diameters located at lower, cooler elevations than females, which selected smaller diameter trees found at higher, warmer elevations. However, in a forest with less historical disturbance and more structural diversity, we found sexes differed in how they selected from available habitats. These data show that heterogeneity in environmental conditions can lead to different patterns in selection, even between sites located within a small geographic area. They also show that eastern red bats sexually segregate on the local landscape in the presence of diverse forest conditions but may not do so in the absence of such diversity. We recommend managing forests to maintain structural diversity across an elevational gradient to provide male and female eastern red bats with suitable day-roosting habitat in southeast Ohio.
Journal Article
Host, Pathogen, and Environmental Characteristics Predict White-Nose Syndrome Mortality in Captive Little Brown Myotis (Myotis lucifugus)
by
Winters, Harrison D.
,
Sigler, Lauren E.
,
Kath, Joseph A.
in
Animal behavior
,
Animal diseases
,
Animals
2014
An estimated 5.7 million or more bats died in North America between 2006 and 2012 due to infection with the fungus Pseudogymnoascus destructans (Pd) that causes white-nose syndrome (WNS) during hibernation. The behavioral and physiological changes associated with hibernation leave bats vulnerable to WNS, but the persistence of bats within the contaminated regions of North America suggests that survival might vary predictably among individuals or in relation to environmental conditions. To investigate variables influencing WNS mortality, we conducted a captive study of 147 little brown myotis (Myotis lucifugus) inoculated with 0, 500, 5000, 50,000, or 500,000 Pd conidia and hibernated for five months at either 4 or 10°C. We found that female bats were significantly more likely to survive hibernation, as were bats hibernated at 4°C, and bats with greater body condition at the start of hibernation. Although all bats inoculated with Pd exhibited shorter torpor bouts compared to controls, a characteristic of WNS, only bats inoculated with 500 conidia had significantly lower survival odds compared to controls. These data show that host and environmental characteristics are significant predictors of WNS mortality, and that exposure to up to 500 conidia is sufficient to cause a fatal infection. These results also illustrate a need to quantify dynamics of Pd exposure in free-ranging bats, as dynamics of WNS produced in captive studies inoculating bats with several hundred thousand conidia may differ from those in the wild.
Journal Article
Frequent Arousals from Winter Torpor in Rafinesque’s Big-Eared Bat (Corynorhinus rafinesquii)
by
Thomas, Steven C.
,
Johnson, Joseph S.
,
Lacki, Michael J.
in
Activity patterns
,
Ambient temperature
,
Animal behavior
2012
Extensive use of torpor is a common winter survival strategy among bats; however, data comparing various torpor behaviors among species are scarce. Winter torpor behaviors are likely to vary among species with different physiologies and species inhabiting different regional climates. Understanding these differences may be important in identifying differing susceptibilities of species to white-nose syndrome (WNS) in North America. We fitted 24 Rafinesque's big-eared bats (Corynorhinus rafinesquii) with temperature-sensitive radio-transmitters, and monitored 128 PIT-tagged big-eared bats, during the winter months of 2010 to 2012. We tested the hypothesis that Rafinesque's big-eared bats use torpor less often than values reported for other North American cave-hibernators. Additionally, we tested the hypothesis that Rafinesque's big-eared bats arouse on winter nights more suitable for nocturnal foraging. Radio-tagged bats used short (2.4 d ± 0.3 (SE)), shallow (13.9°C ± 0.6) torpor bouts and switched roosts every 4.1 d ± 0.6. Probability of arousal from torpor increased linearly with ambient temperature at sunset (P<0.0001), and 83% (n=86) of arousals occurred within 1 hr of sunset. Activity of PIT-tagged bats at an artificial maternity/hibernaculum roost between November and March was positively correlated with ambient temperature at sunset (P<0.0001), with males more active at the roost than females. These data show Rafinesque's big-eared bat is a shallow hibernator and is relatively active during winter. We hypothesize that winter activity patterns provide Corynorhinus species with an ecological and physiological defense against the fungus causing WNS, and that these bats may be better suited to withstand fungal infection than other cave-hibernating bat species in eastern North America.
Journal Article
Capture rates of Eptesicus fuscus increase following white‐nose syndrome across the eastern US
by
Turner, Gregory G.
,
Simonis, Molly C.
,
Johnson, Joseph S.
in
Animal diseases
,
Animal lactation
,
Animal populations
2024
Emerging infectious diseases threaten wildlife globally. While the effects of infectious diseases on hosts with severe infections and high mortality rates often receive considerable attention, effects on hosts that persist despite infection are less frequently studied. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a persisting species susceptible to infection by the invasive fungal pathogen Pseudogymnoascus destructans (Pd; causative agent for white‐nose syndrome), across the eastern US using a 30‐year dataset. Capture rates of male and female E. fuscus increased from preinvasion to pathogen establishment years, with greater increases to the capture rates of females than males. Among females, capture rates of pregnant and post‐lactating females increased by pathogen establishment. We outline potential mechanisms for these broad demographic changes in E. fuscus capture rates (i.e., increases to foraging from energy deficits created by Pd infection, increases to relative abundance, or changes to reproductive cycles), and suggest future research for identifying mechanisms for increasing capture rates across the eastern US. These data highlight the importance of understanding how populations of persisting host species change following pathogen invasion across a broad spatial scale. Understanding changes to population composition following pathogen invasion can identify broad ecological patterns across space and time, and open new avenues for research to identify drivers of those patterns. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a species that is annualy exposed and infected by the invasive fungal pathogen Pseudogymnoascus destructans (Pd); causative agent for white‐nose syndrome), using a 30‐year dataset across the eastern US. Here, the overall capture rates of adult E. fuscus increased from preinvasion to Pd establishment years across the eastern US. In conclusion, our work highlights the need to better understand how host populations change across broad spatial scales with continued pathogen exposure.
Journal Article
Buildings provide vital habitat for little brown myotis (Myotis lucifugus) in a high‐elevation landscape
by
Treanor, John J.
,
Slusher, Alexandra C.
,
Johnson, Joseph S.
in
adults
,
altitude
,
Ambient temperature
2019
Bats in North America are currently experiencing dramatic population declines due to the disease white‐nose syndrome. The long‐term viability of vulnerable species requires recognition of critical habitats, including those also occupied by humans. Our study aimed to quantify the importance of buildings to little brown myotis (Myotis lucifugus) in Yellowstone National Park, a high‐elevation landscape with relatively few human structures and abundant alternative roosting habitat. We measured roost preferences and thermoregulation in adult male and female bats roosting in buildings, trees, and rocks using temperature‐sensitive radio‐transmitters. We also studied microclimates within each roost type for comparison to roost preferences. We found reproductive females roosting in building attics on 84% of all possible days, while males roosted exclusively in rock crevices or in trees. This dichotomous roosting pattern reflected differences in roost microclimates. All roost types buffered bats from daily minimum ambient temperatures; however, buildings were more insulated from low ambient temperatures during the middle of the maternity season. Male bats roosting in rocks and trees predominantly thermoconformed to roost temperatures, while females roosting in buildings sustained higher body temperatures than males throughout the day. Pregnant and lactating females also used torpor frequently, with skin temperatures reaching <10°C, and a gestation period lasting 49–89 d. These results show that cool summer temperatures at high elevations present an energetic challenge to little brown myotis. Buildings provide critical habitat for reproductive females and likely allow for larger populations than would be possible in their absence, making these roosts a priority for long‐term conservation of this declining species.
Journal Article
Correction: Winter habitats of bats in Texas
2019
[This corrects the article DOI: 10.1371/journal.pone.0220839.].
Journal Article
Long‐term exposure to an invasive fungal pathogen decreases Eptesicus fuscus body mass with increasing latitude
2023
Invasive pathogens threaten wildlife health and biodiversity. Physiological responses of species highly susceptible to pathogen infections following invasion are well described. However, the responses of less susceptible species (relative to highly susceptible species) are not well known. Latitudinal gradients, which can influence body condition via Bergmann's rule and/or reflect the time it takes for an introduced pathogen to spread geographically, add an additional layer for how mammalian species respond to pathogen exposure. Our goal was to understand how hosts less susceptible to pathogen infections respond to long‐term pathogen exposure across a broad latitudinal gradient. We examined changes in body mass throughout pathogen exposure time across the eastern United States (latitude ranging 30.5° N–44.8° N) in Eptesicus fuscus, a bat species classified as less susceptible to infection (relative to highly susceptible species) by the invasive fungal pathogen that causes white‐nose syndrome, Pseudogymnoascus destructans (Pd). Using 30 years of spring through fall adult capture records, we created linear mixed‐effects models for female and male bats to determine how mass or mass variation changed across the eastern United States from pre‐Pd invasion years through Pd invasion (0–1 years with Pd), epidemic (2–4 years with Pd), and established years (5+ years with Pd). By Pd establishment, all female and male bats decreased body mass with increasing latitude across a spatial threshold at 39.6° N. Differences in bat mass north and south of the spatial threshold progressively increased over Pd exposure time‐steps such that body mass was lower in northern latitudes compared to southern latitudes by Pd establishment. Results indicated that the progressive differences in E. fuscus body mass with latitude across the eastern United States are due to long‐term pathogen exposure; however, other environmental and ecological pressures may contribute to decreases in E. fuscus body mass with latitude and long‐term pathogen exposure. As pathogen introductions and emerging infectious diseases become more prevalent on the landscape, it is imperative that we understand how less susceptible species directly and indirectly respond to long‐term pathogen exposure in order to maintain population health in surviving species.
Journal Article