scholarly journals White-nose syndrome restructures bat skin microbiomes

2019 ◽  
Author(s):  
Meghan Ange-Stark ◽  
Tina L. Cheng ◽  
Joseph R. Hoyt ◽  
Kate E. Langwig ◽  
Katy L. Parise ◽  
...  
Keyword(s):  
Fungal Species ◽  
Myotis Lucifugus ◽  
Skin Microbiome ◽  
Pseudogymnoascus Destructans ◽  
Fungal Community Composition ◽  
Microbial Composition ◽  
Pathogen Invasion ◽  
White Nose Syndrome ◽  
Bacterial Microbiome ◽  
Species Specific

AbstractThe skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus,Eptesicus fuscus, andPerimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen,Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and ITS amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructansis present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas present, despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence ofP. destructansfor any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of WNS inM. lucifugus, but not for other bat species impacted by white-nose syndrome.

scholarly journals Hepatic lipid signatures of little brown bats (Myotis lucifugus) and big brown bats (Eptesicus fuscus) at early stages of white-nose syndrome

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Evan L. Pannkuk ◽  
Nicole A. S.-Y. Dorville ◽  
Yvonne A. Dzal ◽  
Quinn E. Fletcher ◽  
Kaleigh J. O. Norquay ◽  
...  
Keyword(s):  
Lipid Metabolism ◽  
Fatty Acid Distribution ◽  
Eptesicus Fuscus ◽  
Myotis Lucifugus ◽  
Pseudogymnoascus Destructans ◽  
Hepatic Lipid ◽  
Early Stages ◽  
White Nose Syndrome ◽  
Big Brown Bats ◽  
Little Brown Bats

AbstractWhite-nose syndrome (WNS) is an emergent wildlife fungal disease of cave-dwelling, hibernating bats that has led to unprecedented mortalities throughout North America. A primary factor in WNS-associated bat mortality includes increased arousals from torpor and premature fat depletion during winter months. Details of species and sex-specific changes in lipid metabolism during WNS are poorly understood and may play an important role in the pathophysiology of the disease. Given the likely role of fat metabolism in WNS and the fact that the liver plays a crucial role in fatty acid distribution and lipid storage, we assessed hepatic lipid signatures of little brown bats (Myotis lucifugus) and big brown bats (Eptesicus fuscus) at an early stage of infection with the etiological agent, Pseudogymnoascus destructans (Pd). Differences in lipid profiles were detected at the species and sex level in the sham-inoculated treatment, most strikingly in higher hepatic triacylglyceride (TG) levels in E. fuscus females compared to males. Interestingly, several dominant TGs (storage lipids) decreased dramatically after Pd infection in both female M. lucifugus and E. fuscus. Increases in hepatic glycerophospholipid (structural lipid) levels were only observed in M. lucifugus, including two phosphatidylcholines (PC [32:1], PC [42:6]) and one phosphatidylglycerol (PG [34:1]). These results suggest that even at early stages of WNS, changes in hepatic lipid mobilization may occur and be species and sex specific. As pre-hibernation lipid reserves may aid in bat persistence and survival during WNS, these early perturbations to lipid metabolism could have important implications for management responses that aid in pre-hibernation fat storage.

scholarly journals Field trial of a probiotic bacteria and a chemical, chitosan, to protect bats from white-nose syndrome

2019 ◽  
Author(s):  
Joseph R. Hoyt ◽  
Kate E. Langwig ◽  
J. Paul White ◽  
Heather M. Kaarakka ◽  
Jennifer A. Redell ◽  
...  
Keyword(s):  
Field Trial ◽  
Infection Intensity ◽  
Probiotic Bacterium ◽  
Myotis Lucifugus ◽  
Probiotic Bacteria ◽  
Control Group ◽  
Pseudogymnoascus Destructans ◽  
Overwinter Survival ◽  
Cage Experiment ◽  
White Nose Syndrome

AbstractTools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungusPseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of two treatments, a probiotic bacterium,Pseudomonas fluorescens, and a chemical, chitosan, to reduce impacts of WNS in two simultaneous experiments conducted with caged and free-flyingMyotis lucifugusbats at a mine in Wisconsin, USA. In the free-flying experiment, treatment withP. fluorescensincreased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by 30 days. Apparent overwinter survival for free-flying chitosan-treated bats was 18.0%, which did not differ significantly from control bats. In the cage experiment, chitosan-treated bats had significantly higher survival until release on March 8 (53%) than control andP. fluorescens-treated bats (both 27%). However, these differences were likely due to within-cage disturbance and not reduced WNS impacts, because chitosan-treated bats actually had significantly higher UV-fluorescence (a measure of disease severity), and body mass, not infection intensity, predicted mortality. Further, few of the bats released from the cage experiment were detected emerging from the mine, indicating that the survival estimates at the time of release did not carryover to overwinter survival. These results suggest that treatment of bats may reduce WNS mortality, but additional measures are needed to prevent declines.

scholarly journals Impacts of White-Nose Syndrome Observed During Long-Term Monitoring of a Midwestern Bat Community

2017 ◽  
Vol 8 (1) ◽  
pp. 69-78 ◽  
Author(s):  
Joseph L. Pettit ◽  
Joy M. O'Keefe
Keyword(s):  
Reproductive Success ◽  
Common Species ◽  
Myotis Lucifugus ◽  
Lasiurus Borealis ◽  
Indiana Bat ◽  
White Nose Syndrome ◽  
Long Term Monitoring ◽  
Species Specific ◽  
Term Monitoring

Abstract White-nose syndrome (WNS) is an emerging fungal disease suspected to have infected Indiana caves in the winter of 2010–2011. This disease places energetic strains on cave-hibernating bats by forcing them to wake and use energy reserves. It has caused >5.5 million bat deaths across eastern North America, and may be the driving force for extinction of certain bat species. White-nose syndrome infection can be identified in hibernacula, but it may be difficult to determine whether bats in a particular area are affected if no known hibernacula exist. Thus, our aim was to use long-term monitoring data to examine changes in a summer population away from hibernacula that may be attributable to WNS effects during winter. We used capture data from a long-term bat-monitoring project in central Indiana with data from 10 repeatedly netted sites consistent across all reproductive periods. We modeled capture data by WNS exposure probability to assess changes in relative abundance of common species and reproductive classes as WNS exposure probability increases. We base exposure probability on a cokriging spatial model that interpolated WNS infection from hibernaculum survey data. The little brown bat Myotis lucifugus, the Indiana bat M. sodalis, and the tri-colored bat Perimyotis subflavus suffered 12.5–79.6% declines; whereas, the big brown bat Eptesicus fuscus, the eastern red bat Lasiurus borealis, and the evening bat Nycticeius humeralis showed 11.5–50.5% increases. We caught more nonreproductive adult females and postlactating females when WNS exposure probabilities were high, suggesting that WNS is influencing reproductive success of affected species. We conclude that, in Indiana, WNS is causing species-specific declines and may have caused the local extinction of M. lucifugus. Furthermore, WNS-affected species appear to be losing pups or forgoing pregnancy. Ongoing long-term monitoring studies, especially those focusing on reproductive success, are needed to measure the ultimate impacts of WNS.

scholarly journals Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis ( Myotis lucifugus )

2015 ◽  
Vol 2 (2) ◽  
pp. 140470 ◽  
Author(s):  
Laura E. Grieneisen ◽  
Sarah A. Brownlee-Bouboulis ◽  
Joseph S. Johnson ◽  
DeeAnn M. Reeder
Keyword(s):  
Infectious Disease ◽  
Myotis Lucifugus ◽  
Eastern North America ◽  
The Novel ◽  
Pseudogymnoascus Destructans ◽  
Term Survival ◽  
White Nose Syndrome ◽  
Myotis Myotis ◽  
The Impact

White-nose syndrome (WNS), an emerging infectious disease caused by the novel fungus Pseudogymnoascus destructans , has devastated North American bat populations since its discovery in 2006. The little brown myotis, Myotis lucifugus , has been especially affected. The goal of this 2-year captive study was to determine the impact of hibernacula temperature and sex on WNS survivorship in little brown myotis that displayed visible fungal infection when collected from affected hibernacula. In study 1, we found that WNS-affected male bats had increased survival over females and that bats housed at a colder temperature survived longer than those housed at warmer temperatures. In study 2, we found that WNS-affected bats housed at a colder temperature fared worse than unaffected bats. Our results demonstrate that WNS mortality varies among individuals, and that colder hibernacula are more favourable for survival. They also suggest that female bats may be more negatively affected by WNS than male bats, which has important implications for the long-term survival of the little brown myotis in eastern North America.

scholarly journals Temporal Changes in Body Mass and Body Condition of Cave-Hibernating Bats During Staging and Swarming

2015 ◽  
Vol 6 (2) ◽  
pp. 360-370 ◽  
Author(s):  
Michael J. Lacki ◽  
Luke E. Dodd ◽  
Rickard S. Toomey ◽  
Steven C. Thomas ◽  
Zachary L. Couch ◽  
...  
Keyword(s):  
Body Mass Index ◽  
Body Mass ◽  
Body Condition ◽  
Leading Edge ◽  
Myotis Lucifugus ◽  
Pseudogymnoascus Destructans ◽  
White Nose Syndrome ◽  
Close Proximity ◽  
Fungal Distribution ◽  
Little Brown Bats

Abstract The rapid colonization of the Pseudogymnoascus destructans fungus across cave systems in eastern North America and the associated bat mortalities (white-nose syndrome; WNS), necessitates studies of cave-hibernating bats that remain unaffected by, or in close proximity to, the leading edge of the fungal distribution to provide baseline predisturbance data from which to assess changes due to fungal effects. Studies of the physiological ecology of cave-hibernating bats during the spring staging and autumn swarming seasons are few, and an understanding of patterns in body condition of bats associated with entry into and emergence from hibernation is incomplete. We sampled bats at the entrance to a cave in Mammoth Cave National Park, Kentucky, during swarming and staging, prior to (2011 and 2012), concurrent with (2013), and following (2014) the arrival of the WNS fungus. We evaluated seasonal and annual changes in body mass and body condition of bats entering and leaving the cave. We captured 1,232 bats of eight species. Sex ratios of all species were male-biased. Capture success was substantially reduced in 2014, following the second winter after arrival of the WNS fungus. Significant temporal variation in body mass and body mass index was observed for little brown bats Myotis lucifugus, northern long-eared bats M. septentrionalis, and tri-colored bats Perimyotis subflavus, but not Indiana bats M. sodalis. Little brown bats and northern long-eared bats demonstrated significant increases in mean body mass index in 2014; this pattern likely reflected a relatively better body condition in bats that survived exposure to the WNS fungus. Most species demonstrated highest body mass and body mass index values in late swarming compared with other sampling periods, with tri-colored bats showing the greatest percent increase in body mass (42.5%) and body mass index (42.9%) prior to entering hibernation. These data indicate significant intraspecific variation in body condition of cave-hibernating bat species, both among years and between the seasons of autumn swarming and spring staging. We suggest this variation is likely to have implications for the relative vulnerability of species to WNS infection across the distribution of the Pseudogymnoascus fungus.

scholarly journals A Culture-Based ID of Micromycetes on the Wing Membranes of Greater Mouse-Eared Bats (Myotis myotis) from the “Nietoperek” Site (Poland)

Animals ◽  
2020 ◽  
Vol 10 (8) ◽  
pp. 1337 ◽  
Author(s):  
Rafał Ogórek ◽  
Klaudia Kurczaba ◽  
Magdalena Cal ◽  
Grzegorz Apoznański ◽  
Tomasz Kokurewicz
Keyword(s):  
Habitat Preferences ◽  
Physiological Saline ◽  
Fungal Species ◽  
Early Spring ◽  
The European Union ◽  
Pseudogymnoascus Destructans ◽  
Pathogenic Potential ◽  
White Nose Syndrome ◽  
Myotis Myotis ◽  
Spring Emergence

Bats play important functions in ecosystems and many of them are threatened with extinction. Thus, the monitoring of the health status and prevention of diseases seem to be important aspects of welfare and conservation of these mammals. The main goal of the study was the identification of culturable fungal species colonizing the wing membranes of female greater mouse-eared bat (Myotis myotis) during spring emergence from the “Nietoperek” underground hibernation site by the use of genetic and phenotypic analyses. The study site is situated in Western Poland (52°25′ N, 15°32′ E) and is ranked within the top 10 largest hibernation sites in the European Union. The number of hibernating bats in the winter exceeds 39,000 individuals of 12 species, with M. myotis being the most common one. The wing membranes of M. myotis were sampled using sterile swabs wetted in physiological saline (0.85% NaCl). Potato dextrose agar (PDA) plates were incubated in the dark at 8, 24 and 36 ± 1 °C for 3 up to 42 days. All fungi isolated from the surface of wing membranes were assigned to 17 distinct fungal isolates belonging to 17 fungal species. Penicillium chrysogenum was the most frequently isolated species. Some of these fungal species might have a pathogenic potential for bats and other mammals. However, taking into account habitat preferences and the life cycle of bats, it can be assumed that some fungi were accidentally obtained from the surface of vegetation during early spring activity. Moreover, Pseudogymnoascus destructans (Pd)—the causative agent of the White Nose Syndrome (WNS)—was not found during testing, despite it was found very often in M. myotis during previous studies in this same location.

scholarly journals Observed Resiliency of Little Brown Myotis to Long-Term White-Nose Syndrome Exposure

2018 ◽  
Vol 9 (1) ◽  
pp. 168-179 ◽  
Author(s):  
Christopher A. Dobony ◽  
Joshua B. Johnson
Keyword(s):  
Survival Rates ◽  
Reproductive Potential ◽  
Myotis Lucifugus ◽  
Recent Past ◽  
Pseudogymnoascus Destructans ◽  
Recent Infection ◽  
Term Survival ◽  
Annual Survival ◽  
White Nose Syndrome

Abstract White-nose syndrome (WNS) is a disease that has killed millions of bats in eastern North America and has steadily been spreading across the continent. Little brown myotis Myotis lucifugus populations have experienced extensive declines; however, some localized populations have remained resilient, with bats surviving multiple years past initial WNS exposure. These persistent populations may be critical to species recovery, and understanding mechanisms leading to this long-term survival and persistence may provide insight into overall bat and disease management. We monitored a maternity colony of little brown myotis on Fort Drum Military Installation in northern New York between 2006 and 2017 to determine basic demographic parameters and find evidence of what may be leading to resiliency and persistence at this site. Total colony size declined by approximately 88% from 2008 to 2010 due primarily to impacts of WNS. Counts of all adults returning to the colony stabilized during 2010–2014 (mean = 94, range 84–101) and increased after 2014 (mean = 132, range = 108–166). We captured 727 little brown myotis (575 females, 152 males) and banded 534 individuals (389 females, 145 males) at the colony. The majority of sampled bats showed evidence of recent past WNS infection and exposure to Pseudogymnoascus destructans, and we documented pervasive presence and limited viability of the fungus within the colony's main roosting structure. We recaptured 98 individually marked females in years after initial banding, and some individuals survived at least 6 y. Ninety-one percent of all adult females, 93% of recaptured bats, and 90% of 1-y-old females (i.e., bats recaptured the first year after initial capture as juveniles) showed evidence of reproduction during the monitoring period. Using mark–recapture models, we estimated annual survival rates of juvenile and adult little brown myotis during 2009–2016 and examined whether reproductive condition or evidence of recent infection of WNS had any effect on survival. Annual survival rates were similar between juveniles and adults, but highly variable, ranging from 41.0 to 86.5%. Models indicated that neither evidence of recent past exposure to WNS nor reproductive status were related to survival. No one parameter stood out as being responsible for this colony's continued existence, and it is likely that many interwoven factors were responsible for the observed resilience. Although relatively high reproductive effort from all females (i.e., both1-y-old and >1-y-old ) and intermittently suitable survival rates have led to the continued persistence of, and population increases in, this summer colony, mortality from WNS and inherently low reproductive potential still seemed to be limiting population growth. Until there is a better understanding of this overall potential resiliency in little brown myotis, we recommend considering minimizing disturbance and direct human involvement within these persisting populations to allow whatever natural recovery that may be occurring to evolve uninterrupted.

scholarly journals The evolution of a bat population with white-nose syndrome (WNS) reveals a shift from an epizootic to an enzootic phase

2019 ◽  
Vol 16 (1) ◽  
Author(s):  
Craig L. Frank ◽  
April D. Davis ◽  
Carl Herzog
Keyword(s):  
Mortality Rate ◽  
Mortality Rates ◽  
Myotis Lucifugus ◽  
Winter Mortality ◽  
Long Term Effects ◽  
Pseudogymnoascus Destructans ◽  
Torpor Bout ◽  
Bout Duration ◽  
White Nose Syndrome ◽  
Fat Reserves

Abstract Background White-nose Syndrome (WNS) is a mycosis caused by a cutaneous infection with the fungus Pseudogymnoascus destructans (Pd). It produces hibernation mortality rates of 75–98% in 4 bats: Myotis lucifugus, M. septentrionalis, M. sodalis, and Perimyotis subflavus. These high mortality rates were observed during the first several years after the arrival of P. destructans at a hibernation site. Mortality is caused by a 60% decrease in torpor bout duration, which results in a premature depletion of depot fat prior to spring. Results Little is known about the long-term effects of Pd on torpor and mortality, thus we conducted a 9-year study on M. lucifugus at 5 of the hibernation sites where Pd first appeared in North America during the winter of 2007–08. The M. lucifugus hibernating at one of these sites one year after the arrival of Pd (2008–09) had: a) a mean torpor bout duration of 7.6 d, b) no depot fat reserves by March, and c) an apparent over-winter mortality rate of 88%. The M. lucifugus hibernating at this same site 6–9 years after the arrival of Pd, in contrast, had: a) a mean torpor bout duration of 14.7 d, b) depot fat remaining in March, and c) an apparent mortality rate of 50%. The number of M. lucifugus hibernating at 2 of these sites has consistently increased since 2010 and is now more than 3.0-fold higher than the number remaining after the winter of 2008–09. Conclusions These findings indicate that this population of M. lucifugus has evolved mechanisms to hibernate well in the presence of Pd, thus reducing over-winter mortality.

scholarly journals Immune responses in hibernating little brown myotis ( Myotis lucifugus ) with white-nose syndrome

2017 ◽  
Vol 284 (1848) ◽  
pp. 20162232 ◽  
Author(s):  
T. M. Lilley ◽  
J. M. Prokkola ◽  
J. S. Johnson ◽  
E. J. Rogers ◽  
S. Gronsky ◽  
...  
Keyword(s):  
Gene Expression ◽  
Immune Response ◽  
Immune Responses ◽  
Lymph Nodes ◽  
Myotis Lucifugus ◽  
Pseudogymnoascus Destructans ◽  
Winter Habitat ◽  
Th17 Response ◽  
White Nose Syndrome ◽  
Psychrophilic Fungus

White-nose syndrome (WNS) is a fungal disease responsible for decimating many bat populations in North America. Pseudogymnoascus destructans ( Pd ), the psychrophilic fungus responsible for WNS, prospers in the winter habitat of many hibernating bat species. The immune response that Pd elicits in bats is not yet fully understood; antibodies are produced in response to infection by Pd , but they may not be protective and indeed may be harmful. To understand how bats respond to infection during hibernation, we studied the effect of Pd inoculation on the survival and gene expression of captive hibernating Myotis lucifugus with varying pre-hibernation antifungal antibody titres. We investigated gene expression through the transcription of selected cytokine genes ( Il6 , Il17a , Il1b , Il4 and Ifng ) associated with inflammatory, Th1, Th2 and Th17 immune responses in wing tissue and lymph nodes. We found no difference in survival between bats with low and high anti- Pd titres, although anti- Pd antibody production during hibernation differed significantly between infected and uninfected bats. Transcription of Il6 and Il17a was higher in the lymph nodes of infected bats compared with uninfected bats. Increased transcription of these cytokines in the lymph node suggests that a pro-inflammatory immune response to WNS is not restricted to infected tissues and occurs during hibernation. The resulting Th17 response may be protective in euthermic bats, but because it may disrupt torpor, it could be detrimental during hibernation.

scholarly journals Resistance in persisting bat populations after white-nose syndrome invasion

2017 ◽  
Vol 372 (1712) ◽  
pp. 20160044 ◽  
Author(s):  
Kate E. Langwig ◽  
Joseph R. Hoyt ◽  
Katy L. Parise ◽  
Winifred F. Frick ◽  
Jeffrey T. Foster ◽  
...  
Keyword(s):  
Growth Rate ◽  
Fungal Pathogen ◽  
Infection Intensity ◽  
Myotis Lucifugus ◽  
Pseudogymnoascus Destructans ◽  
White Nose Syndrome ◽  
The Face ◽  
Declining Populations ◽  
Little Brown Bat ◽  
Declining Species

Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat ( Myotis lucifugus ) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans , which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting populations than in declining populations where the fungus has recently invaded. Fitted models indicate that this is most consistent with a reduction in the growth rate of the pathogen when fungal loads become high. The data are inconsistent with the evolution of tolerance or an overall reduced pathogen growth rate that might be caused by environmental factors. The existence of resistance in some persisting populations of little brown bats offers a glimmer of hope that a precipitously declining species will persist in the face of this deadly pathogen. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

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