The scope and severity of white‐nose syndrome on hibernating bats in North America

Cheng, Tina L.; Reichard, Jonathan D.; Coleman, Jeremy T. H.; Weller, Theodore J.; Thogmartin, Wayne E.; Reichert, Brian E.; Bennett, Alyssa; Broders, Hugh G.; Campbell, Joshua R.; Etchison, Katherine; Feller, Daniel; Geboy, Richard; Hemberger, Traci A.; Herzog, Carl; Hicks, Alan C.; Houghton, Sandra; Humber, Jessica M.; Kath, Joseph A.; King, Richard; Loeb, Susan C.; Massé, Ariane; Morris, Katrina M.; Niederriter, Holly; Nordquist, Gerda; Perry, Roger W.; Reynolds, Richard J.; Sasse, D.; Scafini, Michael R.; Stark, Richard; Stihler, Craig W.; Thomas, Steven C.; Turner, Gregory G.; Webb, Shevenell M.; Westrich, Bradford J.; Frick, Winifred F.

doi:10.1111/cobi.13739

Cited by 157 publications

(150 citation statements)

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“…Our data show that E. fuscus has the most acidic skin ( Fig. 3 ), and this species is also more tolerant of WNS than the other bat species we measured ( Cheng et al , 2021 ). Although P. destructans can grow in vitro from 4.5–11 pH ( Raudabaugh and Miller, 2013 ; Vanderwolf et al , 2021 ), a carboxypeptidase enzyme produced by P. destructans was most active at 3–5 pH compared to 6.5–8.5 pH in vitro ( Beekman et al , 2018 ).…”

Section: Discussionsupporting

confidence: 48%

Skin pH varies among bat species and seasons and between wild and captive bats

Vanderwolf

Kyle

Faure

et al. 2021

Conservation Physiology

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Skin is a key aspect of the immune system in the defence against pathogens. Skin pH regulates the activity of enzymes produced both by hosts and by microbes on host skin, thus implicating pH in disease susceptibility. Skin pH varies inter- and intra-specifically and is influenced by a variety of intrinsic and extrinsic variables. Increased skin alkalinity is associated with a predisposition to cutaneous infections in humans and dogs, and inter-specific and inter-individual variation in skin pH is implicated in differential susceptibility to some skin diseases. The cutaneous pH of bats has not been characterized but is postulated to play a role in susceptibility to white-nose syndrome (WNS), a fungal infection that has decimated several Nearctic bat species. We used non-invasive probes to measure the pH of bat flight membranes in five species with differing susceptibility to WNS. Skin pH ranged from 4.67 to 8.59 and varied among bat species, geographic locations, body parts, age classes, sexes and seasons. Wild Eptesicus fuscus were consistently more acidic than wild Myotis lucifugus, Myotis leibii and Perimyotis subflavus. Juvenile bats had more acidic skin than adults during maternity season but did not differ during swarming. Male M. lucifugus were more acidic than females during maternity season, yet this trend reversed during swarming. Bat skin was more acidic in summer compared to winter, a pattern also reported in humans. Skin pH was more acidic in captive than wild E. fuscus, suggesting environmental impacts on skin pH. The pH of roosting substrates affects skin pH in captive bats and may partially explain seasonal patterns in wild bats that use different roost types across seasons. Future research on the influence of pH on microbial pathogenic factors and skin barrier function may provide valuable insights on new therapeutic targets for treating bat skin conditions.

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Section: Discussionsupporting

confidence: 48%

Skin pH varies among bat species and seasons and between wild and captive bats

Vanderwolf

Kyle

Faure

et al. 2021

Conservation Physiology

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“…White-nose Syndrome (WNS) is an infectious disease of hibernating bats caused by a fungal pathogen ( Pseudogymnoascus destructans ; Pd ) 6 – 9 that was first detected in eastern North America in 2006 10 and has caused rapid and extreme population declines of several species of hibernating bats 11 – 14 . Over the past 15 years, extensive research has revealed much about the disease ecology of WNS, including the interactions between the pathogen, environments where bats hibernate, and the physiology of hibernating bats (see 12 for recent comprehensive review).…”

Section: Introductionmentioning

confidence: 99%

“…One of the challenging aspects of managing WNS is that the pathogen persists in the environment where bats hibernate, exposing bats to infection at the start of each hibernation season 19 , 20 . Understanding the specific conditions that affect disease severity and population declines where the pathogen invades and establishes 12 , 19 , 21 , 22 remains important for informing management response 4 , 11 .…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Perimyotis subflavus has experienced an overall 93% population decline across the range of where WNS has established and the species is currently being evaluated for regulatory protection under the Endangered Species Act 11 . Although the effects of WNS on this species have been well-documented in numerous field studies 11 , 12 , 14 , 21 , 23 , no experimental studies had yet been conducted to examine the species’ hibernation physiology and disease susceptibility. Most experimental infection trials on WNS have been conducted with little brown bats ( Myotis lucifugus ) 8 , 9 , 15 , 30 – 33 and there is a recognized need to study the interactions among host, pathogen, and environmental conditions in other bat species whose populations are declining from WNS 12 .…”

Section: Introductionmentioning

confidence: 99%

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Experimental inoculation trial to determine the effects of temperature and humidity on White-nose Syndrome in hibernating bats

Frick

Johnson

Cheng

et al. 2022

Sci Rep

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Disease results from interactions among the host, pathogen, and environment. Inoculation trials can quantify interactions among these players and explain aspects of disease ecology to inform management in variable and dynamic natural environments. White-nose Syndrome, a disease caused by the fungal pathogen, Pseudogymnoascus destructans (Pd), has caused severe population declines of several bat species in North America. We conducted the first experimental infection trial on the tri-colored bat, Perimyotis subflavus, to test the effect of temperature and humidity on disease severity. We also tested the effects of temperature and humidity on fungal growth and persistence on substrates. Unexpectedly, only 37% (35/95) of bats experimentally inoculated with Pd at the start of the experiment showed any infection response or disease symptoms after 83 days of captive hibernation. There was no evidence that temperature or humidity influenced infection response. Temperature had a strong effect on fungal growth on media plates, but the influence of humidity was more variable and uncertain. Designing laboratory studies to maximize research outcomes would be beneficial given the high costs of such efforts and potential for unexpected outcomes. Understanding the influence of microclimates on host–pathogen interactions remains an important consideration for managing wildlife diseases, particularly in variable environments.

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Bats increased foraging activity at experimental prey patches near hibernacula

Frick

Dzal

Jonasson

et al. 2023

Ecol Sol and Evidence

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Emerging infectious diseases in wildlife can threaten vulnerable host populations. Actions targeting habitat improvements to aid population resilience and recovery may be beneficial long‐term strategies, yet testing the efficacy of such strategies before major conservation investments are made can be challenging. The disease white‐nose syndrome (WNS) has caused severe declines in several species of North American hibernating bats. We tested a novel conservation approach targeted at improving foraging conditions near bat hibernacula by experimentally manipulating insect density in the pre‐hibernation fattening period and spring emergence recovery period. We measured foraging (feeding buzzes) and echolocation activity of little brown bats Myotis lucifugus at ultraviolet (UV) light lures to determine behavioural response to augmented foraging conditions and characterized insect availability at UV light lures. In the fall, bat foraging activity was three times greater (95% CI: 1.5–5.8; p = 0.002) when UV lights were on, but there was no statistical support for differences in echolocation activity response when our experimental design alternated between nights with lights on and off. In the spring, we allowed UV light lures to run consistently each night and compared with a control location in similar habitat. Bat foraging activity was 8.5 times greater (95% CI: 4.5–16.0; p < 0.0001) and echolocation activity was 4.4 times higher (95% CI: 3.0–6.5; p < 0.0001) at UV light lures in the spring experiment. In both the fall and spring, UV light lures resulted in concentrated insect availability, attracting primarily moths (Order: Lepidoptera). In both seasons, nightly temperature had a strong influence on bat foraging, echolocation and insect activity. We show that a bat species threatened by WNS used enhanced foraging habitats near hibernacula during the critical pre‐ and post‐hibernation phases of their annual cycle. While light lures are unlikely to be a long‐term management strategy, our experiment provides initial evidence that bats behaviourally respond with increased foraging activity in areas with augmented insect prey availability. Our experimental results support developing management strategies focused on habitat protection, including restoration and enhancement of foraging habitats, in the immediate vicinity of bat hibernacula.

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The scope and severity of white‐nose syndrome on hibernating bats in North America

Abstract: Article impact statement: Data sharing and coordinated monitoring are needed to assess species' response to threats to inform conservation planning at relevant scales.

Cited by 157 publications

References 30 publications

Skin pH varies among bat species and seasons and between wild and captive bats

Skin pH varies among bat species and seasons and between wild and captive bats

Experimental inoculation trial to determine the effects of temperature and humidity on White-nose Syndrome in hibernating bats

Bats increased foraging activity at experimental prey patches near hibernacula

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