Frequent Arousal from Hibernation Linked to Severity of Infection and Mortality in Bats with White-Nose Syndrome

Deeann M Reeder,Megan E Vodzak,Carol U Meteyer,Craig W Stihler,David S Blehert,Laura E Grieneisen,Gregory G Turner,Craig L Frank,Laura K Muller,Alan C Hicks,Scott R Darling,Roymon Jacob,Sarah A Brownlee,Allen Kurta,Eric R Britzke

doi:10.1371/journal.pone.0038920

Abstract

White-nose syndrome (WNS), an emerging infectious disease that has killed over 5.5 million hibernating bats, is named for the causative agent, a white fungus (Geomyces destructans (Gd)) that invades the skin of torpid bats. During hibernation, arousals to warm (euthermic) body temperatures are normal but deplete fat stores. Temperature-sensitive dataloggers were attached to the backs of 504 free-ranging little brown bats (Myotis lucifugus) in hibernacula located throughout the northeastern USA. Dataloggers were retrieved at the end of the hibernation season and complete profiles of skin temperature data were available from 83 bats, which were categorized as: (1) unaffected, (2) WNS-affected but alive at time of datalogger removal, or (3) WNS-affected but found dead at time of datalogger removal. Histological confirmation of WNS severity (as indexed by degree of fungal infection) as well as confirmation of presence/absence of DNA from Gd by PCR was determined for 26 animals. We demonstrated that WNS-affected bats aroused to euthermic body temperatures more frequently than unaffected bats, likely contributing to subsequent mortality. Within the subset of WNS-affected bats that were found dead at the time of datalogger removal, the number of arousal bouts since datalogger attachment significantly predicted date of death. Additionally, the severity of cutaneous Gd infection correlated with the number of arousal episodes from torpor during hibernation. Thus, increased frequency of arousal from torpor likely contributes to WNS-associated mortality, but the question of how Gd infection induces increased arousals remains unanswered.

Highlights

White-nose syndrome (WNS) is estimated to be responsible for the deaths of at least 5.7 to 6.7 million hibernating bats in the eastern United States and Canada [1,2]
A white fungus identified as Geomyces destructans (Gd) grows on the muzzle, wings, and ears of bats suffering from WNS starting in late January/early February [3,5,6]
WNS Status and TBL female bats were in significantly greater body condition than males at the start of hibernation (BMI: 0.228460.0283 g/mm (N = 32) vs. 0.207360.0210 g/mm (N = 51); t = 23.633, adjusted df = 52.2, p = 0.001), there were no detectable influences of sex on TBL (F(1,76) = 0.031, p = 0.861; partial eta squared = 0.000, power = 0.053)

Summary

Introduction

White-nose syndrome (WNS) is estimated to be responsible for the deaths of at least 5.7 to 6.7 million hibernating bats in the eastern United States and Canada [1,2]. WNS affects at least six (and possibly nine) species of hibernating insectivorous bats [2], including some classified as endangered or threatened. The little brown bat (or, little brown myotis, Myotis lucifugus), which was once the most common hibernating bat in the American Northeast (NE), has incurred an average of 91% mortality in sites that have been affected for at least two years [2] and mathematical models indicate that this species may go extinct in the NE within 16 years [4]. Recent laboratory experiments have demonstrated that cutaneous infection with this fungus is the cause of WNS, but it is not fully understood how such an infection produces mortality during hibernation [7]. It is hypothesized that infection by Gd disrupts normal physiological functions, such as water balance [8] or other aspects of hibernation physiology, including use of torpor [9]

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