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

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.

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

“…In healthy individuals, torpor bouts typically last 12-15 d (Reeder et al 2012;Brownlee-Bouboulis and Reeder 2013), and bouts are separated by brief arousal periods that serve various physiologic purposes (Geiser 2004;Moore et al 2011;Jonasson and Willis 2012). Extensive torpor bouts may facilitate the growth of P. destructans on bats, ultimately causing lesions that disrupt torpor resulting in the premature depletion of energy reserves (Warnecke et al 2012).…”

Electrolyte Depletion in White-nose Syndrome Bats

“…We used a histology scoring system published elsewhere (Reeder et al, 2012) to classify WNS-associated wing damage. Briefly, this scoring system is based on the histopathology determination of severity of fungal erosion and ulceration combined with the extent to which lesions were distributed over the surface area of wing skin on a scale of 0 (no lesions associated with WNS) to 4 (severe damage to wing membrane).…”

“…Dehydration resulting from fungal damage to skin is hypothesized to cause WNS bats to drink more during winter (Cryan et al, 2010;Willis et al, 2011), and possibly cause the more frequent arousals from hibernation associated with WNS mortality (Reeder et al, 2012;Warnecke et al, 2012). Although bats regularly arouse from hibernation to drink, water available in hibernacula may not contain sufficient electrolytes to offset winter losses.…”

Interruption to cutaneous gas exchange is not a likely mechanism of WNS-associated death in bats

“…The causative agent is a fungus, Pseudogymnoascus destructans (Pd) (Lorch et al, 2011;Warnecke et al, 2012), but we do not know how an infection with Pd leads to mortality in hibernating bats. Researchers have formulated several hypotheses, with most including either dehydration or starvation as a proposed proximal cause of death (Boyles and Willis, 2010;Cryan et al, 2010;Reeder et al, 2012).…”