White-nose syndrome increases torpid metabolic rate and evaporative water loss in hibernating bats

Abstract

Fungal diseases of wildlife typically manifest as superficial skin infections but can have devastating consequences for host physiology and survival. White-nose syndrome (WNS) is a fungal skin disease that has killed millions of hibernating bats in North America since 2007. Infection with the fungus causes bats to rewarm too often during hibernation, but the cause of increased arousal rates remains unknown. On the basis of data from studies of captive and free-living bats, two mechanistic models have been proposed to explain disease processes in WNS. Key predictions of both models are that WNS-affected bats will show) higher metabolic rates during torpor (TMR) and ) higher rates of evaporative water loss (EWL). We collected bats from a WNS-negative hibernaculum, inoculated one group with, and sham-inoculated a second group as controls. After 4 mo of hibernation, TMR and EWL were measured using respirometry. Both predictions were supported, and our data suggest that infected bats were more affected by variation in ambient humidity than controls. Furthermore, disease severity, as indicated by the area of the wing with UV fluorescence, was positively correlated with EWL, but not TMR. Our results provide the first direct evidence that heightened energy expenditure during torpor and higher EWL independently contribute to WNS pathophysiology, with implications for the design of potential treatments for the disease.

An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter‐active snake

“…The effects of Oo infection on metabolism and EWL in S. miliarius mirror those induced by the cutaneous fungal pathogen Pseudogymnoascus destructans ( Pd ), the causative agent of white‐nose syndrome in hibernating bats (Lorch et al, ). Bats with clinical Pd infections exhibit elevated rates of metabolism and EWL during torpor (McGuire et al, ). Resultant dehydration may stimulate energetically costly arousal episodes, eventually leading to fat depletion and mortality (McGuire et al, ; Verant et al, ; Warnecke et al, ).…”

“…Bats with clinical Pd infections exhibit elevated rates of metabolism and EWL during torpor (McGuire et al, ). Resultant dehydration may stimulate energetically costly arousal episodes, eventually leading to fat depletion and mortality (McGuire et al, ; Verant et al, ; Warnecke et al, ). Emaciation and/or dehydration associated with Oo effects on host physiology may likewise be a cause of mortality in snakes with SFD, though a direct connection remains to be established.…”

“…Mycotic skin infections may also carry hydric consequences for the host via their effects on cutaneous water exchange (McGuire et al, ; Russo et al, ). We documented an increase in total EWL in SFD‐positive snakes, which may be attributable to increases in cutaneous and/or respiratory water loss rates.…”

“…Perhaps less appreciated are the sublethal effects of fungal infection. Given that these fungal pathogens preferentially invade the skin of their host, the physiological consequences of infection may extend beyond energetic costs of immune system activation to disturbances in water and ion balance (Cryan et al, ; McGuire, Mayberry, & Willis, ; Peterson et al, ; Russo, Ohmer, Cramp, & Franklin, ; Verant et al, ; Voyles et al, ). Thus, the physiological costs and resultant life‐history trade‐offs imposed by certain fungal diseases may be more pronounced than those observed for other pathogens.…”

Genome-Wide Changes in Genetic Diversity in a Population of Myotis lucifugus Affected by White-Nose Syndrome

“…Susceptible species, such as Myotis lucifugus and M. septentrionalis, have shown population declines greater than 90% in affected hibernacula (Frick et al 2015). The infection disrupts hibernation behavior of susceptible species and leads to more frequent arousals from torpor, evaporative water loss, premature energy depletion, and death of susceptible individuals due to emaciation (Willis et al 2011;Reeder et al 2012;Warnecke et al 2013;Verant et al 2014;McGuire et al 2017). Naïve infected M. lucifugus upregulate genes involved in immune pathways during the hibernation period (Field et al 2015(Field et al , 2018Lilley et al 2017).…”