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


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American Journal of Physiology- Regulatory, Integrative and Comparative Physiology

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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 Pseudogymnoascus destructans 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 1) higher metabolic rates during torpor (TMR) and 2) higher rates of evaporative water loss (EWL). We collected bats from a WNS-negative hibernaculum, inoculated one group with P. destructans, 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. fungal diseases of wildlife are on the rise worldwide (13). In contrast to viral and bacterial pathogens, which often lead to systemic infections, fungal pathogens of animals often manifest as superficial skin infections, especially among poikilothermic species. Although typically limited to infecting skin, fungal pathogens can lead to devastating physiological impacts and fatal disease across a range of taxa (1, 4, 5, 35, 36). A mechanistic understanding of pathogenesis in fungal diseases of wildlife is critical for understanding and predicting population-level impacts and developing safe and effective mitigation and management strategies. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, is a recently emerged disease of hibernating bats (5) (25, 42). Since its discovery in 2007, millions of bats have been killed in eastern and central North America, leading to dramatic population declines (16) and the possibility of regional extinctions (15). Recent reviews have summarized our understanding of disease mechanisms in WNS (17, 45). A number of putative virulence factors have now been identified (14, 29), and studies of both captive (42) and free-living (33) bats indicate that the disease causes increased frequency of arousals from torpor during hibernation, emaciation, and death. Infected bats also exhibit signs of altered fluid, electrolyte, and pH balance (10, 11, 26, 41, 43), leading to development of two complementary mechanistic models of WNS pathophysiology (41, 43). Symptoms of WNS develop in a progressive manner (26), and the most pronounced symptoms are only apparent relatively late in hibernation (41, 43). Increased arousal frequency and arousal cascades that may reflect conspecific disturbances (40) in later stages of infection lead to dramatic increases in energy expenditure and are thought to be a primary cause of emaciation (43). This pattern is described in a pathophysiological model proposed by Warnecke et al. (43). The model proposes that lesions in wing tissue, which occur in later stages of fungal infection, lead to altered blood chemistry and hematology and increased water loss, respiratory rate, and energy consumption. More recently, however, Verant et al. (41) found evidence of increased energy turnover at an earlier stage of disease, before a detectable increase in arousal frequency was observed. They proposed a model of earlier-stage disease based on these findings. Their model suggests that increased metabolic rate following initial tissue invasion, combined with reduced excretion of CO2, initiates the cascade of physiological responses observed by Warnecke et al. (15) in the final stages of WNS (16). Two key elements of both models are increased energy expenditure and disruption of osmotic homeostasis (41, 43). Although the cause of increased arousal frequency is unknown, observations of electrolyte and fluid depletion (10) led to the dehydration hypothesis (11, 46) that fluid loss across fungal lesions on the skin increases rates of water loss, resulting in increased arousal frequency and energy depletion. In healthy hibernators, ambient humidity and evaporative water loss (EWL) affect torpor bout duration (3, 38), which suggests that increased EWL due to wing damage could trigger increased arousal frequency and mortality in WNS (46). Thus, understanding the impacts of WNS on energy expenditure and water loss, as predicted by both pathophysiological models of WNS published to date, is a critical step in understanding the mechanism by which fungal infection leads to bat mortality. We conducted an experimental inoculation to test the hypothesis that WNS causes increased energy expenditure and EWL during torpor bouts, as predicted by mechanistic models of WNS (41, 43). Specifically, we predicted that bats inoculated with P. destructans would have 1) higher torpid metabolic rate (TMR) and 2) increased EWL compared with healthy controls. We also measured TMR and EWL in both dry and humidified air to assess the impact of environmental conditions on WNS pathophysiology.

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