Incorporating evaporative water loss into bioenergetic models of hibernation to test for relative influence of host and pathogen traits on white-nose syndrome.

Catherine G Haase,Sarah H Olson,Kirk A Silas,David T S Hayman,Raina K Plowright,Nathan W Fuller,Liam P Mcguire,C Reed Hranac,Kaleigh J O Norquay,Craig K R Willis

doi:10.1371/journal.pone.0222311

Abstract

Hibernation consists of extended durations of torpor interrupted by periodic arousals. The ‘dehydration hypothesis’ proposes that hibernating mammals arouse to replenish water lost through evaporation during torpor. Arousals are energetically expensive, and increased arousal frequency can alter survival throughout hibernation. Yet we lack a means to assess the effect of evaporative water loss (EWL), determined by animal physiology and hibernation microclimate, on torpor bout duration and subsequent survival. White-nose syndrome (WNS), a devastating disease impacting hibernating bats, causes increased frequency of arousals during hibernation and EWL has been hypothesized to contribute to this increased arousal frequency. WNS is caused by a fungus, which grows well in humid hibernaculum environments and damages wing tissue important for water conservation. Here, we integrated the effect of EWL on torpor expression in a hibernation energetics model, including the effects of fungal infection, to determine the link between EWL and survival. We collected field data for Myotis lucifugus, a species that experiences high mortality from WNS, to gather parameters for the model. In saturating conditions, we predicted healthy bats experience minimal mortality. Infected bats, however, suffer high fungal growth in highly saturated environments, leading to exhaustion of fat stores before spring. Our results suggest that host adaptation to humid environments leads to increased arousal frequency from infection, which drives mortality across hibernaculum conditions. Our modified hibernation model provides a tool to assess the interplay between host physiology, hibernaculum microclimate, and diseases such as WNS on winter survival.

Highlights

In periods of food scarcity, hibernators conserve energy by entering torpor, during which body temperature (Tb) is maintained near hibernaculum temperature and metabolic rate is lowered to reduce energy demands [1]
With the continued spread of White-nose syndrome (WNS), it is imperative to understand the effects of hibernaculum microclimate on fungal growth, host physiology, and winter survival
We showed that host parameters, body mass, fat mass, and area-specific rate of evaporative water loss (EWL), were important drivers of torpor bout duration

Summary

Introduction

In periods of food scarcity, hibernators conserve energy by entering torpor, during which body temperature (Tb) is maintained near hibernaculum temperature and metabolic rate is lowered to reduce energy demands [1]. The metabolic byproducts hypothesis suggests that bats accumulate byproducts from biochemical reactions during torpor, and these byproducts need to be excreted as waste as they can be damaging to cellular function [4]. Both of these hypotheses are affected by microclimate, which is supported by empirical evidence of the relationship between hibernaculum temperature and relative humidity and torpor bout duration [3,5,7,8]. The dehydration hypothesis is supported by correlations between torpor bout duration/arousal frequency and hibernaculum temperature and relative humidity in both free living and laboratory conditions [2,5,13]

Methods

Results

Conclusion