Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome

Mayberry, Heather W.; McGuire, L.; Willis, Craig K. R.

doi:10.1007/s00360-017-1119-0

Cited by 29 publications

(25 citation statements)

References 57 publications

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“…Flexible use of torpor could represent a trade-off between energy savings and immune function (Bouma et al, 2010). Reduced torpor expression could also reflect a fever response similar to that observed by Mayberry et al (2018) for hibernating bats with WNS during arousals, and we recommend that future studies test this hypothesis by assessing expression of fevermediating cytokines during WNS recovery (Evans et al, 2015;Lilley et al, 2017). WNS survivors must trade off investment in energetically costly healing against the need to maintain energy balance and, for females, investment in reproduction.…”

Section: Discussionmentioning

confidence: 94%

Disease recovery in bats affected by white-nose syndrome

Fuller

McGuire

Pannkuk

et al. 2020

Journal of Experimental Biology

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Processes associated with recovery of survivors are understudied components of wildlife infectious diseases. White-nose syndrome (WNS) in bats provides an opportunity to study recovery of disease survivors, understand implications of recovery for individual energetics, and assess the role of survivors in pathogen transmission. We documented temporal patterns of recovery from WNS in little brown bats (Myotis lucifugus) following hibernation to test the hypotheses that: (1) recovery of wing structure from WNS matches a rapid time scale (i.e. approximately 30 days) suggested by data from free-ranging bats; (2) torpor expression plays a role in recovery; (3) wing physiological function returns to normal alongside structural recovery; and (4) pathogen loads decline quickly during recovery. We collected naturally infected bats at the end of hibernation, brought them into captivity, and quantified recovery over 40 days by monitoring body mass, wing damage, thermoregulation, histopathology of wing biopsies, skin surface lipids and fungal load. Most metrics returned to normal within 30 days, although wing damage was still detectable at the end of the study. Torpor expression declined overall throughout the study, but bats expressed relatively shallow torpor boutswith a plateau in minimum skin temperatureduring intensive healing between approximately days 8 and 15. Pathogen loads were nearly undetectable after the first week of the study, but some bats were still detectably infected at day 40. Our results suggest that healing bats face a severe energetic imbalance during early recovery from direct costs of healing and reduced foraging efficiency. Management of WNS should not rely solely on actions during winter, but should also aim to support energy balance of recovering bats during spring and summer.

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Section: Discussionmentioning

confidence: 94%

Disease recovery in bats affected by white-nose syndrome

Fuller

McGuire

Pannkuk

et al. 2020

Journal of Experimental Biology

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“…In addition to causing local inflammation and activation of immune responses in locoregional lymph nodes (Lilley et al., ), these inflammatory mediators may have systemic effects. Although the febrile response is inactive during torpor (Prendergast et al., ), bats with WNS in some (Lilley et al., ; Mayberry, McGuire, & Willis, ), but not all (Brownlee‐Bouboulis & Reeder, ; Moore et al., ), previous studies show elevated skin temperature during interbout arousals. Systemic inflammation could also influence the torpor–arousal cycle and contribute to WNS pathology by increasing arousal frequency.…”

Section: Discussionmentioning

confidence: 99%

Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats

et al. 2018

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Hibernation, the use of prolonged torpor to depress metabolism, is employed by mammals to conserve resources during extended periods of extreme temperatures and/or resource limitation. Mammalian hibernators arouse to euthermy periodically during torpor for reasons that are not well understood, and these arousals may facilitate immune processes. To determine whether arousals enable host responses to pathogens, we used dual RNA-Seq and a paired sampling approach to examine gene expression in a hibernating bat, the little brown myotis (Myotis lucifugus). During torpor, transcript levels differed in only a few genes between uninfected wing tissue and adjacent tissue infected with Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome. Within 70-80 min after emergence from torpor, large changes in gene expression were observed due to local infection, particularly in genes involved in pro-inflammatory host responses to fungal pathogens, but also in many genes involved in immune responses and metabolism. These results support the hypothesis that torpor is a period of relative immune dormancy and arousals allow for local immune responses in infected tissues during hibernation. Host-pathogen interactions were also found to regulate gene expression in the pathogen differently depending on the torpor state of the host. Hibernating species must balance the benefits of energy and water conservation achieved during torpor with the costs of decreased immune competence. Interbout arousals allow hibernators to optimize these, and other, trade-offs during prolonged hibernation by enabling host responses to pathogens within brief, periodic episodes of euthermy.

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“…Clinical pathology of Pd infection in North American species is associated with abnormal behaviour, a disturbed natural hibernation cycle characterized by increased arousal frequency resulting in premature depletion of fat stores during hibernation (Reeder et al., 2012). Diseased animals show disturbed electrolyte and hydration balance (Cryan et al., 2013; Willis, Menzies, Boyles, & Wojciechowski, 2011), oxidative stress (Moore et al., 2013), chronic respiratory acidosis (Verant et al., 2014), altered complement protein activity (Moore et al., 2011) and fever response (Mayberry, McGuire, & Willis, 2018). Pd infection does not produce primary inflammatory cellular infiltration into infected tissues (Meteyer et al., 2009), which would be associated with leukopenia (i.e., low white blood cell counts) during mammalian hibernation (Bouma, Carey, & Kroese, 2010).…”

Section: Introductionmentioning

confidence: 99%

Plasma proteomic profiles differ between European and North American myotid bats colonized by Pseudogymnoascus destructans

et al. 2020

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Emerging fungal diseases have become challenges for wildlife health and conservation. North American hibernating bat species are threatened by the psychrophilic fungus Pseudogymnoascus destructans (Pd) causing the disease called white-nose syndrome (WNS) with unprecedented mortality rates. The fungus is widespread in North America and Europe, however, disease is not manifested in European bats. Differences in epidemiology and pathology indicate an evolution of resistance or tolerance mechanisms towards Pd in European bats. We compared the proteomic profile of blood plasma in healthy and Pd-colonized European Myotis myotis and North American Myotis lucifugus in order to identify pathophysiological changes associated with Pd colonization, which might also explain the differences in bat survival. Expression analyses of plasma proteins revealed differences in healthy and Pd-colonized M. lucifugus, but not in M. myotis. We identified differentially expressed proteins for acute phase response, constitutive and adaptive immunity, oxidative stress defence, metabolism and structural proteins of exosomes and desmosomes, suggesting a systemic response against Pd in North American M. lucifugus but not European M. myotis. The differences in plasma proteomic profiles between European and North American bat species colonized by Pd suggest European bats have evolved tolerance mechanisms towards Pd infection.

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Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome

Cited by 29 publications

References 57 publications

Disease recovery in bats affected by white-nose syndrome

Disease recovery in bats affected by white-nose syndrome

Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats

Plasma proteomic profiles differ between European and North American myotid bats colonized by Pseudogymnoascus destructans

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