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

  • Heather W. Mayberry
  • Liam P. McGuire
  • Craig K. R. Willis
Original Paper

Abstract

Hibernating animals use torpor [reduced body temperature (Tb) and metabolic rate] to reduce energy expenditure during winter. Periodic arousals to normal Tb are energetically expensive, so hibernators trade off arousal benefits against energetic costs. This is especially important for bats with white-nose syndrome (WNS), a fungal disease causing increased arousal frequency. Little brown bats (Myotis lucifugus) with WNS show upregulation of endogenous pyrogens and sickness behaviour. Therefore, we hypothesized that WNS should cause a fever response characterized by elevated Tb. Hibernators could also accrue some benefits of arousals with minimal Tb increase, thus avoiding full arousal costs. We compared skin temperature (Tsk) of captive Myotis lucifugus inoculated with the WNS-causing fungus to Tsk of sham-inoculated controls. Infected bats re-warmed to higher Tsk during arousals which is consistent with a fever response. Torpid Tsk did not differ. During what we term “cold arousals”, bats exhibited movement following Tsk increases of only 2.2 ± 0.3 °C, compared to >20 °C increases during normal arousals. Cold arousals occurred in both infected and control bats, suggesting they are not a pathophysiological consequence of WNS. Fever responses are energetically costly and could exacerbate energy limitation and premature fat depletion for bats with WNS. Cold arousals could represent an energy-saving mechanism for both healthy and WNS-affected bats when complete arousals are unnecessary or too costly. A few cold arousals were observed mid-hibernation, typically in response to disturbances. Cold arousals may, therefore, represent a voluntary restriction of arousal temperature instead of loss of thermoregulatory control.

Keywords

Arousals Myotis lucifugus Hibernation energetics WNS Heterothermy 

Abbreviations

Tb

Body temperature

Tsk

Skin temperature

Ta

Ambient temperature

WNS

White-nose syndrome

IR

Infrared

Supplementary material

360_2017_1119_MOESM1_ESM.pdf (330 kb)
Table S1 Details of cold and normal arousals included in analysis. The date of each arousal is reported, along with the Tsk associated with the arousal. The Tsk during steady state torpor prior to the arousal is the Baseline Tsk. The increase in Tsk during the arousal (ΔTsk) is the difference between the maximum Tsk observed during the arousal and the baseline Tsk. For cold arousals we note whether the cold arousal was the final arousal for that bat (yes) or whether the bat subsequently underwent a normal arousal (no) (PDF 329 KB)
360_2017_1119_MOESM2_ESM.asf (6.1 mb)
Video S1: A 1 minute video clip of representative behavior during a normal arousal. At the beginning of the video the bat is roosting on the side of the cage grooming, then crawls around the floor of the cage before getting a drink from the water dish. Note the coordinated and relatively rapid movements. The bat in the clip is Bat 3482 from the control treatment. The arousal occurred on Jan 4, 2014 and lasted 87 minutes. At the end of the arousal the bat rejoined the group of torpid bats visible in the upper right corner of the video (ASF 6200 KB)
360_2017_1119_MOESM3_ESM.asf (6.2 mb)
Video S2: A second video clip from the same normal arousal in Video S1. This clip occurs a few minutes later. As before, the bat crawls around the cage and visits the water dish. At the end of the clip the bat flaps its wings in a brief attempted flight before climbing the wall of the cage. During this normal arousal skin temperature reached a maximum of 26.5°C (ASF 6325 KB)
360_2017_1119_MOESM4_ESM.asf (1.9 mb)
Video S3: The initiation of a cold arousal. On Feb 21, 2014, bat 3485 is active and dislodges bat 3492 from the cluster of torpid bats. Bat 3492 had previously undergone a normal arousal just two days prior, on February 19. This video clip is taken from the control treatment (ASF 1913 KB)
360_2017_1119_MOESM5_ESM.asf (3.1 mb)
Video S4: Bat 3492, having been dislodged from its roost in Video S3, crawls around the floor of the cage. Note the slow, sluggish, uncoordinated nature of the movement compared to the movements in a normal arousal (Video S1, S2). During this cold arousal skin temperature reached a maximum of 8.0°C (ASF 3197 KB)
360_2017_1119_MOESM6_ESM.asf (6.1 mb)
Video S5: Conclusion of a cold arousal. Bat 3492 returns to the wall of the cage after being dislodged from roosting (Video S3) and crawling around the floor of the cage (Video S4). Total duration of the cold arousal was 4 minutes. The bat subsequently underwent a normal arousal one week later on February 29, 2014 (ASF 6279 KB)

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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Heather W. Mayberry
    • 1
    • 2
  • Liam P. McGuire
    • 1
    • 3
  • Craig K. R. Willis
    • 1
  1. 1.Department of BiologyUniversity of WinnipegWinnipegCanada
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of Toronto MississaugaMississaugaCanada
  3. 3.Department of Biological SciencesTexas Tech UniversityLubbockUSA

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