Elsevier

Journal of Thermal Biology

Volume 82, May 2019, Pages 150-156
Journal of Thermal Biology

Numerous cold arousals and rare arousal cascades as a hibernation strategy in European Myotis bats

https://doi.org/10.1016/j.jtherbio.2019.04.002Get rights and content

Highlights

  • Normothermic and cold arousals, where bats stopped their body temperatures at ≤ 10 °C, were found.

  • Cold arousals were a response to disturbance by a neighbour in the same cluster.

  • Arousal cascades, where bats aroused in series, were rare and reached a maximum in mid-January.

Abstract

Hibernating bats optimise the duration of torpor bouts and arousals in relation to hibernaculum microclimatic conditions and fat reserves. Clustering has significant physiological and ecological benefits, promoting successful hibernation of individuals. Such aggregations may help maintain optimal temperatures, allowing better energy utilisation than in solitarily bats. However, aroused bats in a cluster could conceivably disturb those still hibernating, starting an energy-demanding arousal process. Our study was conducted over two winters in two different hibernacula (cave and mine) in the Czech Republic, where Greater mouse-eared bats (Myotis myotis) have previously been diagnosed with white-nose syndrome. In 118 arousal episodes we recorded 193 individual arousals in which a warming phase was observed, 135 (69.9%) being cold arousals, where bats ceased increasing their body temperatures at ≤ 10 °C. The remaining arousals were standard normothermic arousals, where body (fur) surface temperatures reached > 20 °C. Cold arousals occurred during the mid- and late hibernation periods, suggesting they were a response to disturbance by a neighbour in the same cluster. Arousal cascades, where bats aroused in series, were rare (12.7%) and reached a maximum in mid-January. Our data suggest that Myotis bats prolong their torpor bouts using numerous cold arousals but few arousal cascades. Upon arrival of a bat, the clustered bats show tolerance to disturbing by conspecifics.

Introduction

Although hibernating mammals can rewarm from torpor passively as ambient temperature increases (Geiser et al., 2004) many, such as temperate bats, can also change their body temperature from low values during torpor to high normothermic values using endogenous heat production. However, increasing body temperature during arousal above the ambient temperature is energetically costly (Boyles et al., 2006). To manage energy expenditure over the period of hibernation, hibernating mammals optimise roosting site selection and torpor bouts and arousals in relation to both temperature in the hibernaculum and their fat reserves (Geiser and Kenagy, 1988). The selection of roosting site, and hence the temperature at the site, determines the both metabolic rate and energy consumption (Boyles et al., 2007). When fat reserves dwindle, or ambient conditions change, bats may change roost sites during arousal, within or even between hibernacula (Twente 1955; Berkova and Zukal, 2006; Zukal et al., 2016a).

Clustering is a behavioural phenomenon with significant physiological and ecological consequences for successful hibernation. Bats hibernating underground benefit from clustering behaviour during normothermic periods (Boyles et al., 2008), where clusters of just five individuals show reduced energy consumption (Brown, 1999; Boyles and Brack, 2009) and loss of water through evaporation (Thomas and Geiser, 1997, Boratynski et al. 2015). Bats can further decrease their energy expenditure during arousals if individuals in a cluster synchronise arousals in an arousal cascade, thereby sharing the costs via social thermoregulation (Boyles et al., 2008, Boyles and Brack, 2009; Boratynski et al. 2012; Czenze et al., 2013). However, cluster formation can also prove risky to bats already hibernating at the roosting site where the cluster develops. Following the assumption that bats hibernating in clusters conserve energy, individuals should be sensitive to activity in a cluster in order to facilitate arousal cascades; however, bats should also be able to avoid disturbance from a neighbour when arousals are not physiologically or energetically beneficial (Czenze and Willis, 2015). Consequently, arousal cascades should be rare during periods of cluster formation, and their frequency should increase during late hibernation when the frequency of arousals increased linearly with ambient temperature (e.g. Johnson et al., 2012).

Bats also alter their behaviour during hibernation in reaction to infection. Pseudogymnoascus destructans fungus, known cause of white-nose syndrome, forms lesions on the wing tissue, the lesions being more extensive in the Nearctic than Palearctic (Bandouchova et al., 2015; Zukal et al., 2016b), though the duration of normothermic arousals does not differ between infected and healthy bats (Warnecke et al., 2012; Brownlee-Bouboulis and Reeder, 2013). Strategies that facilitate energy conservation are likely to face selection pressure. One such strategy is social thermoregulation, where individuals that live within groups limit their activity during arousal and reduce the number of individuals in clusters (Wilcox et al., 2014; Bohn et al., 2016). Arousal cascades, synchronised arousals, if they are advantageous, should be very common and represent most of the arousals during hibernation (Czenze and Willis, 2015). During arousal cascade bats may be able to rewarm at the same time and reduce individual costs by sharing heat energy with other group members (Boyles et al., 2008). However, temperature preference is not a fixed phenomenon but depends on many intrinsic and extrinsic factors, including the reduction of individual costs, thermal conditions available in the environment, and cluster size (Boyles et al., 2007; Wojciechowski et al., 2007). Following mass mortalities of WNS-infected bats in the Nearctic, fewer bats were found in hibernacula, which may be adaptation to WNS (Frick et al., 2015), despite of the fact that not all bats react the same. The effective size of the cluster could also be affected by maintaining a body temperature lower than normothermic temperature, which may represent a strategy noted by Jonasson and Willis (2012) as cold arousals, where individuals hibernating in a cluster reduce the negative impact with other conspecifics (Czenze et at. 2013).

Given that bats with WNS in the Nearctic exhibit aberrant behaviour during hibernation, we decided to investigate the behaviour of bat species tolerant to WNS (Zukal et al., 2016b). The greater mouse-eared bat (Myotis myotis, body mass 20–35 g) is a common species in European underground hibernacula (Řehák et al., 1994) and prevalence of WNS in the species is one of the highest in the Palearctic (Zukal et al., 2014). Despite their infection tolerance, however, an increased P. destructans infection intensity of over 300 lesions disrupt blood homeiostasis (Bandouchova et al., 2018). Myotis myotis often hibernate in clusters, though these tend to be contain fewer individuals than in some North American species (Frick et al., 2015). Considering the relative lack of knowledge on hibernation behaviour under pathogen pressure, we investigated 1) the pattern of arousals in hibernating WNS-tolerant bats, 2) the frequency of arousal synchronisation concerning the “arousal hypothesis” of Boyles et al. (2008), which suggests that clustering minimises heat loss, and 3) whether synchronised rewarming and number of arousals increase late during the season of hibernation, when fat reserves are more likely to be depleted.

Section snippets

Study sites

This study was conducted over the winters of 2012/13 and 2013/14 in the Šimon and Juda Mine near Malá Morávka in the Jeseníky Mountains (50°03′N, 17°18′E; 900 m a.s.l.) and the Kateřinská Cave in the Moravian Karst (49°21′N, 16°48′E, 345 m a.s.l.), Czech Republic. The two hibernacula are among the most important hibernacula for M. myotis in the Czech Republic, with approximately 500–700 individuals hibernating in the mine and 50–120 in the cave from mid-November to mid-April.

The Šimon and Juda

Arousal episode characteristics

In total, 71 794 thermal images were recorded of four different bat clusters (one per year in both SVM and KC), each with 3–16 individuals. Arousals lasted up to 525 min, with a median of 70 min (Tab. S1). We found no evidence of any relationship between time of arousals and sunset (Rayleigh's test: Z = 0.61, p = 0.364, mean vector = 0.27, n = 193).

We recorded individual arousals of 193 bats. In 135 (69.9%) arousals, bats cease lowering their Ts at a steady-state with ΔTs≤ 10 °C (cold arousals

Discussion

We observed 70% of arousal episodes where bats ceased Ts temperature elevation at < 10 °C. We called these “cold arousals” as they were characterised by obvious warming and cooling phases, clearly differing from low Ts changes lacking a temperature elevation (Bartonička et al., 2017). During cold arousals, Ts increased by ≤ 6 °C compared to ≥18 °C for normothermic arousal episodes. While bats frequently relocated after normothermic arousal episodes, they did not move during cold arousal

Acknowledgments

We are very grateful to Justin Boyles, Virgil Brack and the other two reviewers for their comments and suggestions that allowed us to greatly improve the quality of the manuscript, to Kevin Roche for linguistic comments on the manuscript. This study was supported through grants from the Czech Science Foundation No. 17-20286S and Masaryk University MUNI/A/1436/2018.

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      Although the function of cold arousals is not completely understood, it is likely they are less energetically costly compared to rewarming to normothermia (Mayberry et al., 2018). Cold arousals and movement at low Tb may also prolong torpor bouts between two successive normothermic arousals (Bartonička et al., 2017), allowing bats to reduce the energetic costs of disturbance by cluster-mates with behaviour that facilitates energy saving (Mayberry et al., 2018; Blažek et al., 2019). As we hypothesised, bats reacted to disturbance with controlled energy saving behaviour (Blažek et al., 2019).

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