Turner James M, Warnecke Lisa, Wilcox Alana, Baloun Dylan, Bollinger Trent K, Misra Vikram, Willis Craig K R
Department of Biology and Centre for Forest Interdisciplinary Research, University of Winnipeg, Winnipeg, MB R3B2E9, Canada.
Department of Veterinary Pathology and Canadian Wildlife Health Cooperative, University of Saskatchewan, Saskatoon, SK S7N5B4, Canada.
Physiol Behav. 2015 Mar 1;140:71-8. doi: 10.1016/j.physbeh.2014.12.013. Epub 2014 Dec 4.
The emerging wildlife disease white-nose syndrome (WNS) affects both physiology and behaviour of hibernating bats. Infection with the fungal pathogen Pseudogymnoascus destructans (Pd), the first pathogen known to target torpid animals, causes an increase in arousal frequency during hibernation, and therefore premature depletion of energy stores. Infected bats also show a dramatic decrease in clustering behaviour over the winter. To investigate the interaction between disease progression and torpor expression we quantified physiological (i.e., timing of arousal, rewarming rate) and behavioural (i.e., arousal synchronisation, clustering) aspects of rewarming events over four months in little brown bats (Myotis lucifugus) experimentally inoculated with Pd. We tested two competing hypotheses: 1) Bats adjust arousal physiology adaptively to help compensate for an increase in energetically expensive arousals. This hypothesis predicts that infected bats should increase synchronisation of arousals with colony mates to benefit from social thermoregulation and/or that solitary bats will exhibit faster rewarming rates than clustered individuals because rewarming costs fall as rewarming rate increases. 2) As for the increase in arousal frequency, changes in arousal physiology and clustering behaviour are maladaptive consequences of infection. This hypothesis predicts no effect of infection or clustering behaviour on rewarming rate and that disturbance by normothermic bats contributes to the overall increase in arousal frequency. We found that arousals of infected bats became more synchronised than those of controls as hibernation progressed but the pattern was not consistent with social thermoregulation. When a bat rewarmed from torpor, it was often followed in sequence by up to seven other bats in an arousal "cascade". Moreover, rewarming rate did not differ between infected and uninfected bats, was not affected by clustering and did not change over time. Our results support our second hypothesis and suggest that disturbance, not social thermoregulation, explains the increased synchronisation of arousals. Negative pathophysiological effects of WNS on energy conservation may therefore be compounded by maladaptive changes in behaviour of the bats, accelerating fat depletion and starvation.
新出现的野生动物疾病白鼻综合征（WNS）会影响冬眠蝙蝠的生理和行为。感染真菌病原体毁灭假裸囊菌（Pd），这是已知的第一种针对蛰伏动物的病原体，会导致冬眠期间觉醒频率增加，从而使能量储备过早耗尽。受感染的蝙蝠在冬季的集群行为也会显著减少。为了研究疾病进展与蛰伏表现之间的相互作用，我们对实验接种Pd的小棕蝠（Myotis lucifugus）在四个月内的复温事件的生理（即觉醒时间、复温速率）和行为（即觉醒同步性、集群）方面进行了量化。我们测试了两个相互竞争的假设：1）蝙蝠会适应性地调整觉醒生理，以帮助补偿能量消耗高昂的觉醒增加。该假设预测，受感染的蝙蝠应增加与群体伙伴觉醒的同步性，以从社会体温调节中受益，和/或单独的蝙蝠比集群个体表现出更快的复温速率，因为随着复温速率增加，复温成本会下降。2）至于觉醒频率的增加，觉醒生理和集群行为的变化是感染的适应不良后果。该假设预测感染或集群行为对复温速率没有影响，并且正常体温的蝙蝠的干扰导致了觉醒频率的总体增加。我们发现，随着冬眠的进行，受感染蝙蝠的觉醒比对照组变得更加同步，但这种模式与社会体温调节不一致。当一只蝙蝠从蛰伏中复温时，在觉醒“级联”中，通常会有多达七只其他蝙蝠依次跟随。此外，受感染和未受感染的蝙蝠之间的复温速率没有差异，不受集群影响，也不会随时间变化。我们的结果支持我们的第二个假设，并表明干扰而非社会体温调节解释了觉醒同步性的增加。因此，WNS对能量保存的负面病理生理影响可能会因蝙蝠行为的适应不良变化而加剧，加速脂肪消耗和饥饿。
