Can bats sense smoke during deep torpor?

Abstract

While torpor is a beneficial energy-saving strategy, it may incur costs if an animal is unable to respond appropriately to external stimuli, which is particularly true when it is necessary to escape from threats such as fire. We aimed to determine whether torpid bats, which are potentially threatened because they must fly to escape, can sense smoke and whether respiration rate (RR), heart rate (HR) and reaction time of torpid bats prior to and following smoke introduction is temperature-dependent. To test this we quantified RR and HR of captive Australian tree-roosting bats, Nyctophilus gouldi (n=5, ~10g), in steady-state torpor in response to short-term exposure to smoke from Eucalyptus spp. leaves between ambient temperatures (T) of 11 and 23°C. Bats at lower T took significantly longer (28-fold) to respond to smoke, indicated by a cessation of episodic breathing and a rapid increase in RR. Bats at lower T returned to torpor more swiftly following smoke exposure than bats at higher T. Interestingly, bats at T<15°C never returned to thermoconforming steady-state torpor prior to the end of the experimental day, whereas all bats at T≥15°C did, as indicated by apnoeic HR. This shows that although bats at lower T took longer to respond, they appear to maintain vigilance and prevent deep torpor after the first smoke exposure, likely to enable fast escape. Our study reveals that bats can respond to smoke stimuli while in deep torpor. These results are particularly vital within the framework of fire management conducted at T<15°C, as most management burns are undertaken during winter when bats will likely respond more slowly to fire cues such as smoke, delaying the time to escape from the fire.

A burning question: what are the risks and benefits of mammalian torpor during and after fires?

“…During torpor, locomotor and sensory capabilities are reduced ( Scesny, 2006 ; Rojas et al , 2012 ; Luo et al , 2014 ; Nowack et al , 2016a ; Bartonička et al , 2017 ), which could prevent them from sensing and reacting to smoke and other fire cues in time to escape. However, torpid dunnarts ( Sminthopsis crassicaudata ), pygmy-possums ( Cercartetus nanus ) and bats ( Lasiurus borealis and Nyctophilus gouldi ) can respond to smoke, but the response is slowed at low T a ( Scesny, 2006 ; Stawski et al , 2015b ; Nowack et al , 2016a ; Doty et al , 2018 ). Dunnarts, S. crassicaudata , in shallow torpor with a T b of ~18 to 25°C rewarmed from torpor about 40 min after smoke exposure.…”

“… Doty et al (2016b) Long-eared Bat Nyctophilus gouldi Captive Torpid bats respond to smoke within seconds, but exposure to cold slows response. Doty et al (2018) Eastern red bat Lasiurus borealis Field Bats flushed by fire and ‘smoked’ from hibernaculum. Observed on ground still partially torpid attempting to fly or crawl.…”

“…For torpid long-eared bats ( N. gouldi ) the response to smoke, measured as an increase in respiration rate, was rapid and occurred within 1 s at T a 21.4°C ( T b ~22.4°) and 36 s at T a 11.9°C ( T b ~12.9°C). All bats rapidly (~8–15 min) rewarmed from torpor ( Doty et al , 2018 ). Eastern red bats, L. borealis , responded occasionally to fire noise at low T a , but when fire noise and smoke were combined all bats arose ( Scesny, 2006 ).…”

“…After the cessation of smoke exposure, long-eared bats ( N. gouldi ) re-entered torpor, but they never returned to thermo-conforming, steady-state torpor prior to the end of the experimental day at low T a , although those at warmer T a did ( Doty et al , 2018 ). Not returning to steady-state torpor at low T a will increase energy expenditure, but presumably this cost is traded-off with the benefits of maintaining vigilance in the case of repeated smoke exposure.…”

Animal movements in fire‐prone landscapes

“…The behavioural response of many species to fire cues points to the importance of a rapid reaction to incipient fire. For instance, eastern red bats ( Lasiurus borealis ), which hibernate beneath leaf litter, rewarmed from torpor in response to smoke and the sound of flames (Scesny, ), while smoke exposure initiated rapid rewarming in Gould's long‐eared bats ( Nyctophilus gouldi ) and fat‐tailed dunnarts ( Sminthopsis crassicaudata ) (Stawski et al ., ; Doty et al ., ). These flight responses are presumably due to the flammability of their retreat sites.…”