Implicating a Temperature-Dependent Clock in the Regulation of Torpor Bout Duration in Classic Hibernation

Abstract

Syrian hamsters may present 2 types of torpor when exposed to ambient temperatures in the winter season, from 8°C to 22°C (short photoperiod). The first is daily torpor, which is controlled by the master circadian clock of the body, located in the SCN. In this paper, we show that daily torpor bout duration is unchanged over the 8°C to 22°C temperature range, as predicted from the thermal compensation of circadian clocks. These findings contrast with the second type of torpor: multi-day torpor or classic hibernation. In multi-day torpor, bout duration increases as temperature decreases, following Arrhenius thermodynamics. We found no evidence of hysteresis from metabolic inhibition and the process was thus reversible. As a confirmation, at any temperature, the arousal from multi-day torpor occurred at about the same subjective time given by this temperature-dependent clock. The temperature-dependent clock controls the reduced torpor metabolic rate while providing a reversible recovery of circadian synchronization on return to euthermy.

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“…In many small hibernators, length of each torpor bout gradually increases from the beginning, reaches its peak in the middle, and then decreases at the end of the hibernation season, even in constant ambient temperature conditions (MacCannell & Staples, 2021) (Ortmann & Heldmaier, 2000) (Arnold et al, 2011) (Sheriff et al, 2013) (Siutz et al, 2018). Ambient and core body temperatures also affect duration of each deep torpor bout, suggesting involvement of a temperature-sensitive process in the regulation of torpor-IBA cycles (MacCannell & Staples, 2021) (Twente & Twente, 1965) (Geiser & Kenagy, 1988) (Malan et al, 2018). Metabolic rate measured by oxygen consumption contributes to the determination of torpor-IBA timings in golden mantled ground squirrels and garden dormice (Geiser & Kenagy, 1988) (Ruf et al, 2021), although the exact metabolic process responsible for determination of torpor-IBA timing is not yet clear.…”

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“…Ambient and core body temperatures also affect duration of each deep torpor bout, suggesting involvement of a temperature-sensitive process in the regulation of torpor-IBA cycles 13,[25][26][27] .…”

“…In many small hibernators, length of each torpor bout gradually increases from the beginning, reaches its peak in the middle, and then decreases at the end of the hibernation season, even in constant ambient temperature conditions (MacCannell & Staples, 2021) (Ortmann & Heldmaier, 2000) (Arnold et al, 2011) (Sheriff et al, 2013) (Siutz et al, 2018). Ambient and core body temperatures also affect duration of each deep torpor bout, suggesting involvement of a temperature-sensitive process in the regulation of torpor-IBA cycles (MacCannell & Staples, 2021) (Twente & Twente, 1965) (Geiser & Kenagy, 1988) (Malan et al, 2018). Metabolic rate measured by oxygen consumption contributes to the determination of torpor-IBA timings in golden mantled ground squirrels and garden dormice (Geiser & Kenagy, 1988) (Ruf et al, 2021), although the exact metabolic process responsible for determination of torpor-IBA timing is not yet clear.…”

“…ω 1 may correspond to the period generated by such mechanisms. In contrast, timing of shallow/daily torpor, an adaptive response to winter condition or food shortage, during which basal metabolisms and Tb drops for a shorter period, typically several hours and within a day, is related to circadian rhythm in some species, including Djungarian hamster ( Phodopus sungorus ), which exhibits seasonal shallow/daily torpor, and mice entering fasting-induced torpor (Körtner & Geiser, 2000) (Malan et al, 2018) (Oklejewicz et al, 2001) (van der Vinne et al, 2018) (Kirsch et al, 1991) (Ruf & Geiser, 2015). Thus, the situation is still complex and further research is needed to determine whether is sensitive to ambient temperature during hibernation.…”

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“…Moreover, in Syrian hamsters, the circadian system does not participate in the temporal organization of torpor–arousal cycles during prolonged hibernation at 6°C (Oklejewicz, Daan & Strijkstra, 2001). Recent research has revealed that a temperature‐dependent clock regulates the reduction of MR in multi‐day torpor and regains circadian synchronization after arousal (Malan et al ., 2018). In golden‐mantled ground squirrels ( Spermophilus lateralis ) and Arctic ground squirrels, the circadian clock genes and c‐fos expression in the SCN are suppressed during deep torpor and reversed during arousal from a torpid state (Bitting et al ., 1994; Ikeno et al ., 2017).…”