Daily body temperature rhythms persist under the midnight sun but are absent during hibernation in free-living arctic ground squirrels

Abstract

In indigenous arctic reindeer and ptarmigan, circadian rhythms are not expressed during the constant light of summer or constant dark of winter, and it has been hypothesized that a seasonal absence of circadian rhythms is common to all vertebrate residents of polar regions. Here, we show that, while free-living arctic ground squirrels do not express circadian rhythms during the heterothermic and pre-emergent euthermic intervals of hibernation, they display entrained daily rhythms of body temperature (T(b)) throughout their active season, which includes six weeks of constant sun. In winter, ground squirrels are arrhythmic and regulate core body temperatures to within ±0.2°C for up to 18 days during steady-state torpor. In spring, after the use of torpor ends, male but not female ground squirrels, resume euthermic levels of T(b) in their dark burrows but remain arrhythmic for up to 27 days. However, once activity on the surface begins, both sexes exhibit robust 24 h cycles of body temperature. We suggest that persistence of nycthemeral rhythms through the polar summer enables ground squirrels to minimize thermoregulatory costs. However, the environmental cues (zeitgebers) used to entrain rhythms during the constant light of the arctic summer in these semi-fossorial rodents are unknown.

Figure 1.

Annual patterns of core T_b of a representative male and female arctic ground squirrel together with double-plotted actograms of when T_b remained at euthermic levels (each row represents two consecutive days). For actograms, the x-axis is the time of day (hour) and black bars indicate intervals when T_b was above the mean. Blocks indicated by a and e during heterothermy of hibernation are torpor intervals that are expanded in the insert indicated by the arrow; b indicates the prolonged interval of euthermic T_b that occurs in males after heterothermy ends but before they emerge from their burrows; f indicates the post-emergence interval in females; g and c are mid active season intervals; d indicates when this male remained in the burrow prior to first torpor; h is the pre-immergence interval in this female. Box graphs b–d and f–h show the F—periodograms for rhythms of T_b that correspond to 10 day intervals indicated on the actograms and T_b traces. Black lines indicate the strength of rhythms (Q); curved grey lines indicate 95% confidence limit.