The bear circadian clock doesn’t ‘sleep’ during winter dormancy

Abstract

BackgroundMost biological functions are synchronized to the environmental light:dark cycle via a circadian timekeeping system. Bears exhibit shallow torpor combined with metabolic suppression during winter dormancy. We sought to confirm that free-running circadian rhythms of body temperature (Tb) and activity were expressed in torpid grizzly (brown) bears and that they were functionally responsive to environmental light. We also measured activity and ambient light exposures in denning wild bears to determine if rhythms were evident and what the photic conditions of their natural dens were. Lastly, we used cultured skin fibroblasts obtained from captive torpid bears to assess molecular clock operation in peripheral tissues. Circadian parameters were estimated using robust wavelet transforms and maximum entropy spectral analyses.ResultsCaptive grizzly bears housed in constant darkness during winter dormancy expressed circadian rhythms of activity and Tb. The rhythm period of juvenile bears was significantly shorter than that of adult bears. However, the period of activity rhythms in adult captive bears was virtually identical to that of adult wild denning bears as was the strength of the activity rhythms. Similar to what has been found in other mammals, a single light exposure during the bear’s active period delayed subsequent activity onsets whereas these were advanced when light was applied during the bear’s inactive period. Lastly, in vitro studies confirmed the expression of molecular circadian rhythms with a period comparable to the bear’s own behavioral rhythms.ConclusionsBased on these findings we conclude that the circadian system is functional in torpid bears and their peripheral tissues even when housed in constant darkness, is responsive to phase-shifting effects of light, and therefore, is a normal facet of torpid bear physiology.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0173-x) contains supplementary material, which is available to authorized users.

The Clock Keeps Ticking: Circadian Rhythms of Free-Ranging Polar Bears

“…Denning bears have sharply reduced levels of activity (Messier et al, 1994; Ware et al, 2012), but whether the circadian clock operates in denning polar bears is unknown. Mammals living in nonpolar regions that undergo deep hibernation or daily torpor exhibit a range of circadian characteristics including complete loss of circadian rhythmicity to apparent entrainment to environmental cues and expression of free-running rhythms (Körtner and Geiser, 2000; Heller and Ruby, 2004; Revel et al, 2007; Gür et al, 2009; Healy et al, 2012; Jansen et al, 2016). We identified denning events in the data set using a control chart-based algorithm applied to collar temperature data to identify extended periods of warm temperatures that are indicative of denning events because the insulated snow dens of polar bears result in the collar temperature sensor remaining well above ambient air (Olson, 2017; Rode et al, 2018).…”

“…Plotting of activity as actograms and period and phase analyses were carried out using custom MATLAB scripts (The MathWorks, Natick, MA), adapted from the code developed for Jansen et al (2016). The MATLAB scripts are publicly posted (https://osf.io/jqtge/).…”

Hibernating bear serum hinders osteoclastogenesis in-vitro

“…iii) It is also possible that serum factors affect bone metabolism indirectly through the modulation of circadian rhythm. Jansen et al, [23] showed when bear's fibroblasts were cultured with active and hibernation phase serum containing medium, cell molecular rhythm was akin to those of active and hibernation phases, respectively. Circadian rhythm can govern OC activity and formation through different pathways, such as: 1) Regulation of aryl hydrocarbon receptor nuclear translocator-like (Bmal1) in OC [54], 2) Modulation of Bmal1 in osteoblasts which leads to alteration in RANKL expression [55], and 3) β-adrenergic and glucocorticoid signaling in OC [56,57].…”

“…The use of bear serum for cell culture has been investigated in recent years. The in-vitro experiments have indicated that the use of active and hibernating bear serum for cell culture can induce active-like and hibernation-like cell responses, respectively [ 23 – 25 ]. For example, the use of hibernating bear serum inhibits proteolysis, and increases protein content in muscle cells [ 25 ].…”

Ecophysiology of mammals

“…also influence the use of torpor (Adams 2010;Rintoul and Brigham 2014). The control of hibernation and daily torpor is one area of ongoing interest, particularly related to neural regulation and brain function (Schwartz et al 2013;Scherbarth et al 2015;Jansen et al 2016), bone loss due to inactivity (Doherty et al 2014;Ma et al 2015;Wojda et al 2016), fat storage and use (Frank and Storey 1995;Contreras et al 2014), maintaining cellular functions (Zhang et al 2014b;Yuan et al 2015), and the microbiome (Carey and Assadi-Porter 2017). Not all mammals adjust their torpor use the same way in response to environmental perturbation; Doty et al (2016) recently reported that daily torpor use after a wildfire decreased in lesser longeared bats (Nyctophilus geoffroyi), in contrast to increased torpor use reported for terrestrial small mammals.…”