The wonders of hibernation in the animal kingdom

Animals inhabiting ecosystems with seasonal low resource availability and high-energy have developed torpor. During this state animal´s metabolic rate falls below that of the basic metabolic rate and the body temperature, heart rate and breathing fall drastically (1). A single torpor can last for up to a day triggered by low food availability (2). However, to cope with seasonal reduced energy expenditure animals evolved multiday torpor (hibernation). This process is controlled through both external and internal signals; however, the exact mechanisms of hibernation remain unclear (3). Therefore, this essay will aim to discuss the mechanisms that govern the phases of hibernation.


Multiday torpor causes a decrease of metabolic rate to approximately 1-2% and a decrease in body temperature to -2⁰C. Breathing can be suspended for up to 150 minutes and the heart rate lowered to 3-5 beats per minute thus decreasing the metabolic rate drastically (1,4,5). This state begins with pre-hibernation when the energy store is increased (6). To allow this the body becomes resistant to leptin during the fattening period as leptin would normally decrease food intake, preventing the accumulation of fat stores in white adipose tissue (WAT) (7,8). To prevent organ damage and adjust the body to the temperature change the animal also enters multiple short hibernations, each further lowering the brain temperature, respiration and heart rate (9). To maintain this hibernation the circadian clock expresses proteins such as the mitochondrial enzyme PDK4 which shuts down carbohydrate oxidation in mammals (10). This, and the suppression of lipolysis, lovers the utilisation of stored energy in WAT and metabolism maintaining hibernation for several months (11,12).


Deep hibernation is interknitted with interbout arousal (IBA) governed by the fluctuations of melatonin concentration and brown adipose tissue activity which arouses animals for a few hours, before returning to the state of hibernation (6,11). Although this requires re-warming of the body which costs energy, it might be important to prevent death of hunger or thirst as animals have been found to supply with food (1,13). However, it was observed that several hibernators utilise this time for sleep. The EEG scans showed that the hibernation pattern resembled the awake EEG, suggesting that the animals in hibernation do not experience sleep periods and must awake to prevent brain damage (14). The process of hibernation can be triggered externally, nevertheless, the temperature varies with years and several species have very exact hibernation timing, suggesting internal triggers for hibernation (9). This follows the final arousal from hibernation which has been mainly linked the androgen and sex hormone testosterone but also to temperature and light (2). Both hormones are of highest concentrations during final arousal in male arctic ground squirrels (15). This could explain the timing of mating, which occurs shortly after arousal from hibernation.


The process of hibernation involves pre-hibernation, maintenance, IBA and final arousal and allows animals to survive prolonged conditions of low temperature and food availability. Further understanding of the mechanisms will give insights into the possible correlation between internal and external stimuli on the behaviour of hibernators.


References

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  2. Melvin RG, Andrews MT. Torpor induction in mammals: recent discoveries fueling new ideas. Trends Endocrinol Metab. 2009;20(10):490–8.

  3. Körtner G, Geiser F. The temporal organization of daily torpor and hibernation: Circadian and circannual rhythms. Chronobiol Int. 2000;17(2):103–28.

  4. South KE, Haynes K, Jackson AC. Hibernation Patterns of the European Hedgehog, Erinaceus europaeus, at a Cornish Rescue Centre. Anim an open access J from MDPI. 2020 Aug 14;10(8):1418.

  5. Zatzman ML. Renal and cardiovascular effects of hibernation and hypothermia. Cryobiology. 1984;21(6):593–614.

  6. Epperson LE, Martin SL. Quantitative assessment of ground squirrel mRNA levels in multiple stages of hibernation. Physiol Genomics. 2002 Aug 14;10(2):93–102.

  7. Kronfeld-Schor N, Richardson C, Silvia BA, Kunz TH, Widmaier EP. Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. Am J Physiol Regul Integr Comp Physiol. 2000 Oct;279(4):R1277-81.

  8. Hampton M, Melvin RG, Andrews MT. Transcriptomic analysis of brown adipose tissue across the physiological extremes of natural hibernation. PLoS One. 2013;8(12):e85157.

  9. Strumwasser F. Factors in the pattern, timing and predictability of hibernation in the squirrel, Citellus beecheyi. Am J Physiol Content. 1958;196(1):8–14.

  10. Buck MJ, Squire TL, Andrews MT. Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genomics. 2002;8(1):5–13.

  11. Yan J, Burman A, Nichols C, Alila L, Showe LC, Showe MK, et al. Detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics. 2006;25(2):346–53.

  12. Dark J, Miller DR, Lewis DA, Fried SK, Bunkin D. Noradrenaline‐Induced Lipolysis in Adipose Tissue is Suppressed at Hibernation Temperatures in Ground Squirrels. J Neuroendocrinol.