Metabolic Flexibility: Hibernation, Torpor, and Estivation

Abstract

Many environmental conditions can constrain the ability of animals to obtain sufficient food energy, or transform that food energy into useful chemical forms. To survive extended periods under such conditions animals must suppress metabolic rate to conserve energy, water, or oxygen. Amongst small endotherms, this metabolic suppression is accompanied by and, in some cases, facilitated by a decrease in core body temperature-hibernation or daily torpor-though significant metabolic suppression can be achieved even with only modest cooling. Within some ectotherms, winter metabolic suppression exceeds the passive effects of cooling. During dry seasons, estivating ectotherms can reduce metabolism without changes in body temperature, conserving energy reserves, and reducing gas exchange and its inevitable loss of water vapor. This overview explores the similarities and differences of metabolic suppression among these states within adult animals (excluding developmental diapause), and integrates levels of organization from the whole animal to the genome, where possible. Several similarities among these states are highlighted, including patterns and regulation of metabolic balance, fuel use, and mitochondrial metabolism. Differences among models are also apparent, particularly in whether the metabolic suppression is intrinsic to the tissue or depends on the whole-animal response. While in these hypometabolic states, tissues from many animals are tolerant of hypoxia/anoxia, ischemia/reperfusion, and disuse. These natural models may, therefore, serve as valuable and instructive models for biomedical research.

The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

“…The ability of animals to face prolonged periods of food shortage is under strong natural selection (Geiser and Stawski, 2011;Lindstedt and Boyce, 1985;McCue, 2012;Millar and Hickling, 1990;Staples, 2016). Body reserves (i.e.…”

Effects of short and extended fasting periods and cattle breed on glycogenolysis, sarcomere shortening and Warner-Bratzler shear force

“…Some mammalian species have the ability to suppress the metabolic rate to conserve energy, water, or oxygen to survive extended periods of food restriction. This metabolic suppression is often accompanied by a decrease in core body temperature, that is, hibernation or daily torpor (Staples, 2016). Fujita et al (2013) identified a bovine hibernation-specific protein complex in Holstein non-pregnant cows that increased as soon as fasting commenced.…”

A radical shift in perspective: mitochondria as regulators of reactive oxygen species

“…Mitochondrial substrate oxidation capacity is markedly decreased, especially for succinate but also with NADH-linked substrates, during the torpor phase of hibernation (Staples, 2014(Staples, , 2016. As discussed above, a decrease in mitochondrial capacity for substrate oxidation may affect the production of H 2 O 2 more than the pathways for its consumption, thereby decreasing [H 2 O 2 ] ss .…”

“…As discussed above, a decrease in mitochondrial capacity for substrate oxidation may affect the production of H 2 O 2 more than the pathways for its consumption, thereby decreasing [H 2 O 2 ] ss . However, there are indications that proteomic and allosteric regulation of mitochondrial substrate oxidation may form part of the adaptation to torpor (reviewed in Staples, 2014Staples, , 2016. Posttranslational modifications such as glutathionylation may decrease enzymatic flux and, at the same time, either decrease or increase ROS production as seen with complex I and II, respectively (reviewed in Mailloux and Treberg, 2016).…”