Non-Shivering Thermogenesis in Birds: A Role for Skeletal Muscle

Avian non-shivering thermogenesis (NST) is still a controversial topic. Empirical data collected in the past two decades have demonstrated that NST is potentially one of the mechanisms deployed by birds to modulate their thermoregulation. Their skeletal muscle expresses several features that qualify it to be the main tissue involved in such mechanism. Because birds lack brown adipose tissue, exclusively found in eutherian mammals, they have been inaccurately excluded from the orthodox definition for NST. However, birds possess a large muscle mass, represented particularly by their pectoral/flight muscles rich in mitochondria, endoplasmic/sarcoplasmic reticulum membranes, and blood capillary supply. Birds maintain higher resting body temperatures, around 41oC, than their mammalian counterparts, either monotremes and marsupials (around 34oC) or eutherians (around 37-39oC). Furthermore, many bird species are usually exposed to extremely low ambient temperatures during wintertime, and some bird species can become heterothermic when facing unfavorable environmental thermal conditions or food availability. With regards to the latter, some bird species may undergo daily torpor, lowering significantly their body temperatures to save energy. Thus, NST, at least theoretically if not effectively, would allow birds to face these challenges with lower energy expenditures than they would if they relied solely on the mechanical contraction of their skeletal muscles to generate the required additional heat to either keep their bodies warm in extreme cold weather conditions or warming them up during the rewarming phase of daily torpor. Mechanisms like the calcium leakage through the endoplasmic/sarcoplasmic reticulum and the proton leakage through the mitochondrial membranes, in the latter case by means of proteins, like the adenine nucleotide translocase (ANT) and the skeletal muscle uncoupling protein UCP2, are strong candidates as modulators of NST in birds.