Hibernation and Gas Exchange

Abstract

Hibernation in endotherms and ectotherms is characterized by an energy-conserving metabolic depression due to low body temperatures and poorly understood temperature-independent mechanisms. Rates of gas exchange are correspondly reduced. In hibernating mammals, ventilation falls even more than metabolic rate leading to a relative respiratory acidosis that may contribute to metabolic depression. Breathing in some mammals becomes episodic and in some small mammals significant apneic gas exchange may occur by passive diffusion via airways or skin. In ectothermic vertebrates, extrapulmonary gas exchange predominates and in reptiles and amphibians hibernating underwater accounts for all gas exchange. In aerated water diffusive exchange permits amphibians and many species of turtles to remain fully aerobic, but hypoxic conditions can challenge many of these animals. Oxygen uptake into blood in both endotherms and ectotherms is enhanced by increased affinity of hemoglobin for O₂ at low temperature. Regulation of gas exchange in hibernating mammals is predominately linked to CO₂/pH, and in episodic breathers, control is principally directed at the duration of the apneic period. Control in submerged hibernating ectotherms is poorly understood, although skin-diffusing capacity may increase under hypoxic conditions. In aerated water blood pH of frogs and turtles either adheres to alphastat regulation (pH ∼8.0) or may even exhibit respiratory alkalosis. Arousal in hibernating mammals leads to restoration of euthermic temperature, metabolic rate, and gas exchange and occurs periodically even as ambient temperatures remain low, whereas body temperature, metabolic rate, and gas exchange of hibernating ectotherms are tightly linked to ambient temperature.

Hemoglobin function and allosteric regulation in semi-fossorial rodents (family Sciuridae) with different altitudinal ranges

“…In mountain ranges of western North America, burrow-dwelling rodents in the squirrel family (Sciuridae) are common denizens of the alpine and subalpine zones, most notably the golden-mantled ground squirrel (Callospermophilus lateralis) and the yellow-bellied marmot (Marmota flaviventris), which occur at the highest possible elevations in the contiguous United States (Armstrong, 1972;Chappell and Dlugosz, 2009). In addition to the hypoxic challenges associated with life underground and life at high altitude, many sciurid rodents face additional gas transport challenges associated with depressed ventilation and episodic breathing during winter hibernation (Milsom, 1992;Milsom and Jackson, 2011;Webb and Milsom, 1994). In hibernating ground squirrels, prolonged periods of apnea can result in wide fluctuations in arterial P O2 and plasma pH (Maginniss and Milsom, 1994;Malan et al, 1973;Musacchia and Volkert, 1971).…”

“…Likewise, in hibernating mammals, a left-shifted blood-O 2 equilibrium curve can help safeguard arterial O 2 saturation during apneic periods and prevent unfavorable O 2 release to tissues (Maginniss and Milsom, 1994;Milsom and Jackson, 2011;Revsbech et al, 2013). An increase in blood-O 2 affinity can be achieved by changes in the intrinsic O 2 affinity of hemoglobin (Hb), changes in the sensitivity of Hb to allosteric effectors and/or changes in the concentrations of allosteric effectors within the erythrocyte.…”

Decrease in the red cell cofactor 2,3-diphosphoglycerate increases hemoglobin oxygen affinity in the hibernating brown bearUrsus arctos

“…In spite of substantial downregulation of ventilation and heart rate, most hibernators likely experience only slight or no hypoxia and in some ground squirrels arterial O 2 tension (PO 2 ) is normal during torpor (16). As opposed to smaller hibernators that exhibit periods of spontaneous arousals back to normothermic temperature and metabolic rate (33,31), bears do not arouse to normothermic temperature during winter but have shallow multiday cyclic (1.6 -7.3 days) fluctuations in body temperature (43). Nevertheless, as demonstrated in a recent study (43), bears exhibit a strong active aerobic metabolic depression and a weight-specific metabolic rate similar to that of smaller hibernators (20,25,43), and for this reason, they are now recognized as true hibernators, even though they do not show the dramatic drop in body temperature and arousals typical of small hibernators (43).…”

Changes in the cerebellar cytoarchitecture of hibernating hedgehogErinaceus europaeusL. (Mammalia): an immunocytochemical approach

“…Previous experimental data demonstrated peculiar neurotransmitter characteristics typical of different brain regions. Indeed, it has to be considered that in hibernating species, some neurons generate and conduct impulses and initiate synaptic transmission at the low temperature associated with deep torpor, albeit with reduced capacities (Harris & Milsom 1995;Milsom & Jackson 2011). On the other hand, recent studies in hamster demonstrated that during the torpor phase of hibernation several metabolites, i.e.…”