Physiology of hibernation under the ice by turtles and frogs

Abstract

Successful overwintering under ice by an air-breathing vertebrate requires either effective aquatic respiration if dissolved O 2 is available or the capacity for prolonged anaerobic metabolism if O 2 supplies are limiting. Frogs can remain aerobic for many weeks when submerged at low temperature, even at water PO 2 as low as 30 mmHg, but are unable to survive even 1 week in anoxic water. Fuel reserves of hibernating frogs limit aerobic submergence, whereas acidosis may limit anoxic submergence. Freshwater turtles can also satisfy all or most of their O 2 needs in wellaerated water at low temperature by aquatic respiration, but certain species, in particular painted and snapping turtles, can also survive for up to 4-5 months without O 2 . Key adaptations of the painted turtles, and presumably snapping turtles, include metabolic depression and the exploitation of the shell and other bones to buffer lactic acid. As in frogs, glycogen and glucose are the only fuel sources during anoxia, and stores do not seem to be limiting in the painted turtle. Significant differences in anoxia tolerance exist among chelonian species that can be attributed, at least in part, to the magnitude of metabolic depression, the effectiveness of lactic acid buffering, and the size of glycogen stores.

No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates

“…Among the most robust of hypoxia-tolerant vertebrates is the freshwater turtle Trachemys scripta, which can withstand complete anoxia for days at room temperature to weeks in winter hibernation (Jackson and Ultsch, 2010); even at room temperature, 24 h of anoxia and re-oxygenation results in no evident loss of neurons…”

“…It may be present chronically, during the animal's entire life (naked mole-rats), on a seasonal basis (fresh-water turtles, hibernating ground squirrels) or during execution of particular behaviors necessary for survival (diving seals). It is hoped that consideration of the similarities and differences in how the brains of these different vertebrates cope with hypoxia will increase our appreciation of how nervous systems are adapted for life in specific ecological niches as well as inform advances in therapy for neurological conditions such as stroke and epilepsy.Down for the count: hypoxia tolerance in the freshwater turtle brainAmong the most robust of hypoxia-tolerant vertebrates is the freshwater turtle Trachemys scripta, which can withstand complete anoxia for days at room temperature to weeks in winter hibernation (Jackson and Ultsch, 2010); even at room temperature, 24 h of anoxia and re-oxygenation results in no evident loss of neurons …”

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

“…In Trachemys turtles, anoxia causes profound redistribution of blood flow to the most vital organs, including brain, heart and skeletal muscle, while the perfusion of lungs, gut and kidneys is drastically reduced (Stecyk et al, 2004). The shell, being essential for the buffering lactic acid in anoxia (Jackson and Ultsch, 2010), receives a large proportion of cardiac output in anoxic turtles (Stecyk et al, 2004). Conversely, it is possible that the high levels of circulating NO found here induce vasodilatation in specific tissues and hence sustain their perfusion during anoxia.…”

“…In contrast to mammals, where particularly the heart and brain are extremely sensitive to even brief periods of anoxia, freshwater turtles, including Trachemys scripta, survive weeks of anoxia during winter when submerged under icecovered ponds or several hours at room temperature (Ultsch and Jackson, 1982;Herbert and Jackson, 1985). This is achieved by a core of adaptations: (1) strong metabolic depression (whereby a reduced anaerobic energy supply is at balance with a reduced energy demand), (2) reorganization of blood flow to the most vital organs, (3) utilization of the shell calcium carbonate to buffer metabolic acidosis and high lactate levels, and (4) constitutively high levels of antioxidants, including thiols, that act as a redox buffer against reactive oxygen species generated at reoxygenation (Jackson, 2000;Hermes-Lima and Zenteno-Savín, 2002;Nilsson and Lutz, 2004;Bickler and Buck, 2007;Overgaard et al, 2007;Jackson and Ultsch, 2010). However, the molecular mechanisms underlying these extreme adaptive responses to low O 2 remain to be fully understood.…”

Cellular Basis for Learning Impairment in Fragile X Syndrome

“…Among the most robust of hypoxia-tolerant vertebrates is the freshwater turtle Trachemys scripta, which can withstand complete anoxia for days at room temperature to weeks in winter hibernation (Jackson and Ultsch, 2010); even at room temperature, 24 h of anoxia and re-oxygenation results in no evident loss of neurons No oxygen? No problem!…”