To freeze or not to freeze: adaptations for overwintering by hatchlings of the North American painted turtle

Abstract

Many physiologists believe that hatchling painted turtles (Chrysemys picta) provide a remarkable, and possibly unique, example of 'natural freeze-tolerance' in an amniotic vertebrate. However, the concept of natural freeze-tolerance in neonatal painted turtles is based on results from laboratory studies that were not placed in an appropriate ecological context, so the concept is suspect. Indeed, the weight of current evidence indicates that hatchlings overwintering in the field typically withstand exposure to ice and cold by avoiding freezing altogether and that they do so without benefit of an antifreeze to depress the equilibrium freezing point for bodily fluids. As autumn turns to winter, turtles remove active nucleating agents from bodily fluids (including bladder and gut), and their integument becomes a highly efficient barrier to the penetration of ice into body compartments from frozen soil. In the absence of a nucleating agent or a crystal of ice to 'catalyze' the transformation of water from liquid to solid, the bodily fluids remain in a supercooled, liquid state. The supercooled animals nonetheless face physiological challenges, most notably an increased reliance on anaerobic metabolism as the circulatory system first is inhibited and then caused to shut down by declining temperature. Alterations in acid/base status resulting from the accumulation of lactic acid may limit survival by supercooled turtles, and sublethal accumulations of lactate may affect behavior of turtles after the ground thaws in the spring. The interactions among temperature, circulatory function, metabolism (both aerobic and anaerobic), acid/base balance and behavior are fertile areas for future research on hatchlings of this model species.