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

Abstract

SUMMARY 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.

Hatching behavior of eastern long-necked turtles ( Chelodina longicollis ): The influence of asynchronous environments on embryonic heart rate and phenotype

“…It is not known how C. longicollis and E. macquarii accelerate development, but heart rates are not fixed and environmental conditions merely determine the limits of heart rate and thus developmental rate (McGlashan et al, 2012;Loudon et al, 2013). Synchronous hatching has evolved in many aquatic turtles with many abiotic and biotic factors serving as the cues (Webb et al, 1986;Thompson, 1989;Lindeman, 1991;Packard et al, 1997;Doody et al, 2001;Spencer et al, 2001;Packard and Packard, 2004;Tucker et al, 2008;Colbert et al, 2010;Spencer and Janzen, 2011). Synchronous hatching is not a passive action, it is driven by embryo-embryo communication in the nest.…”

Do current environmental conditions explain physiological and metabolic responses of subterranean crustaceans to cold?

“…Cold exposure is well known to induce aerobic metabolism perturbations (Hochachka and Somero, 2002), resulting in a decrease in ATP production. Thus, some organisms have to use anaerobic means for some portion of their energy needs (Costanzo et al, 2004;Hartley et al, 2000;Packard and Packard, 2004). However, the energetic yield of aerobic metabolism is largely superior to that of anaerobic metabolism (Hochachka and Somero, 2002).…”

Potential sources of intra-population variation in painted turtle (Chrysemys picta) hatchling overwintering strategy

“…Winter oxygen concentration in nests was consistently similar to the oxygen concentration of air (21.0% oxygen); thus, gas exchange is probably not a challenge to terrestrially overwintering hatchling turtles that breathe with their lungs. In contrast, gas exchange in aquatic sites presents a challenge during winter, especially because hatchlings have a lower anoxia tolerance compared to adults (Packard and Packard, 2004;Reese et al, 2004), and must rely on less-efficient cutaneous routes of gas exchange. Lower anoxia tolerance in hatchlings may itself be a driving factor in the prevalence of terrestrial overwintering by hatchling turtles (Gibbons, 2013).…”

“…Mean, minimum and maximum nest temperatures, as well as the amount of time a nest spent below −0.6°C (freezing point of body fluids for hatchlings) (Packard and Packard, 2004) and −4°C (lower limit for freeze ( tolerance) (Storey et al, 1988) from October until April was calculated to understand the nest environment to which hatchlings were exposed.…”