The role of the integument as a barrier to penetration of ice into overwintering hatchlings of the painted turtle (Chrysemys picta)

Abstract

Hatchlings of the North American painted turtle (Chrysemys picta) spend their first winter of life inside a shallow, subterranean hibernaculum (the natal nest) where they may be exposed for extended periods to ice and cold. Hatchlings seemingly survive exposure to such conditions by becoming supercooled (i.e., by remaining unfrozen at temperatures below the equilibrium freezing point for body fluids), so we investigated the role of their integument in preventing ice from penetrating into body compartments from surrounding soil. We first showed that hatchlings whose epidermis has been damaged are more likely to be penetrated by growing crystals of ice than are turtles whose cutaneous barrier is intact. We next studied integument from a forelimb by light microscopy and discovered that the basal part of the α‐keratin layer of the epidermis contains a dense layer of lipid. Skin from the forelimb of other neonatal turtles lacks such a layer of lipid in the epidermis, and these other turtles also are highly susceptible to inoculative freezing. Moreover, epidermis from the neck of hatchling painted turtles lacks the lipid layer, and this region of the skin is readily penetrated by growing crystals of ice. We therefore conclude that the resistance to inoculation imposed by skin on the limbs of hatchling painted turtles results from the presence of lipids in the α‐keratin layer of the epidermis. Neonates apparently are able to avoid freezing during winter by drawing much of the body inside the shell, leaving only the ice‐resistant integument of the limbs exposed to ice in the environment. The combination of behavior and skin morphology enables overwintering hatchlings to exploit an adaptive strategy based on supercooling. J. Morphol. 246:150–159, 2000 © 2000 Wiley‐Liss, Inc.

Low Temperature Dormancy Affects the Quantity and Quality of the Female Sexual Attractiveness Pheromone in Red-sided Garter Snakes

“…The pheromone of red-sided garter snakes may be similarly derived. First, the skin may increase its lipid production to retard transcutaneous water loss during low temperature dormancy, which is a common process in sauropsids during cold acclimation (e.g., turtles, Willard et al 2000;pigeons, Peltonen et al 2000). Second, as is the case in mallards, the lipids would be modified by enzymes that are activated by cold temperatures.…”

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

“…Evidence supporting this idea comes from several experiments demonstrating that neonates whose body surface makes intimate contact with wet soil seldom are inoculated when water in the soil subsequently freezes (Packard and Packard, 1993a,b, 1995, 2003aPackard et al, 1997bPackard et al, , 1999a. Moreover, damage to the integument greatly increases the risk of freezing by hatchlings (Willard et al, 2000), presumably by providing a pathway for ice to grow through what is otherwise a highly resistant barrier. It is noteworthy, however, that the integument affords little resistance to the penetration of ice into turtles in the days immediately after hatching (Costanzo et al, 2000b;Packard and Packard, 2003b), at which time neonates are highly susceptible to freezing by inoculation (Fig.·5).…”

“…The 'bricks' in the stratum corneum of mammalian epidermis are the corneocytes, and the 'mortar' is the lipid occupying the intercellular domain (Elias, 1983;Elias and Menon, 1991;Menon and Ghadially, 1997). Moreover, lipids in the extracellular matrix of mammalian stratum corneum limit the loss of water from body compartments to the surrounding atmosphere (Elias and Friend, 1975;Grubauer et al, 1989;Elias and Feingold, 1992), whereas lipids in the α-keratin layer of flexible skin from exposed surfaces of neonatal painted turtles seemingly resist the penetration of ice crystals into body compartments from frozen soil (Willard et al, 2000). The parallels in structure and function between flexible skin of turtles and the integument of mammals are apparent.…”

“…The α-keratin layer of skin from exposed surfaces of the forelimbs, for instance, has dense deposits of lipid in the inner domain whereas the α-keratin layer of integument from more protected sites at the base of the neck lacks such deposits (Willard et al, 2000). The exposed sites on the forelimbs are suspected to be resistant to inoculation while skin at the base of the neck and limbs is thought to be penetrated more readily by crystals of ice (Packard and Packard, 1995).…”

“…Moreover, even when temperatures in nests are sufficiently benign that hatchlings could conceivably survive a short bout of freezing (e.g. Nagle et al, 2000;Costanzo et al, 2004), the turtles are unlikely to be frozen Packard, 1995, 2003a,b;Willard et al, 2000) for reasons detailed below.…”