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First published online July 26, 2004
Journal of Experimental Biology 207, 2897-2906 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01123

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

Gary C. Packard^* and Mary J. Packard

Department of Biology, Colorado State University, Fort Collins, CO 80523-1878, USA

View larger version (24K): [in a new window]   Fig. 1. Temperature profiles for representative nests at our study site in north-central Nebraska. Both nests contained eight painted turtles that were hatched in the laboratory and then placed into the nests in late October. (A) A relatively warm nest; (B) a relatively cold nest. The broken horizontal lines mark the equilibrium freezing point for bodily fluids of hatchlings (Storey et al., 1991; Packard and Packard, 1995; Costanzo et al., 2000b). Animals in this study hatched on substrates of vermiculite and consequently had a somewhat greater capacity for supercooling than turtles hatching in the field (Packard et al., 2001). Data are from Packard et al. (1997a).

View larger version (12K): [in a new window]   Fig. 2. Hatchling painted turtles were inoculated with ice at temperatures only slightly below the equilibrium freezing point for bodily fluids (approx. -0.7°C). After the animals had frozen to a thermal equilibrium at -2°C, they were exposed for varying periods to temperatures between -2 and -4°C (as indicated by lines representing the different temperature profiles). Samples were removed at times designated by arrows, and the turtles were allowed to thaw slowly. The number to the left of each solidus is the number of survivors; the number to the right of each solidus is the sample size. Data are from Packard et al. (1999b) and Packard and Packard (in press).

View larger version (11K): [in a new window]   Fig. 3. Values for the limit of supercooling for individual painted turtles collected at our field site in north-central Nebraska in September (four hatchlings from each of three clutches) and November (four hatchlings from each of four clutches). The turtles were placed into the experimental protocol the day after they were removed from the nests in which they completed incubation and hatched. The distribution of values for animals studied in September differs from that for turtles studied in November (Wilcoxon two-sample test, z=3.86, P<0.001). Data are from Packard et al. (2001).

View larger version (13K): [in a new window]   Fig. 4. Values for the limit of supercooling for individual painted turtles that hatched from eggs incubated on natural soil in the laboratory. Unacclimated animals were studied within days of the time they hatched; animals in the high acclimation group were held at 24°C for 6 weeks; turtles in the low acclimation groups were acclimated to 3°C over periods of 6 weeks and 15 weeks. The distribution of values for unacclimated animals differs from the distribution for turtles acclimated at high temperature (Wilcoxon two-sample test, z=4.87, P<0.001), and the distribution for the latter differs from that for hatchlings acclimated at low temperature for 6 weeks (Wilcoxon two-sample test, z=5.40, P<0.001). Data are from Packard and Packard (2003c).

View larger version (15K): [in a new window]   Fig. 5. The risk to hatchling painted turtles of freezing by inoculation was assessed in animals that had just completed incubation at 27°C (unacclimated) and in neonates that were acclimated at a high temperature (24°C) or a low temperature (3°C). Turtles were placed individually into artificial nests where they came into intimate contact with moist soil. Water in the soil first was caused to freeze at a temperature above the equilibrium freezing point for bodily fluids of hatchlings, so turtles came into contact with ice before they were susceptible to freezing. Temperature then was lowered to -2°C, which is above the temperature at which hatchlings freeze spontaneously by heterogeneous nucleation, and this temperature was maintained for 7 days. Spikes (exotherms) in the temperature profiles yielded evidence for freezing by the turtles themselves. A malfunction of an environmental chamber caused background noise to be extraordinarily high in temperature profiles for unacclimated turtles, and some freezing exotherms consequently may have escaped detection. Indeed, all the animals for which no exotherm was detected (hatched bar in left column) are thought to have frozen. Letters displayed in italics above the bars are from one statistical analysis, and those within the bars are from another. Bars that share a letter from the same analysis cannot be distinguished statistically. Figure reproduced from Packard and Packard (2003b).

View larger version (16K): [in a new window]   Fig. 6. Straight lines fit to the displayed values for total lactate in bodies of supercooled hatchlings of the painted turtle describe rates of accumulation of this metabolic end-product at 0°C (), -4°C () or -8°C (). Animals that were held for 25 days at -8°C () were probably dead at the point in time when they were sampled, so data for these turtles were not used in computing the regression line for that temperature. The regression lines, which were forced through the origin, have the following equations: lactate at 0°C=0.035 mgxday; lactate at -4°C=0.306 mgxday; lactate at -8°C=1.462 mgxday. Figure reproduced from Hartley et al. (2000).