Hibernation in the eastern box turtle, Terrapene c. carolina

Sub-zero winter air temperatures are common throughout much of the geographic range of Terrapene c. carolina. To examine the consequences of such conditions, we monitored microhabitat and body temperatures of box turtles in southwestern Ohio over three hibernal seasons. A simulated hibernaculum was constructed and monitored over three seasons to further explore the potential exposure of these turtles to freezing conditions. We obtained multi-year field data for three turtles and single-season data for seven others. All of our turtles hibernated in the woods and all survived hibernation. The depth of hibernacula beneath the soil was variable but never exceeded 14 cm, and averaged only 4-5 cm. The amount of leaf litter varied, but averaged about 8 cm. Snow cover was uncommon, sparse, and ephemeral. The duration of hibernation averaged 142 d and showed no significant annual variation. Some turtles moved to a new hibernation site early or late in the hibernal season, but most did not. The weather pattern varied from year to year, but no winter was atypically severe. Body temperatures approximated, but were sometimes lower than, adjacent soil temperatures. In spite of the considerable insulation provided by the cover of leaf litter, some box turtles experienced body temperatures of -0.3 C or below during each winter of our study. Although freezing can be a significant contributor to winter mortality, these composite data suggest that body freezing is neither a rare nor necessarily a lethal event in the life history of T. carolina. al of Herpetology, Vol. 25, No. 3, pp. 3 -341, 991 ight 1 91 Society for the Study of Amphibians and Reptiles ation in the Eastern Box Turtle, Terrapene c. carolina IS L. CLAU SEN, PAUL M. DANIEL, SUPING JIANG, The eastern box turtle, Terrapene c. carolina, is among the most common terrestrial reptiles in the eastern United States. Its range extends south to southern Georgia and north to southern New Hampshire in the east, and to northern Michigan in the west (Conant, 1975). Sub-zero winter temperatures are common throughout much of this geographic area. Eastern box turtles typically overwinter by burrowing into woodland soil beneath a cover of leaf litter. The burrows are usually shallow. The top of the carapace is often initially nearly flush with the soil surface; however, the turtles will frequently burrow deeper as the weather becomes colder (Carpenter, 1957; Dolbeer, 1971). The surrounding soil, with its associated cover of leaves and (sometimes) snow, provides considerable protection from low air temperatures (Reagan, 1974). Some individuals resume surface activity in the winter after their initial entry into hibernation, and they may even move from one hibernation site to another (Allard, 1935; Carpenter, 1957; Dolbeer, 1971; Congdon et al., 1989). The shallowness of their burrows is surprising, since they are capable of more extensive excavations (Allard, 1948). Box turtles also may leave their hibernacula in the spring well before the last frost. Hibernation is a critical period in the biology of box turtles (Schwartz et al., 1984). Winter cold appears to be the primary natural cause of box turtle death (Neill, 1948; Schwartz and Schwartz, 1974) and specific examples of presumed freezing-induced mortality have been reported (Cahn, 1933; Allard, 1935, 1948). These and other anecdotal reports suggested that body freezing is necessarily lethal for box turtles. Legler (1960), however, demonstrated that thermal gradients exist with the body of a cooling turtle, and he hypothesized that some portions of the animal might freeze without causing death. Costanzo and Claussen (1990) confirmed the existence of substantial thermal gradients and demonstrated that T. carolina is, in fact, remarkably tolerant of body freezing. This species thus joi s the short list of vertebrates now known al., 1989). The shallowness of their burrows surprising, since they are capable of more ensive excavations (Allard, 1948). Box turtles ay leave their hibernacula in the spring 334 This content downloaded from 157.55.39.186 on Tue, 11 Oct 2016 04:22:37 UTC All use subject to http://about.jstor.org/terms HIBERNATION IN BOX TURTLES to be capable of withstanding the freezing of a substantial portion of their body fluid (see Claussen et al., 1990 for a recent review). Here we present data on the winter biology of this reptile and document the thermal conditions encountered by hibernating box turtles. We hypothesized that the turtles would not uncommonly experience body temperatures low enough to promote the formation of body ice, at least in southwestern Ohio, where winter temperatures are often severe, yet snow cover sparse. MATERIALS AND METHODS Miami-Whitewater Forest Study.-We conducted this study from the fall of 1986 through the spring of 1989 at the Braille Trail Area within Miami-Whitewater Forest in Hamilton County, Ohio. The study site, which included both grassland (mowed on a three-year cycle) and woodland habitats, was visited 41 times during the hibernal season (late October through early April) over a three year period. For purposes of simplicity, we will equate the terms "winter" and "hibernal season" in the discussion to follow. Six turtles were captured in the study area and taken to the laboratory overnight for mounting of Model L Mini-Mitter radio-transmitters (see Adams et al., 1989). Before mounting, the temperature-sensitive transmitters were calibrated in a series of water baths of known temperature. After cold-anesthetizing each turtle, we drilled a hole of approximately 3 mm diameter through the seventh lateral scute from the front on the right side of the animal. The probe of a transmitter was then inserted approximately 1.5 cm through this hole in the carapace into the peritoneal cavity of the turtle. The turtle was then restrained with strapping tape and the transmitters, waterproofed and fitted into a clear plastic tube, were secured to its posterior carapace with fiberglass, which also sealed the carapace hole. All turtles were released within 24 h at the site of capture. Two box turtles were monitored for three, and a third turtle for two consecutive years. We have data for only one hibernal season for all other individuals. We used a directional antenna and receiver to locate these animals at 7-14 d intervals. Animals buried in the soil under a cover of leaf litter were assumed to be in hibernation. Once an animal was located, we noted its behavior and, if it was in hibernation, we noted the depth of the cover of leaf litter and the distance from the top of the carapace to the soil surface. The number of transmitter clicks per 100 sec was recorded and these data were later converted to body temperatures. A hand-held thermocouTturtle (ave.) Tturtle Tair I Tsb-leaf Tentrance Tsub-leaf