Natural freeze tolerance in the terrestrial turtle, <i>Terrapene carolina</i>

Costanzo, Jon P.; Claussen, Dennis L.

doi:10.1002/jez.1402540215

Cited by 51 publications

(16 citation statements)

References 13 publications

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“…However, contrary to our expectation (based on Neill 1948, Carpenter 1957, our analysis revealed that minimum winter temperature was negatively related to survival. This may be explained by the fact that box turtles are well adapted to low winter temperatures, both in their ability to burrow deep in the soil (Carpenter 1957, Doroff and Keith 1990, Converse et al 2002, and in their ability to tolerate freezing temperatures (Costanzo and Claussen 1990, Doroff and Keith 1990, Costanzo et al 1993. Warmer temperatures would result in higher metabolic DEMOGRAPHICS OF ORNATE BOX TURTLES rates in overwintering turtles, which in turn could deplete lipid reserves to levels from which some turtles could not recover.…”

Section: Discussionmentioning

confidence: 99%

Demographics of an Ornate Box Turtle Population Experiencing Minimal Human-Induced Disturbances

Converse

Iverson

Savidge

2005

Ecological Applications

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Human‐induced disturbances may threaten the viability of many turtle populations, including populations of North American box turtles. Evaluation of the potential impacts of these disturbances can be aided by long‐term studies of populations subject to minimal human activity. In such a population of ornate box turtles (Terrapene ornata ornata) in western Nebraska, we examined survival rates and population growth rates from 1981–2000 based on mark–recapture data. The average annual apparent survival rate of adult males was 0.883 (se = 0.021) and of adult females was 0.932 (se = 0.014). Minimum winter temperature was the best of five climate variables as a predictor of adult survival. Survival rates were highest in years with low minimum winter temperatures, suggesting that global warming may result in declining survival. We estimated an average adult population growth rate (λ^) of 1.006 (se = 0.065), with an estimated temporal process variance (σ^2) of 0.029 (95% ci = 0.005–0.176). Stochastic simulations suggest that this mean and temporal process variance would result in a 58% probability of a population decrease over a 20‐year period. This research provides evidence that, unless unknown density‐dependent mechanisms are operating in the adult age class, significant human disturbances, such as commercial harvest or turtle mortality on roads, represent a potential risk to box turtle populations.

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Section: Discussionmentioning

confidence: 99%

Demographics of an Ornate Box Turtle Population Experiencing Minimal Human-Induced Disturbances

Converse

Iverson

Savidge

2005

Ecological Applications

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“…Other members of the Emydidne (..g., C. picta, Terrapene corolina, and Terrapene ornata), whose center of geographic distribution is at a higher latitude than that of any other turtle family (Conant and Clollins 1991: Ernst et al 1994'. Holman and Andrews 1994, are adapted to tolerate the freezing of their tissues (Storey et al 1988;Costanzo and Claussen 1990;Costanzo et al 1995), but the freeze-tolerance status of spotted turtles is as yet untested. Frseze-tolerance is not necessarily required for survival at northern latitudcs, because the Zo values for northern C. serpentina, a freeze-intolerant species, were also very low (range 0-4"C; Brown and Brooks 1994).…”

Section: Discussionmentioning

confidence: 99%

Phenology and ecology of hibernation in spotted turtles (Clemmys guttata) near the northern limit of their range

Litzgus¹,

Costanzo²,

Brooks³

et al. 1999

Can. J. Zool.

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Using mark-recapture techniques, temperature-sensitive radio transmitters, and miniature temperature data loggers we investigated the hibernation ecology of northern temperate zone spotted turtles (Clemmys guttata) in Georgian Bay, Ontario, over 4 winters (1993-1997). We observed 18 hibernacula that were occupied by 34 turtles; 11 hibernacula were apparently occupied by single turtles, and 7 were used communally by up to 9 individuals. Hibernacula were located in swamps and were of 2 types: sphagnum moss hummock (n = 15) and rock cavern (n = 3). Almost half of the individuals (16 of 34) used the same hibernaculum in at least 2 winters. Turtles entered hibernacula between mid-September and October, when their body temperature was between 12 and 16°C, and exited them in mid to late April, when ambient temperatures ranged between 1 and 5°C. A waterproof temperature data logger attached to a turtle indicated that this turtle was protected from freezing in a thermally stable hibernaculum (body temperature range 0.3-3.9°C) despite highly variable (a 37°C change over 5 days) and low air temperatures (minimum -35°C). Loss of body mass (2%) during hibernation was not significant. We observed no mortality within hibernacula over the 4 winters; however, 3 turtles were destroyed by predators near the hibernacula. These data provide insight into the role of climate in limiting the northern distribution of this species.

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“…Accordingly, they are one of the few adult turtles shown to have some degree of freeze tolerance. Turtles from Ohio recovered from freezing in laboratory studies at a T b as low as x3.6 xC for up to 3-4 days, during which 44-58% of the body water froze (Costanzo & Claussen, 1990 ;Costanzo, Lee & Wright, 1993;Storey et al, 1993). Whether hibernating eastern box turtles use either slight supercooling or freeze tolerance naturally has yet to be demonstrated, but either could come into play during winters with exceptionally cold spells coupled with lack of snow cover for insulation, or perhaps during periods in spring when emerged turtles are threatened with sudden cold snaps.…”

Section: (4 ) Eastern Box Turtle (Terrapene Carolina)mentioning

confidence: 99%

The ecology of overwintering among turtles: where turtles overwinter and its consequences

2006

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Turtles are a small taxon that has nevertheless attracted much attention from biologists for centuries. However, a major portion of their life cycle has received relatively little attention until recently - namely what turtles are doing, and how they are doing it, during the winter. In the northern parts of their ranges in North America, turtles may spend more than half of their lives in an overwintering state. In this review, I emphasise the ecological aspects of overwintering among turtles, and consider how overwintering stresses affect the physiology, behaviour, distributions, and life histories of various species. Sea turtles are the only group of turtles that migrate extensively, and can therefore avoid northern winters. Nevertheless, each year a number of turtles, largely juveniles, are killed when trapped by cold fronts before they move to safer waters. Evidently this risk is an acceptable trade-off for the benefits to a population of inhabiting northern developmental habitats during the summer. Terrestrial turtles pass the winter underground, either in burrows that they excavate or that are preformed. These refugia must provide protection against desiccation and lethal freezing levels. Some burrows are extensive (tortoise genus Gopherus), while others are shallow, or the turtles may simply dig into the ground to a safe depth (turtle genus Terrapene). In the latter genus, freeze tolerance may play an adaptive role. Most non-marine aquatic turtles overwinter underwater, although Clemmys (Actinemys) marmorata routinely overwinters on land when it occurs in riverine habitats, Kinosternon subrubrum often overwinters on land, and several others may overwinter terrestrially on occasion, especially in more southern climates. For northern species that overwinter underwater, there are two physiological groupings, those that are anoxia-tolerant and those that are relatively anoxia-intolerant. All species fare well physiologically in water with a high partial pressure of oxygen (PO2). A lack of anoxia tolerance limits the types of habitats that a freshwater turtle may live in, since unlike sea turtles, they cannot travel long distances to hibernate. Hatchlings of some species of turtles spend their first winter in or below the nest cavity, while hatchlings of other species in the same area, including northern areas, emerge in the autumn and presumably hibernate underwater. All hatchlings are relatively anoxia-intolerant, and there are no studies to date of where hatchling turtles that do not overwinter in or below the nest cavity spend their first winter. Equally little is known of the ontogeny of anoxia tolerance, other than that adults of all species are more anoxia-tolerant than their hatchlings, probably because of their better ossified shells, which provide adults with more buffer reserves and a larger site in which to sequester lactate. The northern limits of turtles are most likely determined by reproductive limitations (time for egg-laying, incubation, and hatching) than by the rigors of hibernation. Mortalit...

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Natural freeze tolerance in the terrestrial turtle, Terrapene carolina

Cited by 51 publications

References 13 publications

Demographics of an Ornate Box Turtle Population Experiencing Minimal Human-Induced Disturbances

Demographics of an Ornate Box Turtle Population Experiencing Minimal Human-Induced Disturbances

Phenology and ecology of hibernation in spotted turtles (Clemmys guttata) near the northern limit of their range

The ecology of overwintering among turtles: where turtles overwinter and its consequences

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