Torpor and Other Physiological Adaptations of the Badger (Taxidea taxus) to Cold Environments

Oxygen consumption (V̇o2) and heart rate were measured at ambient temperatures between +20 and −40 C. Basal metabolic rate was 0.3 cm³/g·h (65 beats/min), the body temperature was 38 C, the lower critical temperature (Tlc) was 10 C, and conductance was 0.01225 cm³/g·h°C. Fat composition of 79 adult badgers captured during the winter showed maximal fat deposition of 31% body weight in November. Fat stores were reduced 37% between November and March. The burrow temperature remained between 0 and 4 C throughout the winter. Badgers in outdoor enclosures during the winter of 1977–1978 reduced their above-ground exposure by 93% from November through February. Two badgers remained below ground for more than 70 consecutive days during the 1978-1979 winter. While below ground, one telemetered badger entered a state of torpor, on 30 occasions, characterized by a 50% reduction in heart rate (from 55 to 25 beats/min) and a 9 C reduction in body temperature (from 38 to 29 C). The torpor cycle lasted an average of 29 h (entrance-15 h, torpor-8 h, arousal-6 h). Each cycle provided a 27% or 81 kcal/cycle reduction in energy expenditure.


INTRODUCTION
Many temperate-zone mammals exhibit both behavioral and physiological adaptations to cold. One of the most effective behavioral mechanisms is to avoid extreme cold through the use of a burrow or den (Pruitt 1960;Vose and Dunlap 1968;Stephenson 1969;Brocke 1970). Reliance on a fossorial shelter may be reflected in an animal's quality of thermal insulation, its ability to lower its metabolic requirements through hypothermia, and its dependence upon fat storage during winter. The badger, Taxidea taxus, is a semifossorial mammal that remains below the ground for extended periods during midwinter in response to cold (Harlow 1979a). McNab (1966) reported that fossorial rodents tend to have higher conductance (the reciprocal of insulation) than predicted by standard formulas. This same characteristic may be reflected by the badger. A high thermal conductance may restrict the badger's exposure to cold and consequent predatory activity during the winter, causing an increased reliance on fat reserves. In addition, the badger is an opportunistic feeder which relies primarily on small mammals, which may be more difficult to obtain during the winter (Lampe 1976). Badgers which are restricted to a winter den because of food shortage and cold may, therefore, have to reduce their energy requirements for activity and maintenance of body temperature (Mrosovsky 1976) in order to conserve fat stores. Morrison (1960) stated that fat reserves in mammals within the size range of badgers would not be sufficient to sustain these animals over a winter season without a 267 substantial reduction in metabolism. However, he also suggested that there is little need for extensive hypothermia in mammals of this size because of their relatively large body mass and fat reserves. Bears, Ursus sp. (Nelson 1973;Folk 1974), the opossum, Didelphis marsupialis (Brocke 1970), and the European badger, Meles meles (Slonin 1952;Johansson 1957) are known to exhibit signs of torpor. It is possible that the American badger also has the ability to lower its body temperature and metabolic requirements during the winter while beneath the ground and thereby conserve energy.
It is, therefore, the purpose of this study to investigate the badger's (1) winter activity and behavioral avoidance of cold temperatures, (2) thermal insulation, (3) seasonal fat utilization, and (4) energy requirements during the winter in order to understand the badger's adaptations to conditions of cold and food scarcity.

EXPERIMENTAL ANIMALS
Badgers were collected in Albany County, Wyoming, during the summers of 1977 and 1978 and maintained either in outdoor enclosures or in rooms exposed to outside temperature and photoperiod. Only female badgers weighing between 7.5 and 9.5 kg were used in this study. They were fed Purina Dog Chow consisting of 21%, 8%, and 4.51% crude protein, fat, and fiber, reslpectively, and with a gross energy content of 5.15 kcal/g.

RESPONSE TO COLD TEMPERATURES
Oxygen consumption (Vo,) on six badgers was derived from the changes in composition of a measured flow of air through a 50liter respirometer. Rate of flow was measured with a Datametrics model 800-L hot wire anemometer and maintained at 6 liters/min. A portion of this air, scrubbed of CO2 and water, was measured for oxygen content with a Beckman M-3 paramagnetic oxygen analyzer, and Vo, was calculated from formula number 10 of Depocas and Hart (1957). Oxygen consumption was determined between 1600 and 2200 MST at 10 C increments between +20 and -40 C on animals previously fasted for 16 h. The lower critical temperature (T1e) was determined by the method of Welch (1978) from the intersection of regression lines representing Vo, at different ambient temperatures. Thermal conductance was obtained from the slope of the regression line representing o0, at temperatures below the T1,. Values obtained by this method were within 5% of those obtained from a chloroform/ methanol extraction of whole carcasses.
The right femur was removed from each carcass, weighed to 0.001 g, and broken into shards. The shards were placed into a 30-ml Teflon centrifuge tube which contained a grid platform constructed so that the shards were supported over 5 ml of a chloroform/ methanol (2:1) solution. When the shards were spun at 800 X g for 15 min, virtually all marrow fat was removed from the femur and dissolved in the solution. Fat content of the bone marrow was then determined by evaporating the chloroform/methanol solution and weighing the fat residue to 0.001 g.

MEASUREMENT
Telemetry transmitters for heart rate and body temperature were developed (Weeks et al. 1978) and surgically implanted into the peritoneal cavities of badgers during the winter of 1977-1978 and again in the winter of 1978-1979. Stainless-steel electrocardiogram (EKG) electrodes leading from the transmitters were implanted 2 cm on either side of the sternum. Heart rate and Vo, of badgers were determined simultaneously in the laboratory by using varying ambient temperatures to promote significant changes in metabolism (Holter et al. 1976). Telemetered animals weighing an average of 8kg were released into separate outdoor enclosures made of cyclone fencing measuring 5 m on a side and extending 2 m beneath the ground with an enclosed bottom. Heart rate and body temperature signals transmitted from badgers within each enclosure were picked up by a ferrite rod antenna within polyvinylchloride (PVC) tubing buried 1 m below ground. Signals were processed by a digital/ analog ratemeter (Harlow et al. 1979) and continuously recorded on an Esterline Angus model 402 multichannel recorder located in an insulated building 15 m from the enclosure.

BURROW TEMPERATURE AND BURROW USE
The temperature 6 cm above the ground and within two burrows was monitored continuously during the winter of 1977-1978 with a Dickerson 7-day Minicorder, model 42-2. To monitor burrow temperature, thermocouple probes from the recorder were pushed through the dirt plugging the entrance and as far into the burrow as possible.
The length of time each badger spent in its burrow was determined with a directional photocell monitoring system placed at the burrow entrance (Harlow 1979b).
A Student t-test and least-squares regression were employed to examine differences between means and linear correlation of data, respectively (Neter and Wasserman 1974).

Basal metabolic rate (BMR) for badgers
weighing an average of 9.0kg was 0.3 cm3/g-h or 311 kcal/day, 14% below the 363 kcal/day value predicted from the equation M = 70 W0.75 (Kleiber 1975). The lower critical temperature (T10) was 10 C, while conductance was calculated as 0.01225 cm3/g/h/oC ( fig. 1) during the winter of 1977-1978 reduced their above-ground activity by 93% from November through February. This was followed by a 220% increase in aboveground nocturnal activity by April, when temperatures were warmer (fig. 6). The 1978-1979 winter had ambient temperatures of about 10 C lower than the previous year. Two badgers monitored January through March remained below ground for 74 and 85 continuous days.
Heart rate of badgers was significantly (r = .97) correlated with oxygen consumption ( fig. 7). The heart rate of badgers while below ground during February and March 1978 was about 65 beats/min (figs. 8 and 9), which corresponds to a metabolic rate of 0.32 cm3/g. h. Above-ground behavior consisted of foraging, feeding, and digging activities. During February, badgers were active above ground between 1500 and 0100 MST and had an average heart rate of 90 beats/min (0.42 cm/g-h) ( fig. 8) activity over a greater number of hours per day (1600-0600 MST) with an average heart rate of 150 beats/min (0.96 cm3/g*h) ( fig. 9). During the winter 1978-1979, continuous telemetry signals were received for only one of the two badgers remaining constantly below ground. During this time, the heart rate was only occasionally elevated above 55 beats/min (0.27 cm3/g-h). In addition, on 30 occasions the badger entered torpor which was characterized by a drop of 9 C in body temperature and a 50% reduction in heart rate ( fig. 10). initial reduction in heart rate to the end of arousal (defined as the return to a resting heart rate of 55 beats/min).

DISCUSSION
Conductance is an exponential function of body weight and can therefore be predicted from the general formula: C = 1.02 W-o.505 (Herreid and Kessel 1967). The observed value of 0.01225 cm3/g/h/1C was 16% higher than the predicted value of 0.01027 cm3g/h/oC for a 9.0 kg animal. Gettinger (1975) found low values of conductance for fossorial animals and expressed this as an adaptation for preventing excessive heat loss. McNab (1966), however, characterized fossorial rodents as having high conductance as a means of limiting the heat load incurred during active digging. It is difficult to explain the high conductance values observed for the temperatezone badger during winter in terms of the need to dissipate heat, but it may indeed be associated with the thermal buffering effect of the burrow. The coyote, Canis latrans, is generally nonfossorial and, as a result, is exposed to cold temperatures for longer periods than the badger during the winter. Kleiber's (1975)  In the present study, oxygen consumption and heart rate were highly correlated, and the curve fell midway between those obtained by Lampe (1976) from two female badgers on a treadmill. Heart rate was therefore used to estimate metabolic ex- fat utilization, as indicated by carcass analysis of field animals. The more severe 1978-1979 winter, however, was associated with prolonged restriction below ground by badgers within the enclosures. These animals had a daily energy expenditure of 240 kcal, which is about 25% lower than that observed in February of the previous year and 13% below the BMR calculated in the laboratory.

Insulation of the badger is significantly lower (P < .005; F*-statistic of error sum of squares [SSE] [Neter and Wasserman 1974, p. 163]) than insulation calculated from data presented by Shield (1972) on coyotes similarly tested (fig. 1). Conditions associated with burrows (see Swan 1974) could reduce winter thermal stress to the badger and therefore be correlated with a higher thermal conductance (lower insulation). The BMR of badgers is 30% below that predicted by Iverson's (1972) equation for mustelids and 14% below that predicted by
In a study of the European badger, Johansson (1957) showed that many aspects of the animal's annual cycle are similar to those of hibernators. In addition, Slonin (1952)  present study has demonstrated the ability of the American badger to enter a state of shallow torpor. Induction into torpor may be in response to cold temperatures and food deprivation. It appears that the badger utilizes its ability for short-term hypothermia only during the coldest months of winter. In addition, Harlow (1979a) showed that badgers fasted 30 days had a 22% reduction in basal metabolism. Therefore, both factors may be acting in concert to cause the badger to go hypothermic.
Body temperature and metabolism during the torpor cycle are close to predicted values. For example, Swan (1974) characterizes torpor by a reduction in metabolism along a temperature coefficient (Qlo) slope of about 2.0. The badger had a Qio of 2.15 as its metabolism dropped from 0.26 cm3/ g.h at 37 C to 0.13 cm3/g.h at 28 C. In addition, animals with Qio values near 2.0 are characterized by a 7.18% drop in Vo, per 0C (Morrison 1960). From this relationship, the predicted Vo, of a badger that dropped its body temperature 9 C would be 0.130 cm3/g-h, which closely approximates the 0.133 cm3/g.h calculated from heart rate while in torpor. Assuming a specific heat of tissue to be 0.82 kcal/kg/oC (Hart 1951), it would require 59.8 kcal to raise the temperature of an 8-kg animal by 9 C. It required 60.2 kcal to bring the badger's temperature from 28 C to 37 C, very close to the predicted expenditure. However, the 4 h required for this arousal were 1.5 h longer than predicted by the formula: 0C min-' = 2.03S-0.'04 (Bartholomew 1972). It has long been known that small heterothermic mammals warm up more rapidly than large ones. As a consequence, Pearson (1960) believes that large mammals cannot afford the time necessary to enter and emerge from torpidity each day. Torpor, however, was observed in the badger only during the cold months of December and January and did not occur every day. Periods of lowest body temperature varied in length from 6 to 18 h with an average 29-h torpor cycle from entrance to the end of arousal. In addition, normothermic periods were not characterized by foraging activity but by states of rest or sleep. As a consequence, the time required for the badger to arouse is insignificant as long as the torpor cycle provides an energy saving. Energy expenditure during the 29-h torpor cycle required 220 kcal for an 8-kg animal. Entry into torpor accounted for 26/% of the total energy spent in the torpor cycle, and torpor itself accounted for 31.5%. The remaining 42.50% was used during arousal. If the badger slept continuously with a heart rate of 55 beats/min for the same period, it would expend 300 kcal. Therefore, torpor provided the badger a 277% energy savings or 8.5 g of fat during the period of an average cycle. This would amount to a total of 255 g of fat, which would allow the badger an extra 10 days of rest without food during early spring to act as a buffer against bad weather and food scarcity.