1. Rewarming rate from torpor and body mass were inversely related in. 86 mammals ranging in body mass between 2 and 8500 g.

  2. Most of the mammalian taxa investigated showed a similar change of rewarming rate with body mass. Only the insectivores showed a more pronounced increase in rewarming with a decrease in body mass than did the other taxa. The rates of rewarming of marsupials were similar to those of placentals.

  3. At low air temperature (Ta), the rate of rewarming of marsupials was not related to body mass, although a strong relationship between the two variables was observed in the same species at high Ta.

  4. The slopes relating rewarming rates and body mass of the mammalian groups and taxa analysed here were similar to those obtained earlier for mass-specific basal metabolic rate (BMR) and body mass in mammals, suggesting that the rate of rewarming and BMR are physiologically linked.

One of the major differences between hibernation in ectotherms and endotherms is that endotherms actively terminate the torpor episode by internal heat production. All heterothermic endotherms actively raise their body temperature (Tb) from low levels during torpor. However, not all rewarm at the same rate. Slow rewarming rates have been observed in large species, with small species showing rapid rewarming, and Heinrich and Bartholomew (1971) demonstrated that body mass and rewarming rates in heterothermic vertebrates show an inverse allometric relationship.

Although body mass appears to have a strong impact on rewarming rates, it is not the only factor that influences the process. For example, low air temperatures (Ta) considerably slow the rate of rewarming in marsupials (Geiser and Baudinette, 1987). It also has been shown that acclimation to high temperatures reduces the rewarming rates in bats (Stones and Wiebers, 1967). Furthermore, the rate of rewarming is not uniform throughout the arousal process. Slow rates are observed at the beginning of the arousal process when Tb values are low; fastest rewarming rates are observed at Tb values that are several degrees below the normothermic Tb (Lyman, 1948; Hammel, 1986). It also has been suggested that rewarming rates may differ between mammalian groups (Heldmaier, 1978). In particular, Wallis (1982) and Fleming (1985a,b) claimed from data on a small number of species (N=5) that marsupials rewarm significantly more slowly than do placental mammals.

We compared rewarming rates from torpor as a function of body mass in 86 species, ranging in body mass between 2 and 8500 g, from the three mammalian subclasses. We re-examined the previously suggested differences between mammalian taxa and studied the influence of Ta on the rewarming rate.

Body masses and rewarming rates of 17 marsupial species were collected from data in the literature or measured in the present study (Table 1). Rates of rewarming in the present study were measured by 2- to 3-cm rectal insertion of a thermocouple probe and readings were taken at intervals of several minutes. The thermocouple wire was taped to the tail of the animals. The rewarming rates of marsupials were compared with values from the literature from one monotreme, six insectivores, 33 bats, 28 rodents and one carnivore (Table 1). The fastest rewarming rate that could be obtained for each species was used in the comparison because in most studies this was the only value reported. These rewarming rates were usually measured at ‘room temperature’, i.e. a Ta of about 20°C. In marsupials, arousal rates at a Ta of 9–11 °C were compared with those at a Ta of 18–24 °C from species ranging in body mass between 8 and 120 g to determine whether the inverse relationship between body mass and rewarming rate observed at high Ta (Heinrich and Bartholomew, 1971) is maintained at low Ta. In many of the accounts in the literature, it was not clear whether the authors determined maximum arousal rates over a short time or the fastest overall rewarming rates from the beginning of the arousal until normothermic Tb values were reached. We therefore investigated whether maximum arousal rates (over a 10-min interval) and fastest overall arousal rates (from beginning to end of the arousal process) differ significantly in marsupials for which reliable data on both rates were available. Both the maximum arousal rate and the fastest overall arousal rate of marsupials were compared with values from the other mammalian taxa. Large placental mammals show distinct temperature differences during rewarming between the anterior and posterior part of the body (Lyman, 1948; Lyman et al. 1982). For those placental mammals in which head or oesophageal rewarming rates were available these measurements were used, because maximum rectal rewarming rates in these animals reflect redistribution of heat with blood flow from the warmer anterior part to the cooler posterior part of the body rather than a direct rate of heat production.

Table 1.

Rewarming rates in mammals

Rewarming rates in mammals
Rewarming rates in mammals

Body masses and arousal rates were transformed to logarithmic values. Least squares linear regressions were performed on the transformed data for all hetero thermic mammals and on the different mammalian taxa. The curves relating body mass and rewarming rates of the various groups were compared for differences in elevation and slope using an F-test. We also investigated whether rewarming rates of daily heterotherms (torpor duration several hours) and hibernators (torpor duration several days or weeks) (see Geiser, 1988) were different; bats were excluded from this comparison because in many species it is not known whether they show daily or prolonged torpor. Statistical differences were assumed significant at the 95 % level (P < 0·05).

Rewarming rates of heterothermic mammals were inversely related to body mass (Tables 1, 2; Fig. 1). Most small mammals of body mass less than 10 g rewarmed at rates of about 1 °C min−1 or more, whereas larger species of body mass greater than 1000g rewarmed at rates of about 0.1°Cmin−1 or less.

Table 2.

Allometric relationships between body mass and rates of rewarming in heterothermic mammals

Allometric relationships between body mass and rates of rewarming in heterothermic mammals
Allometric relationships between body mass and rates of rewarming in heterothermic mammals
Fig. 1.

Logarithmic plot of rewarming rates from torpor and body mass in heterothermic mammals. The symbols indicate: (▪) echidna, Tachyglossus aculeatus-, (– • –) marsupials, maximum rewarming rate over 10min; (---○---) marsupials, fastest overall rewarming rate; (▵) insectivores; (▴) bats; (◊) rodents; and (◻) badger, Taxidea taxas. The regression lines were fitted to log-transformed data from Table 1 and the equations are shown in Table 2.

Fig. 1.

Logarithmic plot of rewarming rates from torpor and body mass in heterothermic mammals. The symbols indicate: (▪) echidna, Tachyglossus aculeatus-, (– • –) marsupials, maximum rewarming rate over 10min; (---○---) marsupials, fastest overall rewarming rate; (▵) insectivores; (▴) bats; (◊) rodents; and (◻) badger, Taxidea taxas. The regression lines were fitted to log-transformed data from Table 1 and the equations are shown in Table 2.

Marsupials and placentals rewarmed at similar rates. When the rewarming rates and body masses of all placentals and those of marsupials were fitted with two parallel regressions rather than a single regression, we could detect no statistical differences between slope and elevation of the two regression lines, nor was the relationship improved by the two-line fit (Table 2). Within the marsupials, overall and maximum rates of rewarming were also indistinguishable. In a comparison with the different mammalian taxa, both overall and maximum rewarming rates of marsupials did not differ in slope and elevation from those in bats and rodents. However, a difference in the slope relating rewarming rate and body mass could be detected between insectivores and the other mammalian taxa. Bats were the only mammalian group in which no significant relationship between body mass and rewarming rate could be detected (Table 2; Fig. 1). The echidna Tachyglossus aculeatus (Monotremata) and the badger Taxidea taxus (Carnivora) were similar to insectivores in their rates of rewarming (Fig. 1). When the hibernators of all mammalian taxa (excluding bats) were compared with the daily heterotherms no significant difference could be detected in slope or elevation of the lines relating body mass and rewarming rate.

The relationship between body mass and rate of rewarming in marsupials at high Ta differed significantly (P < 0·001, t-test; slope and intercept) from that at low Ta (Fig. 2; Table 3). At high Ta (18–24°C), a negative relationship was observed between the two variables, although data were available only for a narrow range of body masses. At low Ta (9–11 °C) no significant relationship between body mass and rate of rewarming could be detected and the slope of the regression line was reversed in comparison to measurements at high Ta (i.e. the larger species rewarmed at a rate similar to or faster than that of the smaller species).

Table 3.

Rates of rewarming of marsupials at different air temperatures

Rates of rewarming of marsupials at different air temperatures
Rates of rewarming of marsupials at different air temperatures
Fig. 2.

Logarithmic plot of rewarming rates and body mass in heterothermic marsupials at high (•, 18–24°C) and low (○·9–11 °C) Ta values. Data are shown in Table 3. Linear regression for Ta=18–24°C, log10y=0·23–0·2710g10x, r2=0.72, P>0·002, 2V=9; for Ta=9–ll°C, log10y= –0·66+0·221og10x, r2=0·11, P < 0·40, N=9.

Fig. 2.

Logarithmic plot of rewarming rates and body mass in heterothermic marsupials at high (•, 18–24°C) and low (○·9–11 °C) Ta values. Data are shown in Table 3. Linear regression for Ta=18–24°C, log10y=0·23–0·2710g10x, r2=0.72, P>0·002, 2V=9; for Ta=9–ll°C, log10y= –0·66+0·221og10x, r2=0·11, P < 0·40, N=9.

The present study shows that body mass and rate of rewarming in heterothermic mammals are inversely related, as has been suggested previously (Heinrich and Bartholomew, 1971). However, at low environmental temperatures this relationship may no longer hold. Differences in the rate of rewarming between the different mammalian taxa were not very distinct.

Air temperature had a profound effect on the rate of rewarming in marsupials. The inverse relationship of rewarming rate and body mass at high Ta was abolished at low Ta. The relatively large surface area of small animals results in a much greater heat loss to the environment than in large species and therefore a large proportion of the internal heat produced during arousal is immediately lost. It has been previously documented that the time required for rewarming from torpor to normothermia in large marsupials is much less affected by a lowering of Ta than in small marsupials (Geiser and Baudinette, 1987).

When the slope of rewarming rate and body mass was compared among different mammalian taxa only the insectivores differed significantly from the other groups. The steeper slope of the line relating these variables in insectivores seems to result from the relatively slow rewarming rates of the poorly insulated, rather large hedgehog and Echinops, and the fast rewarming rates in the very small shrews. The lack of a significant relationship between rewarming rate and body mass in bats could either be because of the small range of body mass available from this order or because other factors, such as climate or state of acclimation, are more important than body mass in determining their rate of rewarming. Unlike the slope relating rate of rewarming and body mass, the elevations of linear regressions from any of the mammalian taxa were statistically indistinguishable.

Rewarming rates of marsupials did not differ substantially from the values for any of the other mammalian groups. This observation does not support earlier suggestions that marsupials show slower rewarming rates than placentals and that this may be due to a lower thermogenic capacity in marsupials (Fleming, 1985b). The apparent lack of brown fat in adult marsupials does not appear to slow their rate of rewarming, thus supporting the findings of Lyman and 0’Brien (1986) that the direct contribution of brown fat to heat production during rewarming from torpor may have been overestimated in the past.

Interestingly, the slopes relating basal metabolic rate (BMR) and body mass of the mammalian groups and taxa show a similar pattern to that observed for the rewarming rates in the present study. When the slopes for rewarming rate as a function of body mass (Table 2) were plotted against the slope of mass-specific BMR as a function of body mass (Hayssen and Lacy, 1985, for the mammalian taxa and Geiser, 1988, for the hibernators and daily heterotherms), a significant linear relationship was observed between the two (Fig. 3). When the same analysis was performed on mammalian orders only, the relationship was also significant (r2=0.97, P < 0·01). The slope relating the two variables was close to 1·0, suggesting that maximum heat production during rewarming from torpor is related to the BMR of the animal. Both BMR and rewarming rate are related to the thermogenic capacity of the combined animal tissues and therefore the correlation between the two is not surprising. However, the strong impact of the value for the insectivores on the regression line necessitates cautious interpretation of this relationship. Because the slopes of BMR versus body mass are, apart from the insectivores, very similar among the mammalian orders (Hayssen and Lacy, 1985) more data on other orders may not further clarify whether BMR and rate of rewarming are related in mammals.

Fig. 3.

The slope of log10 rewarming rate (°C min−1) vs log10 body mass (g) as a function of the slope of log10 basal metabolic rate (BMR, mlO2g−1h−1) vs log10 body mass (g) in mammals. Slopes for rewarming rate vs body mass were taken from Table 2, those for BMR vs body mass from Hayssen and Lacey (1985) and Geiser (1988). When all groups from Table 2 were included in the regression the equation was: y= –0·013+0·95×, r2=0·68, P < 0·01, 7V=8. When only the four mammalian orders from Table 2 were included in the regression the equation was: y=— 0·12+1·10x, r2=0·97, P < 0·01, N=4.

Fig. 3.

The slope of log10 rewarming rate (°C min−1) vs log10 body mass (g) as a function of the slope of log10 basal metabolic rate (BMR, mlO2g−1h−1) vs log10 body mass (g) in mammals. Slopes for rewarming rate vs body mass were taken from Table 2, those for BMR vs body mass from Hayssen and Lacey (1985) and Geiser (1988). When all groups from Table 2 were included in the regression the equation was: y= –0·013+0·95×, r2=0·68, P < 0·01, 7V=8. When only the four mammalian orders from Table 2 were included in the regression the equation was: y=— 0·12+1·10x, r2=0·97, P < 0·01, N=4.

This research was supported by a Flinders University Research Scholarship and by a grant from the Australian Research Council.

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