J Comp Physiol B (1992) 162:696-706

Journal of Comparative ~, ~,..,o."~176176176 and EnvironPhysiology B me.tal Physiology 9 Springer-Verlag 1992

Body temperature and metabolic rate during natural hypothermia in endotherms G. Heldmaier, T. Ruf Department of Biology, Zoology, P.O.B. 1929 Philipps Universitfit, W-3550 Marburg, Federal Republic of Germany Accepted: 5 August 1992

Abstract. During daily torpor and hibernation metabolic rate is reduced to a fraction of the euthermic metabolic rate. This reduction is commonly explained by temperature effects on biochemical reactions, as described by Qlo effects or Arrhenius plots. This study shows that the degree of metabolic suppression during hypothermia can alternatively be explained by active downregulation of metabolic rate and thermoregulatory control of heat production. Heat regulation is fully adequate to predict changes in metabolic rate, and Q~0 effects are not required to explain the reduction of energy requirements during hibernation and torpor. Key words: Daily t o r p o r - Body temperature - Metabolic rate - Hibernation - Hamster, Phodopus sungorus

Introduction In hibernation and daily torpor mammals reduce their energy requirements to a fraction of their euthermic metabolic rate (MR). This reduction can be explained by two different mechanisms. Firstly, the lowered body temperature (Tb) will slow down biochemical reactions as commonly described by the Qlo effect and, secondly, the temperature gradient between an animal and its environment is reduced and less heat production (HP) is required for thermoregulation (Appendix, Eq 1). It is unclear to what extent these two mechanisms contribute to the decrease of MR during hibernation and torpor. Most previous studies focused on the Qt0 effect as the primary Abbreviations: BMR, basal metabolic rate; BW, body weight;

C, thermal conductance; CHL,thermal conductance as derived from HL; CHp, thermal conductance as derived from HP; HL, heat loss; HP, heat production; MR, metabolic rate; RQ, respiratory quotient; Ta, ambient temperature; Tb, body temperature Correspondence to: G. Heldmaier

cause of metabolic suppression. Apparent Qlos between 1.4 and 6 were found in hibernation and daily torpor (Kayser 1964; Geiser 1988). The similarity of most apparent Q10s measured in vivo with Q10s of 2-3 for enzymes or tissues in vitro (O'Connor and McKeever 1950) support the view that enzymatic thermodynamic constraints lower MR in hypothermia (Kayser 1964; Snapp and Heller 1981). In some hibernators unusually large Q10s were observed (Kayser 1961; Wang and Hudson 1971) suggesting that the metabolism is reduced by the combined action of the lowered Tb and some additional physiological inhibition (Malan 1986; Geiser 1988). Daily torpor and hibernation are characterized by a continued thermoregulation in deep hypothermia. Hypothermic mammals and birds respond to thermal stimulation and raise their MR when temperatures fall below the levels preferred in torpor or hibernation (Hainsworth and Wolf 1970; Heller and Colliver 1974; Florant and Heller 1977; Heldmaier and Steinlechner 1981). Evidently, this thermoregulatory control of MR severely questions the assumption of a purely temperature-dependent deceleration of MR, as described by Q~o effects. As far as is known, there has only been one attempt to explain metabolic reduction during hypothermia entirely in terms of thermoregulation (Snyder and Nestler 1990). However, in this study the energy savings during torpor and hibernation were not mainly ascribed to the reduced gradient between the animal and its environment, but to a tremendeous reduction of thermal conductance during hypothermia. Djungarian hamsters show daily torpor at a wide range of Ta from thermoneutrality (23 ~ to - 1 ~ and they adjust torpor TbS ranging from 25 ~ to 13 ~ This behaviour was used, to reevaluate the mechanisms underlying metabolic reduction during hypothermia. In particular, attempts were made to determine whether Q 10 effects or continued thermoregulation at a lower setpoint of Tb are responsible for metabolic suppression.

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms

Materials and methods

Results

Djungarian hamsters, Phodopus sungorus, were bred and raised as described previously (Heldmaier and Steinlechner 1981). They were kept in natural photoperiod with food ad libitum, and under these conditions they show daily torpor during winter months [December-February; Heldmaier and Steinlechner (1981)]. For long-term records of Tb, precalibrated transmitters (accuracy 0.1 ~ were implanted i.p. (Mini-Mitter, Model X, Sunriver, Oregon, USA). After termination of the experiments calibration was checked again. Transmitter signals were received through commercial car radios and processed by a microcomputer system as described previously (Ruf and Heldmaier 1987), modified for the use of IBM compatible computers. This system allowed continuous recordings of Tb in l-rain intervals over prolonged periods of time. For measurement of MR the hamsters were maintained in their standard size cages (3.0 1) in a climate chamber (500 SD Weiss, Giegen, FRG) and chamber temperature was controlled at 2, 5, 10, 15, 20 or 23 ~ with an accuracy of -/-_0.1 ~ During the experiments To was measured with thermocouples fixed to the inside wall of the cages. This Ta measured inside the cages was used for evaluation of results. The cages were sealed by a PVC top, and food and water was provided inside the cage ad libitum. Air was pumped through the cages with a flow rate of 40-60 1 9h - ~ and the 0 2 and CO2 content was measured by an O2-analyser (Ametek S IIIa Pittsburgh, PA, USA) and a CO2-analyzer (UNOR 6N Maihak, Hamburg, FRG). Both are two-channel analysers with 0.001 d Vol% resolution which compared sample air from the cages with reference air from the climate chamber. Air was dried with an electric freeze trap prior to analysis (Cooler ECP, M & C Products, Ratingen, FRG; -- 15 ~ and the flow of dried air was continuously monitored by electronic mass flow meters for each channel (FM 360 Tylan, Eching, FRG). The climate chamber was continuously supplied with outside air dried to a dewpoint of - 15 ~ A magnetic valve system allowed the measurement of six hamster cages simultaneously, in time intervals of 1 rain. An additional channel was used for automated continuous zero readjustment and calibration checks. This setup allows the measurement of metabolic rate without volume corrections. Metabolic rate was calculated according to the equation :

Q10 effect versus thermore#ulatory control of metabolic rate

MR

[ml O2 "h -1] = dVol%

O 2 9

Flow [1-h-l] 9 10

HP was calculated from MR and the respiratory quotient (RQ) according to the equation (Heldmaier 1975): HP

[mW] = (4.44+ 1.43. RQ). MR

For simultaneous records of HP and HL during torpor hamsters were placed in a gradient-layer calorimeter instead of standard size metabolic cages. This calorimeter was specifically designed for hamster size and flow rates with a measuring range of 0-3 W (Thermonetics, San Diego, CA, USA, i.d. 22.4 x 10.8 x 10.8 era). HL was calculated from the calorimeter outputs (calorimeter wall, door, d T sensor and platemeter) and calibration constants, as derived from the heat output of a resistance wire inside the device, supplied with various currents and voltages. Thermal conductance was calculated from Tb, T~ and HP (Cup) or HL (CHL) according to the equations: CHp [mW.~ Cur

[mW-~

1]_ =

HP Tb--To HL

Tb-- To

All thermocouples, outputs from analysers and flowmeters, and temperature transmitter signals were interfaced to an IBM compatible computer via 16 bit A/D converters (Datalog MDP 8082, PC Labcard 712), which also controlled the magnetic valves for online channel selection. This allowed continuous records of MR, Tb and Ta in largely undisturbed animals over prolonged periods of time. Under these conditions Djungarian hamsters will spontaneously enter torpor about every 3rd day.

697

T h e r m o r e g u l a t i o n o f e n d o t h e r m s requires a c o n t r o l l e d r e g u l a t i o n o f m e t a b o l i c H P , w h i c h d e p e n d s u p o n the t e m p e r a t u r e g r a d i e n t b e t w e e n a n a n i m a l a n d its e n v i r o n ment. I n h y p o t h e r m i a this g r a d i e n t is r e d u c e d , c a u s i n g a proportional reduction of MR (Appendix). For example, at T a = 1 6 ~ a euthermic Djungarian hamster ( T b = 36 ~ has a resting M R o f 2.4 m l 0 2 " g - 1 . h - 1 . This generates a n a p p r o p r i a t e a m o u n t o f h e a t to b a l a n c e H L a n d to m a i n t a i n a Tb-T, g r a d i e n t o f 20 ~ D u r i n g d a i l y t o r p o r , Tb c a n be l o w e r e d to 21 ~ i.e. the t e m p e r a t u r e g r a d i e n t t o the e n v i r o n m e n t is r e d u c e d to 5 ~ ( - 7 5 % ) a n d the h a m s t e r needs p r o p o r t i o n a l l y less energy to m a i n t a i n Tb at the l o w e r level, i.e. 0.6 ml 0 2 " g - 1 . h - 1 . I g n o r i n g this t h e r m o r e g u l a t o r y c o n t r o l one c o u l d a l t e r n a t i v e l y calculate a n a p p a r e n t Q l o for the r e l a t i o n b e t w e e n Tb a n d M R . U s i n g the figures m e n t i o n e d a b o v e , this gives a Q10 o f 2.69 (Eq. 4, A p p e n d i x ) . This is a r e a s o n a b l e Qlo for b i o l o g i c a l systems, a n d it is t e m p t i n g to c o n c l u d e t h a t the r e d u c t i o n o f M R c a n be adequately explained by enzymatic thermodynamics. T h e r e f o r e , the m a g n i t u d e o f a t e m p e r a t u r e effect does n o t a l l o w to differentiate b e t w e e n a n e n z y m a t i c - t h e r m o d y n a m i c or t h e r m o r e g u l a t o r y i n d u c e d s u p p r e s s i o n o f MR. H o w e v e r , the p r o b l e m o f differentiating b e t w e e n the two p o s s i b l e effects c a n be a p p r o a c h e d in t w o ways. Firstly, the time c o u r s e o f Tb, H P a n d H L d u r i n g ent r a n c e into t o r p o r s h o u l d reveal w h e t h e r in fact M R is g o v e r n e d b y c h a n g e s in Tb, o r vice versa, t h a t r e d u c t i o n s o f T b are a c o n s e q u e n c e o f r e d u c e d M R . Secondly, s t e a d y state M R d u r i n g t o r p o r s h o u l d be affected b y Tb. I n the case o f Qlo effects a n e x p o n e n t i a l decrease o f M R w i t h d e c r e a s i n g Tb w o u l d be expected. If, h o w e v e r , M R is determined by thermoregulatory control, then a linear decrease o f M R w i t h d e c r e a s i n g T b T a g r a d i e n t s (Fig. 1, top) w o u l d be expected.

Time-course of heat production and heat loss during torpor T o r p o r was i n i t i a t e d b y a r a p i d d e c r e a s e in m e t a b o l i c H P , f o l l o w e d b y a decline in Tb (Fig. 2). W h e n Tb a p p r o a c h e d the t o r p o r level, the m e t a b o l i c r a t e was slightly i n c r e a s e d a g a i n to m a i n t a i n a c o n s t a n t Tb d u r i n g t o r p o r . T o r p o r was t e r m i n a t e d b y a r a p i d increase in M R w h i c h e l e v a t e d T b to n o r m o t h e r m i c levels w i t h i n a b o u t 40 rain at 10 ~ T,. T h e r m a l c o n d u c t a n c e as o b t a i n e d directly f r o m h e a t loss (CHI.) r e m a i n e d c o n s t a n t d u r i n g these m a j o r changes in H P a n d T b. Slight v a r i a t i o n s o f CHL were o n l y o b s e r v e d d u r i n g the active state o f h a m s t e r s , w h i c h were a s s o c i a t e d w i t h the u l t r a d i a n v a r i a t i o n s o f Tb a n d M R , b u t m i n i m a l values o f CHL r e m a i n e d c o n s t a n t except for a slight n o c t u r n a l increase ( T a b l e 1). T h e r m a l c o n d u c t a n c e c a l c u l a t e d f r o m h e a t p r o d u c t i o n (CHp) s h o w e d a n a p p a r e n t decrease a n d increase d u r i n g t r a n sient states o f T b, i n d i c a t i n g n e g a t i v e h e a t s t o r a g e d u r i n g

698

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms

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Fig. 2.24-h record of body temperature (Tb), heat production (HP), and heat loss (HL) of a Djungarian hamster showing a spontaneous bout of torpor during daytime hours (top section). Thermal conductance was calculated from heat production (CHp) as well as from heat loss (CuL) (bottom section)

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Hg. 1. Relations between T b and MR. The top sections show changes expected in M R due to Q~o temperature effects (left) or when controlled by thermoregulation (right). In the latter case M R should correlate linearly with the temperature gradient between Tb and T,. The bottom sections show results obtained with Djungarian hamsters (Phodopus sungorus) during torpor and normothermia. Hamsters were implanted with intraabdominal temperature transmitters, and Tb and M R were simultaneously monitored at 2, 10 or 23 ~ T~ for several weeks. Djungarian hamsters became torpid during their diurnal sleeping phase and T b decreased to 13-27 ~ during different torpor episodes. The higher Tbs were preferably adjusted during torpor at thermoneutrality whereas the lowest TbS were found in torpor episodes observed at 2 ~ Thirty-minute means for Tb and M R during steady state in torpor (i.e., at constant Tb) and normothermia in between torpor episodes were used. Data from three different individuals which showed torpor at least at two different Tas.

entry into torpor and positive heat storage during arousal from torpor. However, during conditions of steady state in torpor and normothermia, CHp was indistinguishable from CHL (Table 1). The initial undershoot of MR was rather consistent in all hamsters (see low SEM for HP during entrance in Table 1) and was only about 50% of the MR observed during maintenance of torpor. This minimal MR was not reached at minimal Tb but when T b was still declining (23.3 ~ The subsequent increase in MR to reach the final torpor level was then accompanied by a further decrease in T~ to 19.4 ~ Q~os calculated for the different stages of torpor reveal values of 4.14 for the entrance into torpor, a Q10 of 0.2 for the transition from entrance to maintenance of torpor and a Q~0 of 1.88 for the difference between torpor and the active state.

1. Body temperature (T0, heat production (HP), heat loss (HL) and thermal conductance as calculated from H P (CHp) and from HL (CHL) in normothermic (night, day) and torpid Djungarian hamsters at Ta= 9.3 4-0.1 ~ M e a n s + SEM. n = 10 Table

Tb [~ HP [mW 9 g - l ] H L [roW 9g - l ] Cnp [mW - g - 1 . oC - 1] CnL [mW. g - t . o c - t I

Night a

Day a

Entrance"

Torpor b

Arousal c

35.5_+0.28 20.3_+0.63 20.7_+0.58 0.78 4- 0.032 0.80-+0.025

34.3+0.24 17.2_+0.54 18.2_+0.39 0.69 • 0.019 0.71 +0.016

23.3_+0.78 3.6+0.33 9.5_+0.68 0.25 -+ 0.017 0.69-+0.025

19.4-1- 1.05 6.7_+0.72 6.8-+0.70 0.67 4- 0.018 0.69-+0.022

31.8-t-0.69 36.3--+ 1.31 17.2_+ 1.86 1.58 4- 0.046 0.74-+0.058

" all values determined at minimal heat production b all values determined at minimal body temperature

c all values determined at maximal heat production

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms 6

Metabolic- rate at different Tb-T a gradients: linear or exponential reduction? The previous data were determined from torpor at an T, of 9.3 ~ but Djungarian hamsters may enter torpor over a wide range of experimental T, from thermoneutrality (23 ~ to about - 1 ~ TbS during torpor were found to be most frequently around 18 ~ however, they could vary between 13 and 25 ~ in individual torpor bouts. This allowed M R to be measured at various levels of Tb and various temperature gradients between Tb and T~. The individual variability of Tb during torpor may be illustrated by two examples: (1) at T , = 4 . 6 ~ hamster # 2 adjusted a torpor-Tb of 17.5 ~ (MR 1.20 ml O2 9 g - 1 . h - l ) , and (2) at Ta= 15.2 ~ the torpor-Tb was 22.3 ~ (MR 0.63 ml 0 2 " g - 1 . h - l ) , i.e. M R was inversely related with T b during torpor. Hamster 4~3 preferred a constant Tb during most torpor episodes. At T,=15.1 ~ it adjusted Tb at 21.4~ (MR 0.73ml O2 " g - t . h-1). When Ta was lowered to - 0 . 1 ~ it displayed torpor with a Tb=21.7~ (MR 2.51ml Oz" g - 1 . h-~), i.e. despite a constant Tb there was a threefold difference in MR. In the latter case torpor M R was even greater than basal M R during euthermia (2.1 ml 02 9g-1 . h - l ) . In Fig. 1 (bottom) MRs from 3 individual hamsters are presented either as related to Tb (left) or as related to the temperature gradient (right). The figure gives no evidence for an exponential relation between Tb and M R as expected from Q10 effects. F o r visual orientation within the scattered data points we marked data sets obtained from individual hamsters at one level of T, with regression lines, indicating that within such a uniform set of data a correlation with T, does exist. In the right hand section of Fig. 1 the same data were plotted as a function o f the temperature gradient between T a and Tb. In spite of differences in BW and C, the data fi'om these individuals clearly supported the hypothesis that MR's during both normothermia and torpor are always linearly related to the (Tb- T,) gradient. The variation of the data is probably due to the fact that TbS and MRs were measured in different individuals with differing BW and C. In order to verify this observation, a similar analysis was performed on the records of a total of 42 torpor episodes at different levels of Tb in ten hamsters. Mean values for Tb and M R ' s during thermoequilibrium were calculated for each hamster (Fig. 3, instead of individual records as used in Fig. 1). This analysis clearly shows that in all hamsters M R was linearly related to the temperature gradient confirming the predictions assuming thermoregulatory control of M R during hypothermia. In one hamster we obtained torpor episodes at ten different combinations of T, and Tb. The data from this individual (insert in Fig. 3) underline the strong linearity of M R with the temperature gradient. The lowest Tb-T, gradients occurred when hamsters displayed torpor at thermoneutrality. Under these conditions we observed a slight increase in C (0.93 __0.05 m W 9 g 1 9 ~ ~), but MRs were still as expected from the Tb-T a gradient.

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Fig. 3. Metabolic rate as a function of the temperature gradient between T b and T. (data from ten hamsters). Each individual is represented with a different symbol. Each data point represents Tb T~ and M R during a single torpor episode, or normothermia in between torpor episodes. Only steady state values at constant Tb during torpor as well as normothermia were used. One hamster with the greatest incidence of torpor (insert) demonstrates linearity within individuals. Regressions were calculated for each individual, and the mean for all regressions was plotted in this graph (b = 0.106, a=0.362, r = 0.970), Since thermal conductance was not minimal during torpor episodes at very small gradients, in particular when T, was within thermoneutrality, the regression lines were calculated for T b - r a gradients above 7 ~ only

Discussion

Entrance into torpor T o r p o r in Djungarian hamsters was always initiated by a suppression of MR. Consequently Tb decreased due to the deficit of HP. The minimum M R of about 25 % of B M R was reached within 60 rain after onset of a torpor episode. Within that period of time Tb decreased to about 23 ~ and this decrease continued for another 2 h. Minimum Tb was typically observed about 3 h after onset of a torpor episode. During this final decline of Tb no further decrease in M R was observed. In contrast, at low Ta we regularly observed a slight increase in MR, which accompanied the gradual decrease of Tb towards the maintenance level during torpor. All these observations suggest that torpor is initiated by an active downregulation of MR. Thus, hypothermia is the result but not the cause of metabolic suppression. This is not a unique observation of torpor in Djungarian hamsters but is similar to entrance into torpor and hibernation in other species. In woodchucks entering hibernation a decrease of M R clearly preceded the decrease in Tb (Lyman 1958). M R reached a minimum within 6 h whereas T b continued to decrease for the entire 12-h period of measurement. A similar time-course was measured in golden hamsters where M R decreased to a minimum within 3 h and Tb required about 8 h to reach its minimum (Lyman 1948). Rather large differences were observed in Spermophilus richardsonii where M R

700

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms

reached its minimum within 2 h. At that time Tb was still above 30 ~ and required further 12 h to approach the hibernation level (Wang 1978). Daily torpor is most frequently found in mammals weighing less than 100 g. Due to their low body mass and relatively large surface area Tb can change rapidly. But even under these conditions an initial suppression of MR was observed similar to our present measurements in Djungarian hamsters, e.g. in Tamias striatus, Mus musculus, Peromyscus maniculatus (Wang and Hudson 1971; Hudson and Scott 1979; Nestler 1990). All these observations support the view that the decrease of Tb during entrance into the torpid state is a consequence of the initial downregulation of MR. However, the decrease in Tb requires simultaneous changes of both HP and the central nervous regulation of Tb. From our present results we cannot differentiate to what extent either changes in the set point of Tb and/or changes in the threshold of effector mechanisms are involved (Rautenberg 1989). Heller et al. (1977) have demonstrated that the hypothalamic threshold for HP is continuously lowered during entrance into hibernation. In fact this threshold temperature was always adjusted below the actual level of Tb. This simple arrangement could guarantee a continuous decrease in Tb which is not counteracted by thermoregulatory HP.

Metabolic control durin# torpor Torpid Djungarian hamsters increased their MR when T~ was lowered indicating intact thermoregulatory control of HP even in torpor (Heldmaier and Steinlechner 1981). This is not a unique ability of torpid hamsters but has been frequently observed in other species of torpid and hibernating animals. The first observations on regulated control of MR and Tb were presented by Wyss (1932) in hibernating common dormice. Thermal sensitivity of ground squirrels was found to persist even in deep hibernation (Lyman and O'Brien 1972). Originally this was interpreted as an alarm response which initiates arousal at low T, to protect hibernators from the danger of freezing. Later studies in several species of ground squirrels and marmots demonstrated that peripheral and central thermosensitivity is maintained in hibernation and enabled hibernators to control their Tb with similar precision as in euthermia (Heller and Colliver 1974; Heller et al. 1978). Small changes in Tb caused proportional changes in HP which allowed hibernators to maintain Tb constant at their preferred levels despite changes in Ta. For animals exhibiting daily torpor detailed studies on central thermosensitivity are lacking. However, a large number of studies clearly show that torpid animals increase their HP when T~ or Tu falls below a certain threshold level. Torpid hummingbirds raised their MR when T, fell below 18 ~ (Hainsworth and Wolf 1970); this increase was proportional with the increase in cold load and hummingbirds could maintain Tb at 18 ~ even when T, fell close to 0 ~ Similar proportional control of MR was observed during daily torpor in the Djun-

garian hamster, in mice, in several species of torpid marsupials and in Rufous hummingbirds (Hudson and Scott 1979; Heldmaier and Steinlechner 198l; Geiser 1986; Geiser and Baudinette 1987; Hiebert 1990; this study). In Djungarian hamsters this regulation appears rather complex, since they adjust their Tb to a wide range of temperatures between 13 and 25 ~ during torpor. For all combinations of Tb and T, in euthermia and torpor the same proportional and linear relation with HP was found, as predicted from the physics of heat transfer.

Metabolic suppression versus Q10 effects Despite the abundant evidence for active downregulation of MR during entrance into hypothermia, as well as controlled regulation during maintenance of hypothermia, many authors prefer the view that MR in hibernation and torpor is reduced by Q10 effects (Kayser 1964; Hammel et al. 1968; Wang and Hudson 1971 ; Snapp and Heller 1981; Geiser 1988). Only a few authors doubted the validity of Qlos in natural hypothermia (Mrosovsky 1971 ; Snyder and Nestler 1990; Storey and Storey 1990). During hibernation and daily torpor Q~os of the order of 2-6 were found in most cases, but extremes reached 15 (Wang and Hudson 1971; Geiser 1988 for review). Most in vitro Q~0s for tissue MR are of the order of 2-3. This partial coincidence, as well as the principal nature of thermodynamic enzymatic temperature effects, apparently support the predominance of Q~o effects during natural hypothermia. However, experimental evidence for this assumption is still missing. It would require that Tb is actively lowered by, for example, an increase in C and that MR consequently decreases passively as a function of Tu (Tucker 1965a, b; Snapp and Heller 1981). However, the actual measurements by direct calorimetry in this study show that there is no major change of C during torpor (Table 1). A similar result can be calculated from direct calorimetry in the hibernator Spermophilus lateral&, which maintained a constant C of 0.25 W 9kg- 1. ~ ~ during entrance into hibernation which was equal to the minimum C of euthermic resting animals (Snapp and Heller 1981). These measurements are supported by behavioural observations. All mammals entering torpor in a cold environment retreat into their well-insulated burrows and nests and assume a hunched posture or even show social huddling. These measures decrease C instead of increasing it. A noticeable increase in C would require a stretched posture, panting, sweating or saliva spreading, responses which have never been reported in mammals entering torpor or hibernation. This indicates a low level of C, i.e. hibernators and daily heterotherms apparently retain body heat and cool down as slowly as possible. However, in contrast to Snyder and Nestler (1990), we found no evidence for the assumption that animals entering torpor have the ability to further decrease C severalfold below the minimum C observed in euthermia. We conclude that MR is actively suppressed in daily torpor and hibernation. Relations between Tb and MR

G. H e l d m a i e r , T. R u f : B o d y t e m p e r a t u r e a n d m e t a b o l i c rate in e n d o t h e r m s

follow the rules predicted from the physics of heat transfer at constant, minimal C (Appendix). Entrance into hypothermia is initiated by an active downregulation of MR, and Tb decreases due to insufficient HP. During maintenance of torpor, both Tb and MR can be subjected to controlled regulation. At moderate hypothermia minimum MR is kept constant. Tb will passively follow changes in Ta and will adjust at a certain level above Ta as determined by HP and C (Eqs. 2, 3, Appendix). When Tb reaches a critical temperature hibernators as well as daily heterotherms enhance their HP in order to prevent further hypothermia, i.e., in this case Tb is controlled actively by compensatory HP (Hainsworth and Wolf 1970; Heller and Colliver 1974; Heldmaier and Steinlechner 1981; Geiser and Baudinette 1987). The active downregulation of MR during hibernation and torpor has profound adaptive significances as compared to a passive, temperature-dependent reduction of MR: 1. Q~0 effects would allow an exponential two- to threefold reduction of MR per 10 ~ decrease in Tb, whereas a deliberate reduction allows much greater metabolic suppression in natural hypothermia. This is coincident with the large reductions of MR observed in daily torpor and hibernation. The reduction in MR will simply reduce the T b T a gradient, extrapolating to Tb = Ta at zero MR (Appendix, eqs. 2, 3). 2. According to the Q~0 effect, minimum MRs can only be reached when hibernators lower their Tb close to the freezing point of body fluids, whereas active suppression allows minimum MR's theoretically at any Tb. This coincides with the observation that in hibernation Tbs vary between --2.9 and 10 ~ and even higher minimum TbS of up to 25 ~ can be chosen during aestivation and daily torpor (5-25 ~ Kayser 1961 ; Wang and Hudson 1971; Geiser and Baudinette 1987; Barnes 1989; this study). 3. Due to the constant C no heat is actively dissipated to reach hypothermia, and thus no energy will be wasted during entrance into torpor or hibernation. Thus, even very short hypothermic episodes like daily torpor will save energy. The energy savings will simply change linearly with the changes in the Tb-T~ gradient (Ruf and Heldmaier 1992). Comparative physiology of metabolic rates in torpor

MRs of hibernators or daily heterotherms have been compared previously (Kayser 1964; French 1985; Geiser 1988). However, these studies contained measurements as well as estimates of Tb and/or MR's, and the estimates were partly obtained by assuming Qto effects. This does not allow conclusions about the interaction of Tb and MR. We reanalysed this relation and included only those studies where Tb-Ta and MR were measured, and where the same species were measured in normothermia as well as in torpor (Table 2). In hibernation a minimum MR of about 0.02 ml O2 "g-1. h - ' (0.112 m W . g - ~ ) w a s found in most species which is consistent with previous studies (Kayser 1964; French 1985; Geiser 1988). The hiberna-

701 10

]

,

,

,

I Euthe,mia I ...............

!

O

"eq

0

Z r

~

!

Hibernation 1 bato9 0.01

10

Q---

dormouse 9 9 squirrels9

i 1O0

9

marmotOss~ 9

i 1000

10000

Body Weight (g) Fig. 4. Metabolic rates o f hibernators in e u t h e r m i a a n d in hibernation. T h e regression equation in euthermia is M R = 45.9. B W -~ (n = 17, r = 0.979, P < 0.001 ; m e a n T, = 8.61 ~ m e a n T b = 36.04 ~ a n d in h i b e r n a t i o n M R = 0.039. B W -~ (n=17, r=0.145, n.s. ; m e a n T a = 6.43, m e a n T b = 7.49 ~ C o r r e s p o n d i n g regression e q u a t i o n s for daily h e t e r o t h e r m s as listed in Table 2 are in eut h e r m i a M R = 13.6. B W - ~ (n=25, r=0.766, P 30 ~ in hibernation [Table 2; Kayser (1964)]. If MR as well as Tb depends upon controlled regulation at constant minimum C it would be expected that metabolic suppression in hypothermia is correlated with changes in T b - T a gradient during hibernation and torpor. From Tb-Ta gradients and MR's at normothermia (Table 2) the reduction of MR in hypothermia was calculated by using Eq. 3 (Appendix). These estimates were compared with measured changes in MR (Fig. 5). In all species studied the reduction of MR during hypothermia agreed with the predictions. This relation was identical for hibernators and daily heterotherms, and was also independent of body size. It emphasizes the concept that MR and Tb are

702

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms 4

birchmouse Ill

Os 3~ ~

"7O)

30 0

.

201

1

10~

bat tW ~6 g

"13 rr "13

~dormouse

4

!

,lly

2---

S U g hamstor

10

Djh.amster

ll~squirrel 0 1~3 marmot 0

2

4

6

8

Expected Reduction of MR (ml 02- g-t. h-t) Fig, 5. During hibernation ([]) and daily torpor (m) MR is reduced. This reduction was calculated from the reduced Tb-T. gradient (Appendix l, Eqs. 2 and 3), and compared with the measured reductions in MR from all species listed in Table 2. The regression line indicates measured = expected under the influence of controlled regulation during natural hypothermia. Both depend upon each other as predicted from the physics of heat transfer (Appendix), and no Q~o effects are necessary to explain metabolic suppression in natural hypothermia.

Conclusions

Our findings raise the more general question o f whether Qlo effects can be applied in endotherms. In fact, active thermoregulatory control o f M R implies that there is no a priori reason to assume that M R is governed by passive temperature effects. Thermoregulatory responses of endotherms always include a combination of behavioral and autonomic responses, which are further modified by interactions with other vegetative control systems like osmoregulation, food intake etc. (Rautenberg 1989; Brummermann and Rautenberg 1989). The control of HP is part o f these complex interactions, but in steady state a constant relation between MR, C and Tb-Ta gradient must be maintained (Appendix, Eq. 1), even at different Tbs. Of course, the laws of thermodynamics remain valid for single biochemical processes in endotherm tissues, but the integrated control o f an endotherm obviously overrides direct temperature effects. Physiological control always implies that M R can be varied within a range limited by minimum and maximum turnover rates of biochemical reactions. Therefore, Qlo effects may well be detectable for minimum or maximum turnover rates or for the entire metabolic scope rather than for a given M R within this range. In the present study we analyzed daily torpor and hibernation, but similar relations between T b and M R

I J I 10 20 AmbientTemperatu(~ re

30

Fig. 6. False apparent Qlos which may result from thermoregulatory changes in MR during hypothermia (Eq. 5). The Qio effects were predicted for endotherms with normothermic Tbs= 37 ~ and different degrees of hypothermia ranging from 0.1 to 30 ~ (decrease in Tb) can be predicted for any other form of natural hypothermia. During the circadian resting period Tb is lowered by about 1 ~ in mammals, up to 3 ~ in birds (Aschoff 1982) and may even exceed 6 ~ following starvation or seasonal acclimation in birds (Biebach 1977; Rautenberg 1989; Reinertsen 1989). This nocturnal hypothermia was always found accompanied by reductions in MR, suggesting Q10 effects of about 2-3 (Heusner 1957; Kinnear and Shield 1975; Prinzinger et al. 1981). Our present study indicates that small circadian reductions in Tb cause thermoregulatory reductions in M R close to expected Qlo effects (Appendix, Fig. 6). In addition, Aschoff (1981) has shown that circadian changes in Tb, different from daily torpor, are accompanied by changes in C. These combined reductions of the Tb-To gradient and C could explain the lowered M R during the circadian resting phase. Our knowledge of the in vivo control of MRs is rather limited (Storey and Storey 1990) and only partly understood for the fraction of heat produced by uncoupled respiration in brown fat (Cannon and Nedergaard 1985). An inhibitory role has been discussed for the lowered p H in hypothermia (Malan 1986). However, it is not clear whether this change in pH/PCO2 really acts as a trigger for metabolic suppression, or if it is a concomitant of hypothermia. In torpor, as well as in hibernation, an inhibition of carbohydrate oxidation was observed. The transition from normothermia to hypothermia in Zapus hudsonicus and Spermophilus lateralis was accompanied by a strong inactivation of liver pyruvate dehydrogenase (Storey 1987). This enzyme allows control over carbohydrate influx into the tricarboxylic acid cycle, which indicates that reduction of M R may be initiated by an inactivation of mitochondrial proteins (Storey and Storey 1990). However, it is not known whether M R is suppressed uniformly in all tissues or if tissues are maintained at different functional levels. Considering the similarity of enzymatic temperature effects and thermoregulatory effects on metabolism as outlined in the Appendix, it is tempting to suggest that

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms

703

Table 2. Minimum metabolic rate during euthermia and torpor in hibernation and daily heterothermia

Hibernation Cercartetus lepidus Myotis myotis Zapus princeps Cercartetus concinnus Eliomys quercinus Eliomys quercinus Mesocricetus auratus Citellus lateralis Citellus lateralis Citellus lateralis Citellus citellus Spermpophilus richardsonii Echinops telfairi Marmotaflaviventris Marmota marmota Marmota marmota Marmota monax

Body weight

Euthermia

(g)

Ta (~

12.6 24 27 18.6 58 62 120 200 200 200 300 406 500 2200 3030 3070 4000

Tb (~

Torpor

Reference

Vo2 Ta (~ (ml-g-l-h-1)

Tb (~

Vo2 (ml'g

1.h-1)

5 5.5 4 5 7 5 4 5 10 10 5 15 20 20 11 10 5

33.7 35 36.6 34.4 38.1 38.2 37.2 35.7 38 38 39 34,8 30 36.6 36 35.4 36

7 5.7 6.2 6.7 3.9 5.4 2.88 1.32 1.6 1,6 1.6 1,35 1.20 0.23 0.41 0.261 0.27

5 3.5 4.5 5 5.5 5 5.6 5 2 3.5 5 15 20 5 8.5 6.2 5

5.3 4,5 5.5 5.3 5.9 7 5.8 5.4 3 3.7 7 16.4 20.5 7.9 9.5 8.7 6

0.052 0.02 0,024 0.046 0.04 0.019 0.049 0.043 0.025 0.04 0.02 0.044 0.035 0,023 0.042 0.0167 0.031

Geiser (1987) Pohl (1962) Cranford (1983) Geiser (1987) Kayser (1961) Kayser (1961) Lyman (1948) Snapp and Heller (1981) Heller and Colliver (1974) Heller et al. (1978) Kayser (1961) Wang (1978) Scholl (1974) Florant & Heller (1977) Nagai (1909) Ortmann (1992) Lyman (1958)

13 14

36 34.4

8 4.7

5 14

5.8 16.3

0.25 0.35

5

31.7

6.5

5

6

0.12

Johansen and Krog (1959) Brown and Bartholomew (1969) Brown and Bartholomew (1969) Geiser 1986 Bartholomew and Hudson (1962) Bartholomew and Hudson (1962) Heldmaier 1970 Geiser and Baudinette (1987) Geiser and Baudinette (1987) Geiser and Baudinette (1987) Nestler (1990) Hill (1975) this study this study this study Hudson and Scott (1979) Tucker (1965a, b) Wang and Hudson (1970) Bartholomew and Hudson (1962) Wang and Hudson (1971) Fleming (1980) Neumann and Cade (1965) Neumann and Cade (1965) Bartholomew and Hudson (1960)

Daily Heterothermia:

Sicista betulina Microdipodops pallidus

7.5 12

Microdipodops pallidus

12

Antechinomys taniger Cercaertus nanus

27.4 60

15.5 9

34.8 36

3.4 3.8

15.5 9

16.3 11.6

0.14 0.19

Cercaertus nanus

60

18

36

2.4

18

20.1

0.21

Myotis myotis Sminthopsis crassicaudatus

22 17.3

22 15

37 34.1

3.6 4.81

22 15

23 16.9

0.3 0.29

Sminthopsis macroura

26.9

13

34

4.04

13

18.4

0.33

15

34.3

1.48

15

25.4

0.4

11 14 22.6 16.2 11.1 19 20 30 18

35.9 36.9 35.6 35.4 34.3 36.7 37 37.7 36

4.17 3.1 2.01 3.52 2.7 3.4 3.68 1.25 2.4

11 14 22.9 16 11.22 19 20 16.8 18

21.6 20.3 27.7 21.6 15.5 20 21 17.1 20.1

1.12 0.71 1.04 0.883 0.696 0.7 0.19 0.15 0.21

10 15 23 7.7 24.5

37.9 36.6 36.2 33.6 35.75

3.28 1.69 1.4 2.59 0.85

10 15 19.5 7.7 21

19.5 18 20.7 9 21.3

0.7 0.1 0.3 0.19 0.15

Dasyuroides byrnei Peromyscus maniculatus Peromyscus leucopus Phodopus sunyorus Phodopus sungorus Phodopus sungorus Mus musculus Perognathus californicus Pero#nathus hispidus Cercaertus nanus Tamias striatus Petaurus breviceps Citellus mexicanus Citellus mexicanus Citellus mohavensis

115 18.7 20 28.6 23.2 28.6 30 25 40 60 92 132 201 201 259

704

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms

the thermoregulatory system has evolved in such a way as to optimize the use of temperature dependence of reaction kinetics to cope with changes in Tb. However, this type of control would require temperature coefficients which are not constant but decrease exponentially wi'th falling T,, as shown in Fig. 6. It seems unlikely that such a behaviour can be established in a simple manner by a proper arrangement of the reaction kinetics of the complex biochemical reactions involved in metabolic HP. Such a system would require information about Tb of the animal, which implies per se that changes of metabolic HP associated with changes of Tu are controlled by thermoregulation. Taken together, the results suggest that a simple application of enzymatic thermodynamics to the control of MR in hypothermia does not offer appropriate explanations for the lowered MR. An unbiased use of the apparent Qx0 is misleading since it ignores the effects of thermoregulation. It appears that the proportional relation between TD-T, gradients and MRs in hypothermia has been overlooked, and many Qtos reported in the literature may turn out to be effects of thermoregulation which can produce 'false' Qx0s erroneously suggesting true temperature effects.

Acknowledgement." This study was supported by the Deutsche Forschungsgemeinschaft, Sonderforschungsbereich 305 "Ecophysiology".

Appendix

False Qz0 effects caused by thermoregulation During cold exposure endotherms increase their metabolic HP (MR) in order to maintain a constant Tb. According to the physical laws of heat transfer (Fouriers law of heat flow) this increase is a function of C of the animal and the Tb-T~gradient, as described by the following equation (Scholander et al. 1950): MR

=

C.

(Tb-r~)

(1)

This equation predicts a linear and proportional increase of M R at decreasing T,, when Tb and C are held constant. In the cold most endotherms show only small changes in C and Tb and in fact M R increases almost linearly with increasing cold load. However, T b and C are not always constant nor are they independent variables, but they are changed and controlled by thermoregulating endotherms. Most obvious examples for the variability of Tb are torpor and circadian variations, whereas C shows major changes within the thermoneutral zone. Therefore, MR, C and Tb can be changed deliberately and are controlled simultaneously during thermoregulation. In stable conditions the interrelations predicted by Eq. 1 must always be fulfilled. If TD is lowered during torpor this does reduce the temperature gradient T b Ta, which must either be compensated for by an increase in C or by a decrease in MR. Thus, any decrease in Tb at constant C and constant T, reduces the M R like a Qlo effect. In order to differentiate these thermoregulatory effects on M R from true Qlo effects we call them 'false Qlo effects'. At constant T~ and constant minimum C two different Tbs (Tbt, Tb2) must be associated with two different MRs (MRs, MR2). When these variables are entered in Eq. 1, two separate equations for M R , and MR2 are obtained: MR~ = Cmirl" (T M - Ta) MR2 = Cm~,,' (Tbz-- Ta)

(2) (3)

If MR1, Tbl, T, are known and Cmin remains constant, the changing rates of metabolic HP (MR2) as required at different levels of Tb (Tb2) may be calculated. The measured MR1 and the calculated MR2 can then be used to estimate a false Qlo effect. Qlo factors can be calculated from Eq. 4. This equation is suitable for cases where the two temperatures are not exactly 10 K (10 ~ different from each other:

(4)

Q10 = M R 2

To obtain a single equation for the estimate of false, apparent Qlo effects caused by thermoregulation, Eqs. 2 and 3 for MR1 and MR2 can be substituted into the exponential equation for Q~o (Eq. 4). This gives the following equation:

false Qlo -

(5)

rb2-- r,

The conductance C is eliminated when it is constant at both Tbs, and the false Q 1o can be predicted simply out of T, and the two different TbS as observed in an actual experiment. Eq. 5 allows two general predictions of this false Qlo : firstly, large changes in T b produce large Q~o effects because high values are obtained for the quotient TD~-- Ta. Secondly, large Qlo effects

Tb2-- T~

are produced at high T,s. Thereby, the temperature gradients Tb--T, are small and relatively small changes from Tb~ to Tb2 generate large exponents as well as high values for the quotient

rb~-- ra To illustrate these relations a series of false QloS were calculated for various temperature conditions (Fig. 6). In most cases apparent Qlos between 1.4 and 4.0 were generated. This is generally regarded to be the range of reasonable Qxo s observed in animal tissues, since chemical and enzymatic reactions commonly show a Q,o of 1.44.0 (Christophersen 1973). However, at Tas above 30 ~ the thermoregulatory effects of Tb on metabolism are larger than those predicted by thermodynamic effects of tissue temperature on metabolism. A disadvantage of the temperature coefficient Q ~o is the fact that it changes with temperature. If the enthalpy of activation u of a chemical reaction is constant and does not change with temperature, then the Qlo will become slightly smaller with increasing temperature because of the relation (6): In Qlo -

10-u T- R . ( T + 10)

(6)

Therefore, the temperature dependence of a reaction is more precisely described by the enthalpy of activation u (kJ - mol-1), or, for an entire organism, the apparent enthalpy of activation "u'. This can be easily done using Arrhenius plots, where log M R is plotted as a function of the reciprocal of absolute temperature. It reveals a straight line for constant enthalpy of activation, with a slope representing its magnitude. If M R is measured at two different temperatures, the enthalpy of activation may be computed according to the equation: 'u' =

2.305 9R - (log M R 1 --log MR2)

1

1

(7)

where M R 1 and MRz are the two MRs at temperatures Tbl and Tb2 which must be entered as absolute temperatures in K; R is the gas constant (8.31 J -mo1-1 - K - l ) . To evaluate whether thermoregulatory control of M R at different levels of Tb does imitate Arrhenius plots, the log M R of hamsters was plotted as a function of their Tb [K-1]. The M R was calculated using Eq. 3 at Tbs of 37, 35, 33, 3l, 29, 27 and 25 ~

G. Heldmaier, T. Ruf: Body temperature and metabolic rate in endotherms 4.0 x=

9

"7

15~

cI:

.o_

"~a

25~

_Q

0.2

3.2

,

,

,

~

.

.

.

3.3

.

3.4

Body Temperature (1. 1000) Fig. 7. False apparent Arrhenius plots created for thermoregulatory changes in MR

starting with an 02 consumption of 3.2 ml - g- t 9h - 1 at Tb = 37 ~ and T , = 15 ~ assuming that C remained unchanged (Eqs. 2 and 3). This calculation was made for three different levels of T,: 25, 20 and 15 ~ The resulting values for 0 2 consumption are presented as three Arrhenius plots (Fig. 7). Calculated MRs do not reveal a completely linear regression of log 02 consumption with 1_. HowT ever, if "noisy" biological data are used instead of our calculated values, such small non-linearities are unlikely to be noticed. Regressions calculated for these data, disregarding the small nonlinearity, gave 'false' enthalpies of activation of 49.7, 76.5 and 132.9 kJ 9tool-1 for the three TaS, respectively. These false enthalpies of activation imitated by thermoregulatory control of M R are, like the Q~0 effects, similar to those which may be observed as true thermodynamic effects in isolated tissues or enzymatic reactions.

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