Metabolic and thermoregulatory responses to heat and cold in the

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to ambient temperatures (Ta) between --35 ~ and +34 ~ They tolerated severe cold stress but were less able to withstand hca~. At --35 ~ T a, normal body ...
J. comp. Physiol. 102, 115--122 (1975) 9 by Springer-Verlag 1975

Metabolic and Thermoregulatory Responses to Heat and Cold in the Djungarian Hamster, Phodopus sungorus Gerhard Heldmaier Max-Planck-Institut fiir Verhaltensphysiologie, Erling-Andeehs, Federal Republic of Germany Received April 11, 1975 Summary. Djungarian hamsters, Phodopus sungorus (31.1 g body weight) were exposed to ambient temperatures (Ta) between --35 ~ and +34 ~ They tolerated severe cold stress but were less able to withstand hca~. At --35 ~ Ta, normal body temperature was maintained for several hours. Thereby maximum thermal insulation was calculated at 1.1 g. ~ which is only slightly higher than expected from the hamsters body size. High levels of heat production (60 to 90 roW/g) were maintained for several hours, suggesting that well developed means of heat production are the main reason for cold tolerance of the Djungarian hamster.

Introduction Djungarian dwarf hamsters are one of the smallest species of the rodent family Cricetinae, with body weight ranging from 25 to 50 g in adult individuals. They live in Western Siberia at 50 ~ to 60 ~ latitude, where air temperatures v a r y between + 3 0 ~ in summer and --40 ~ in winter (Flint, 1966). Although data on their microelimate are not available one m a y anticipate t h a t Siberian winter conditions are extremely stressfull for such a small, nocturnal mammal. Daily torpor was observed occasionally in Djungarian hamsters kept in the laboratory. However, these periods of torpor lasted for several hours only and body temperatures never fell below 19 ~ despite much lower exposure temperatures (6 ~ (Figala et al., 1973). This m a y slightly reduce their energy requirements during sleep, but it suggests t h a t Djungarian hamsters do not escape Siberian winter b y extended periods of hibernation in a proper microclimate. Field observations of active Djungarian hamsters during winter support this suggestion (Nekipelov, 1960, cited b y Flint, 1966). Besides these observations of daily torpor and demonstrations of brown fat and nonshivering thermogenesis (Heldmaier, 1971; Heldmaier and Hoffmann, 1974), little is known about thermoregulation in this species. Therefore, the physiological responses to environmental temperature load were investigated in Djungarian hamsters, with special emphasis on their ability to withstand severe cold stress.

Methods Djungarian hamsters have been bred successfully at our institute since 1968 (Figala et al., 1973). Our colony originates from a few individuals caught near Omsk in Western Siberia. They belong to the north-western race of Phodopus 8ungoru8 sungoru8 Pallas which is showing marked seasonal variations in fur eolouration and body weight, changing from dark grey

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fur and large body weight in summer to a white fur and small body weight in winter (Flint, 1966; Veselovsk~ and Grundovg, 1965; Figala et al., 1973). 15 adult individuals (age 9-12 months) of both sexes were used in the present investigation. They were kept singly in plastic cages using sawdust as bedding material. Food was provided ad. lib., consisting of food pellets for rats (Altromin 1324/R) and twice a week lettuce and apples; no water was given at any time. The experiments were performed during March and April 1974 on hamsters living at room temperature (20-23 ~ under natural photoperiodic conditions. At that time they already had dark summer fur and their body weight was in between winter and summer values (mean 31.1 g; range 23.9 to 35.6 g). For measurements of O~-consumption and C02-production the Djungarian hamsters were placed on PVC-grids in small plastic boxes (2.8 1). Within these boxes they were exposed to various ambient temperatures between 34 ~ and --35 ~ in a rapidly responding climate chamber (Klimapriifschrank KSttermann 2113). --35 ~ was the coldest temperature which could be reached inside the metabolic boxes. Ambient temperatures (T a) as used in the present investigation, were measured by a thermocouple fixed to the inside wall of the metabolic box, i.e. they were slightly higher than air temperature produced by the climate chamber due to heat loss of the hamster sitting in the box. All metabolic measurements were made during daytime between 7.30 and 19.00, i.e. the resting time of Djungarian hamsters. First values were read after a three hours equilibration period with the hamster sitting in the box at 25 ~ T a. On the first day metabolism was measured at 34, 30, 27, 20 and 0 ~ T a. One to two weeks later, the metabolism of the same hamsters was measured at 10, --10, --22 and --34 ~ T a. This procedure was chosen in 10 hamsters, whereas the remaining 5 hamsters were first exposed to severe cold and then to moderate temperatures; no different results were obtained with the reversed procedure. 0 e and CO~ was measured in an open system using a paramagnetic O~-analyzer (Magnos, Hartmann and Braun) and an inffared-CO2-analyzer (Urns, Hartmann & Braun). The paramagnetic oxygen analyzer was calibrated at regular intervals using N2-~ air mixtures prepared with a calibration pump (W6sthoff Pumpe G27/3a). 02 and C02 values were calculated for standard temperature and pressure conditions according to the formula described by Heldmaier (1971). Measurements of total evaporative water loss were made simultaneously with O~- and C02measurements in 8 hamsters. Air from the metabolic box was passed through drying tubes filled with a P2Os-based water absorbent (Siecapent, Sehuchardt GmbH) before entering the gas analyzers. Control values of water content of the air entering the metabolic box were obtained by passing the air of the climate chamber through two similar drying tubes simultaneously in each experiment. Water was absorbed for 30 min and measured by weighing the drying tubes to the nearest 0.1 mg. Water weights were converted to evaporative heat loss assuming that evaporation took place at a surface temperature of 36.5 ~ whereby 576 cal are lost by the evaporation of 1 g water. Rectal temperatures were measured at the end of a 1.5 h temperature exposure with a small thermistor probe (Thermophil 4448/H 116 AF). Each hamster was quickly removed from the metabolic box, the probe was inserted 2 em into the rectum and temperature was read on a galvanometer, a procedure which lasted between 5 and 15 sec. Metabolic heat production (HP; roW/g) was calculated from 02-consumption (M; ml/g. h) and the respiratory quotient (RQ; C02/02-ratio) by using the following approximation: H P = (4.44 + 1.43. R Q). M This equation was derived from the caloric equivalents of 02-consumption as published in Documenta Geigy (1960) and by converting them into Watt.

Results W h e n e x p o s e d t o a m b i e n t t e m p e r a t u r e s (Ta) b e l o w 24 ~ D j u n g a r i a n h a m s t e r s m a i n t a i n e d r e l a t i v e l y c o n s t a n t r e c t a l t e m p e r a t u r e s (T~), w i t h m e a n v a l u e s r a n g i n g f r o m 36.1 to 37 ~ (Fig. 1). T h e i r Tre was n o t e v e n i m p a i r e d b y p r o l o n g e d

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Fig. l. 02-consumprAon and body temperature of Djungarian hamsters at various environmental temperatures. Values are single measurements (e) and means (,). The regression for the cold induced increase in O3 consumption (M) is M = 6.39--0.173- T~ (n = 15; r = 0.98). This regression extrapolates to zero O.,-eonsumption at 36.9 ~ (= theoretical body temperature). However, the cold induced increase in O2-consumption is apparently not completely linear. Therefore, two separate regressions were calculated, one for moderately cold Ta's between 24~ and 0 ~ and one for extremely cold Ta's between O ~ and --35 ~ The regression for moderate cold was M = 6.89--0.21. T~ (n = 15; r = 0.97), extrapolating to a theoretical body temperature of 33.2 ~ The regression for extreme cold was M = 6.91--0.14. T a (n = 15; r = 0.94), extrapolating to a theoretical body temperature of 51.2 ~

exposures to --35 ~ f a , in fact t h e y showed slightly higher Tr~'s after 1.5 h in severe cold (36.1 ~ Tre at 24 ~ T~ v e r s u s 37 ~ ~e at --35 ~ T~, p < 0 . 0 0 1 ) . This high T~e was still maintained after 4.5 h in severe cold (36.9 ~ experiments shown in Fig. 2). :In one hamster a continuous record of interscapular temperature was obtained b y a subcutaneously implanted thermocouple. This interscapular temperature was between 0.5 to 2 ~ higher t h a n T~e at each cold exposure temperature. Temperature exposures above t h e r m o n e u t r a l i t y were answered b y a drastic increase in T~e of a b o u t 4 ~ quite in contrast to the constancy of ~ in the cold. This heat induced increase in b o d y temperature was accompanied b y a slight increase in mean Oe-consumption (Fig. 1) ( Q10= 1.87).

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Minimum 02-consumption of 1.7 m l / g . h was found in resting Djungarian hamsters at 24 to 28 ~ T a. This value is 10 to 20% higher than expected for a m a m m a l of 31.1 g body weight, if compared with the allometric predictions of Kleiber (1967) or Brody (1964). Below 25~ Ta, 02-consumption of Djungarian hamsters increases steadily with falling T~, down to --35 ~ with no apparent sign t h a t the limit of their capacity for O2-consumption has been reached. Mean O2-consumption at --35 ~ T~ was 11.8 ml/g. h, which is about 7 times the resting O2-consumption at 25 ~ Ta. This high level of Os-consumption could be sustained for several hours, as indicated by a 4.5 h exposure to m a x i m u m cold in the climate chamber (Fig. 2). As calculated from 08 and CO s measurements, the m a x i m u m thermogenic capacity of Djungarian hamsters observed in the present study was ranging from 60 to 90 m W per g body weight. The respiratory quotient (R Q) was found to be 0.92 at warm and thermoneutral T~'s (Fig. 3). Below thermoneutrality there occurred a rapid decline in I~Q to

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0.74, demonstrating a greater proportion of fat utilized for heat production during cold defense. This final value was reached already at 0 ~ Ta, at an O~-consumption of 7.1 ml/g. h, which indicates t h a t further increase in O2-consumption was not accompanied b y a change in the metabolic sources of heat production. The pattern of evaporative water loss of Djungarian hamsters was similar to patterns usually obtained in small rodents (Fig. 4) (Shkolnik and Borut, 1969; Wunder, 1970; B~udinette, 1972). At 10 ~ T~ the evaporative heat loss resembled about 10% of total heat loss. This percentage increased with increasing ambient temperature, reaching about 40% at 34 ~ Ta. This percentage reveals t h a t Djungarian hamsters have only a moderate evaporative heat loss, since rodents with a large potential for evaporative heat loss, like R a t t u s lutreolus (Collins, 1973), can dissipate 100% of their total heat b y evaporation. The metabolic and temperature responses of Djungarian hamsters were accompanied b y regular postural changes. At ~ ' s above 30 ~ they always lay fiat on their ventral side with limbs extended from the body, and their fur was not evenly fluffed but showed numerous "ventilation g a p s " all over the back of the animals. Only few hamsters showed a small amount of saliva spreading

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on their ventral thoracic surface. At Ta's below 20 ~ they always rested in an extremely hunched posture, sitting only on their hind feet and hiding their face and front feet in the ventral fur. The ventilation gaps observed in the heat gradually disappeared and the fur became evenly fluffed. Total thermal insulation (I) was calculated according to Newtons law of cooling from heat production (HP) and the temperature gradient between the hamster and its environment, by using the formula I -----(Tre-- T~)/HP (Scholander et al., 1950; Hart, 1971) (Fig. 5). At 24 ~ T~ the hamsters were already close to their maximum thermal insulation showing 0.94 g-~ there was a further slight but significant increase in insulation at subzero temperatures where it reached 1.1 g. ~ (p < 0.005). Discussion

The present findings demonstrate an extreme cold tolerance in Djungarian hamsters. They can maintain their body temperature during prolonged periods of cold exposure down to --35 ~ None of the hamsters showed hypothermia, frost-bite or any other signs of cold injury, suggesting that they could withstand even lower temperatures. There is so far only a limited number of severe cold exposure experiments with mammals of similar body size. Hart (1953a, b) investigated three species of Deer mice (body weight 22 to 29 g) and found at --26 ~ ~ a survival time of only 1 to 2 hours. If they were previously cold adapted their survival time was extended and only some of the mice became hypothermic during 3 hours exposure to --26 ~ T a. Golden hamsters which are 3 to 4 times larger than the Djungarian hamster, became hypothermie at --15 ~ T a when previously adapted to 28 ~ and only cold adapted golden hamsters could withstand a short exposure to --30 ~ (Pohl, 1965). Heat resistance of Djungarian hamsters seems rather weak. The hyperthermia developed at 34 ~ T~ may be an effective way to reduce heat gain from the environment, as has been reported for several small rodents from desertlike habitats like the Kangaroo rat (Schmidt-Nielsen, 1965), Spiny mice (Shkolnik and Borut, 1969), Merriams chipmunk (Wunder, 1970), Australian hopping mice (MacMillen and Lee, 1970), California ground squirrel (Baudinette, 1972) and Australian rats (Collins and Bradshaw, 1973 ; Collins, 1973). However, in preliminary experiments several Djungarian hamsters died at 36 ~ T~, suggesting that this protective hyperthermia is limited to relatively moderate heat exposures. Improved cold resistance in mammals can be achieved by two means, either by an improvement of thermal insulation and/or by an enhanced potential for heat production. Maximum thermal insulation of Djungarian hamsters as predicted from their body weight of 31.1 g is 0.99 g. ~ (Herreid and Kessel, 1967). This insulation was obtained by using the regression of minimum thermal conductance versus body weight as published by Herreid and Kessel (1967), and by converting conductance (C) into insulation (I) by I = I / C . Total thermal insulation, as measured in the present experiments is 5 % less than the predicted value at Ta'S between 24 and 0 ~ At subzero temperatures it exceeds the predicted maximum insulation by 12 %. However, this comparison should be regarded with some reservation, since data on thermal insulation in small mammals are

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n o t usually based on severe cold exposure experiments (Herreid and Kessel, 1967; Morrison and Tietz, 1957). This shows t h a t m a x i m u m thermal insulation of Djungarian h~,msters is slightly higher t h a n expected for a m a m m a l of its b o d y size, b u t is certainly not high enough to be responsible for all of their extreme cold tolerance. H e a t production of Djungarian hamsters reached 60 to 90 m W / g in the present experiments, as calculated from their O~-consumption and CO~-production. Similar high values of 02-consumption were also obtained in Deer mice during severe cold exposure (Hart, 1953b). However, t h e y could m a i n t a i n this high level only for a short time, whereas Djungarian hamsters even after 4.5 hours at --35 ~ showed no sign of a decline in heat production. This suggests heat production to be the p r i m a r y reason for cold tolerance in the Djungarian hamster. T~'s from ~-20 to --35 ~ m a y reflect most of the temperature range as experienced b y Djungarian hamsters living in the Siberian steppe. W i t h i n these temperatures t h e y show only small changes in thermal insulation relying mainly on their high potential for heat production. Expert technical assistance of P. Hebblethwaite is gratefully acknowledged. Supported by the Deutsche Forschungsgemeinschaft.

References Baudinette, R. V. : Energy metabolism and evaporative water loss in the California ground squirrel. J. comp. Physiol. 81, 57-72 (1972) ]3rody, S. : Bioenergetics and growth. New York: Reinhold Publishing Corporation 1964 Collins, ]3. G. : Physiological responses to temperature stress by an Australian murid, Rattus lutreolus. J. Mammal. 54, 356-368 (1973) Collins, ]3. G., ]3radshaw, S. D.: Studies on the metabolism, thermoregulation and evaporative water loss of two species of Australian rats, Rattus villosissimus and Rattus rattus. Physiol. Zool. 46, 1-21 (1973) Documenta Geigy: Wissenschaftliche Tabellen. Basel: J. R. Geigy A.G. 1960 Figala, J., Hoffmann, K., Goldau, G. : Zur Jahresperiodik beim Djungarischen Zwerghamster Phodopus sungorus Pallas. Oecologia 12, 89-118 (1973) Flint, W. E. : Die Zwerghamster der pal~iarktisehen Fauna. Wittenberg Lutherstadt: A. Ziemsen 1966 Hart, J. S. : The relation between thermal history and cold resistance in certain species of rodents. Canad. J. Zool. 31, 80-89 (1953a) Hart, J. S. : Energy metabolism of the white-footed mouse, Peromyscus leucopus noveboracensis, after acclimation at various environmental temperatures. Canad. J. Zool. 31, 99--105 (1953b) Hart, J. S. : ]~odents. In: Comparative physiology of thermoregulation, vol. I I (ed. G. Causey Whittew). New York and London: Academic Press 1971 Heldmaier, G. : Zitterfreie W~rmebildung und KSrpergrSl~e bei S~ugetieren. Z. vergl. Physiol. 73, 222-248 (1971) Heldmaier, G., Hoffmann, K. : Melatonin stimulates growth of brown adipose tissue. Nature (Lond.) 247, 224':-225 (1974) Herreid, C. F., Kessel, ]3. C. : Thermal conductance in birds and mammals. Comp. ]3ioehem. Physiol. 21, 405415 (1967) Kleiber, M. : Der Energiehaushalt yon Mensch und I-Ianstier. ttamburg: Parey 1967 )[acMfllen, R. E., Lee, A. K. : Energy metabolism and pulmocutaneous water loss of Australian hopping mice. Comp. ]3iochem. Physiol. 35, 355-369 (1970)

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Morrison, P. R., Tietz, W. J.: Cooling and thermal conductivity in three small Alaskan mammals. J. Mammal. 38, 78-86 (1957) Nekipelow, N. W.: Die transbaikalisehen Zwerghamster und einige 5kologische Besonderheiten der Zwerghamster-Unterfamilie. Izv. Irkutsk. Goss. nautsch.-issledow. AntipestInst. f. Sibirien & Fernen Osten 23 (1960) Pohl, H.: Temperature regulation and cold acclimation in the golden hamster. J. appl. Physiol. 20, 405-410 (1965) Schmidt-Nielsen, K.: Desert animals. Physiological problems of heat and water, 2nd edit. Oxford: Clarendon Press 1965 Seholander, P. F., Hock, R., Walters, V., Johnson, F., Irving, L. : Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99, 237-258 (1950) Shkolnik, A., Borut, A.: Temperature and water relations in two species of spiny mice (Acomys). J. Mammal. 50, 245-255 (1969) Veselovsk~, Z., Grundovs S.: Beitrag zur Kenntnis des Dschungar-Hamsters, Phodopus sungorus (Pallas, 1773). Z. S~ugetierk. 30, 305-311 (1965) Wunder, B. A.: Temperature regulation and the effects of water restriction on Merriam's chipmunk, Eutamias merriami. Comp. Biochem. Physiol. 33, 385-403 (1970) Dr. G. Heldmaier Max-Planck-Institut fiir Verhaltensphysiologie D-8131 :Erling-Andechs Federal Republic of Germany