Summary. 1. Body temperature (Tb), skin temperature. (T~k), metabolic rate (MR), respira'Lory frequency .(D, tidal volume (Vv) and respiratory minute volume ...
Journal of Comparative Physiology. B
J. Comp. Physiol. 140, 241 248 (1980)
9 by Springer-Verlag 1980
Thermoregulation, Respiration and Sleep in the Tasmanian Devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) S.C. Nicol and M. Maskrey Department of Physiology, University of Tasmania, Box 252C, G.P.O., Hobart, Tasmania, Australia 7001 Accepted June 26, 1980
Summary. 1. Body temperature (Tb), skin temperature (T~k), metabolic rate (MR), respira'Lory frequency .(D, tidal volume (Vv) and respiratory minute volume (VE) were measured in adult Tasmanian devils during wakefulness (W), slow wave sleep (SWS) and paradoxical sleep (PS) over a range of ambien?, temperature (Za) from 2 4 5 ~ 2. The thermoneutral zone was 28.5 to 32 ~ During SWS and W shivering occurred at Ta's below 28.5 ~ while above Ta = 32 ~ panting occurred. 3. Below the thermoneutral zone MR and Tb varied cyclically. These cycles were due to alternation of SWS and PS. During PS shivering did not occur and MR fell markedly. 4. T b w a s very variable at Ta's from 12-28 ~ (Fig. 4), with Tb falling as low as 32.5 ~ while Tb'S below 32 ~ were sometimes measured at the beginning of an experiment. Tb increased at lower Ta'S and at T,'s above 28 ~ Panting commenced at Tb = 37 ~ and Tb rarely exceeded 38 ~ during heat exposure. 5. Va- decreased with increasing T~ in W, SWS and PS, but the change was less during PS (Fig. 6). 6. Below the thermoneutral zone, during W and SWS, I?E andfincreased as T, decreased while during PS, I?E a n d f w e r e not affected by Ta (Fig. 6, Table 1). 7. Above the thermoneutral zone, during W and SWS, l?z andfincreased rapidly due to panting, while during PS the panting response was weakened but not abolished (Fig. 6, Table 1). 8. PS appears to have an important role in reducing energy expenditure during rest.
Introduction The Tasmanian devil (Sarcophilus harrMi) is the largest extant marsupial carnivore. Although once widely Abbreviations: B M R basal metabolic rate; M R metabolic rate; PS paradoxical sleep; S W S slow wave sleep; W wakefulness
distributed on the Australian mainland, it is now found only in Tasmania. Like all dasyurid marsupials S. harrisii is active at night, when it feeds mainly on carrion, although occasionally it hunts small animals. S. harrisii is reported to have a daily rhythm of body temperature (Tb) associated with its pattern of activity, with Tb ranging from 32-37.9 ~ (Morrison, 1965; Guiler and Heddle, 1974). Robinson and Morrison (1957) found that a Tasmanian devil exposed to an air temperature of 40 ~ for 6 hours was able to maintain a normal Tb and suggested that this excellent thermoregulation was due to sweating. However, Hulbert and Rose (1972) found a seven fold increase in respiratory frequency (/#) of resting devils during acute heat exposure, with f rising from 20 breaths-min 1 at 20 ~ to 144 breaths.min -1 at 40 ~ while cutaneous water loss increased by only 50%, and concluded that panting, not sweating, was the response of the Tasmanian devil to heat. MacMillen and Nelson (1969) measured basal metabolic rate of one S. harrisii and found a BMR of 0.28 ml 0 2"g-* .h -1 (1.57 W . k g -1) at a Tb of 36.8 ~ and suggested that the thermoneutral zone extended fi'om 20 to 32 ~ Initially the aim of this study was to make a detailed investigation of thermoregulation in the Tasmanian devil. However, during preliminary experiments the animals spent a considerable time asleep in the metabolic chamber, and as thermoregulatory responses were greatly influenced by the state of vigilance of the animal the investigation was expanded to include the effects of sleep on thermoregulation. Using electrophysiological and behavioural criteria, sleep researchers have defined two main sleep states which occur in most mammals: 1: Slow wave sleep (SWS) characterised by a high voltage, low frequency, synchronous cortical EEG and a lower muscle tone than in wakefulness, and 2 : Paradoxical sleep (PS) or REM sleep, characterised by a low voltage, fast, desynchronised EEG similar to wakefulness,
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s.c. Nicol and M. Maskrey: Thermoregulation, Respiration and SIeep in the Tasmanian Devil
a t o n i a of the skeletal muscles, irregularities of respiration a n d heart rate a n d characteristic r a p i d eye movements (Jouvet, 1967). It is generally accepted that the t h e r m o r e g u l a t o r y system of m a m m a l s is inactivated d u r i n g PS, whereas d u r i n g SWS t e m p e r a t u r e regulation appears essentially similar to wakefulness, alt h o u g h Tb is regulated at a lower level (Heller a n d G l o t z b a c h , 1977; Parmeggiani, 1977). This paper examines the t h e r m o r e g u l a t o r y responses of resting T a s m a n i a n devils to a wide range of a m b i e n t t e m p e r a t u r e s a n d the effects of sleep o n these responses.
Assessment of Arousal State. Whether an animal was asleep or not, and what state of sleep it was in was judged on behavioural criteria. The metabolic chamber was fitted with a transparent top, making detailed observations possible. PS was made obvious by rapid eye movements (REMs), twitching of the vibrissae and ears, masticatory movements of the lower jaw and uncoordinated twitches and movements of the limbs. The absence of these signs during sleep was indicative of SWS. Readings were only taken from waking animals which were lying quietly with eyes open.
Results Initial Response of Experimental Animals
Materials and Methods Three adult Tasmanian devils (two female, one male, mean weight 6.5 kg (range 5.54-7.84 kg)) were used in this study. The animals were kept in captivity for eighteen months in a covered outdoor enclosure before the experiments were carried out from November 1978 to March 1979. Preliminary experiments had been performed over the previous six months and so the animals were accustomed to the experimental procedure. The experimental animal was placed in a hessian bag on the day before an experiment and brought to the laboratory where ambient temperature was maintained at 20_+0.5 ~ All measurements were thus made on post-absorptive animals which had been exposed to the same thermal conditions for at least eighteen hours before the commencement of the experiment. The air temperature in the metabolic chamber at the start of each experiment was in the range 14-32 ~ as the animals would not settle down if immediately exposed to extreme temperatures. All experiments were performed between 10.00 a.m. and 6.00 p.m.
Before the start of m o s t experiments the a n i m a l s appeared to be asleep in the bags. W h e n placed in the m e t a b o l i c c h a m b e r they generally settled d o w n quickly, b u t initially there was a slight increase in Tb. At T~'s above a b o u t 28 ~ Tb c o n t i n u e d to rise over a period of hours u n t i l it reached the e q u i l i b r i u m p o i n t for that Ta. A t lower Ta's, Tb a n d M R w o u l d generally decline after the initial rise. This lowering of Tb, which took up to two hours, was associated with entry into sleep, a n d appeared to be a regulated fall often p u n c t u a t e d by bursts of shivering.
Metabolic Rate Body temperature was measured as deep colonic temperature, using a thermistor probe (Yellow Springs 401) inserted approximately 15 cm beyond the anal sphincter and securely taped to the tail. Skin temperature (T~k) was measured on the rump with a disc thermistor (YS409) held in place with cyano-acrylate glue and adhesive tape. These temperatures and the chamber wet (Tub) and dry bulb (Ta) temperatures were recorded on a Beckman type R Dynograph. Oxygen consumption was recorded throughout the experimental period using an open circuit system as described by Nicol (1976). Oxygen consumption rates were converted to metabolic rates (MR), expressed as W.kg -1, assuming an RQ of 0.8, and hence that 1 ml of Oz has a caloric equivalent of 20.1 J, so that lmlO2-g 1-h l = 5 . 5 9 W k g -1. Respiratory frequency Q), tidal volume (VT) and respiratory minute volume (~'E) were measured barometrically as described previously (Nicol and Maskrey, 1977). Pressure changes in the metabolic chamber associated with respiration were measured with a Kyowa PG-10GC pressure transducer, the output of which was displayed on the Beckman recorder. At the beginning of each experiment, with the animal in the chamber, the respiratory recording system was calibrated over a range of frequencies (10 400 cycles.rain 1) using a motor driven piston. As the temperature of the exhaled air may be lower than core temperature, VT was calculated from the pressure changes associated with inspiration. Drift due to slow pressure changes was avoided by AC coupling the transducer output to the recorder. Respiratory parameters were recorded for periods of approximately 3 min. At high respiratory frequenciesmean values were calculated from 60 seconds of record, while at low frequencies mean values were calculated from at least 20 successivebreaths.
Even d u r i n g sleep when Tb a n d M R appeared to have stabilised, the M R record did n o t give a straight line representing m i n i m u m M R . Figure-1 shows a sample metabolic record. Despite the fact that the a n i m a l appeared to be asleep for the entire six a n d three quarter h o u r period shown, there are large, regular variations in M R . Initially, when T, was 15 ~ M R varied from 2 W . k g 1 to 3 W . k g - 2. Lowering the Ta to 10 ~ p r o d u c e d an increase in b o t h the m i n i m u m M R a n d the a m p l i t u d e of the m e t a b o l i c cycle. These cycles of M R were due to bursts of shivering associated with variations in sleep state. Cyclic variations such as this were n o t seen when a n i m a l s were awake. The ascending part of each cycle was associated with intense shivering b u t there were n o n e of the signs of PS. The plateau was associated with a decreased intensity of shivering, a n d periods in which n o shivering was visible. This p a t t e r n persisted into the descending part of the cycle, a n d then gave way to a period of PS. This PS episode resulted in a rapid fall in M R a n d w o u l d be t e r m i n a t e d by a n a b r u p t m o v e m e n t by the a n i m a l , followed by a change in posture a n d violent shivering. Shivering never occurred d u r i n g PS. Brief PS episodes sometimes oc-
S.C. Nicol and M. Maskrey: Thermoregulation, Respiration and Sleep in the Tasmanian Devil
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curred during the plateau period and initial section of the downward curve, but at all times there was a drop in MR. In metabolic studies the value of' oxygen consumption normally used is the resting minimum, which is assumed to be constant, but the metabolic response of a sleeping devil to a given temperature cannot be adequately described simply in terms of the minimum MR. As the maxima and minima were consistent during each experiment, both have been plotted in Fig. 2 as a function of Ta. The figure shows that the amplitude of the cycles increased with decreasing T~, but above a T, of about 28 ~ there is no clear distinction between maxima and minima as no shivering occurred, and variations in M R between the different sleep states were probably due to postural changes. Some points are shown for waking animals but these are not paired because when awake the animals did not show cyclic variations. Fluctuations in M R did, however, occur during wakefulness, as shivering was not continuous even at low temperatures. This produced some points which appeared to be consistent resting maxima and minima.
If the minimum MR only were examined the results would suggest that the thermoneutral zone for S. harrisii extends from about 20-32 ~ but the maxima show that the rate of increase of MR with decreasing temperature is much greater than would be suggested by the minima alone. The maxima represent the MR during shivering which is part of the thermoregulatory response to a Ta below the lower critical temperature. F r o m this graph, and from the fact that shivering was visible in both sleeping and awake devils at Ta'S up to and including 28 ~ the lower critical temperature for S. harrMi would appear to be about 28.5 ~ in both SWS and wakefulness. The minimum M R as shown in Fig. 2 is approximately 1.0 W. kg- 1, which is 64% of the value obtained by MacMillen and Nelson (1969). The maximum M R observed was 7.6 W . k g -1 at 2 ~ in a waking animal compared with a M R of 2 1 W - k g -1 during exercise at 5.6 k i n - h - 1 (Bell et al., in preparation).
Body Temperature Data on body temperature are shown in Fig. 3. The variations in M R were accompanied by cyclic changes in Tb, but these were much less clearly defined than the cycles in metabolic rate. During any one experiment the variation between maximum and minimum Tu at a steady T, rarely exceeded 1 ~ The changes in Tb appeared to lag behind the variations of MR. At low air temperatures there was a substantial increase in Tb; one sleeping devil showing an increase in Tb from 34.4 to 36.4 ~ when T, was lowered from 19 to 7 ~ At temperatures above the lower critical temperature Tb rose quite steeply with increasing Ta. When Ta is raised, S. harrisii appears to allow Tb to rise passively until it reaches approximately 37 ~ when panting occurs. At higher Tb'S the rate of panting increased and so Tb did not rise above 38.5 ~ in resting animals exposed for several hours to ambient temperatures in excess of 40 ~ In some cases, after an initial rise, the devils were able to reduce Tb. At temperatures between about 12 and 28 ~ Tb
S.C, Nicol and M. Maskrey: Thermoregulation, Respiration artd Sleep in the Tasmanian Devil
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was very variable. The lowest Tb measured was less than 31 ~ but this is not shown as the animal was not in equilibrium. Under these intermediate conditions T b does not seem to be closely regulated. To check whether spontaneous diurnal variations in Tb were affecting our results, in three experiments animals were held at a steady Ta of 10, 20 and 30 ~ for a period of seven hours. Once Tb had equilibrated no further change was seen, apart from small oscillations associated with bursts of shivering.
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During SWS respiration was regular while during PS the respiratory record showed large variations in VT and f. Fig. 5 a, b and c shows sample respiratory records at temperatures below the lower critical temperature. During SWS there was an increase in VT and f a s T~ decreased, while PS was characterised by slow
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S.C. Nicol and M. Maskrey: Thermoregulafion, Respiration and Sleep in the Tasmanian Devil
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irregular respiration with frequent periods of apnoea. Figure 5b shows a period of apnoea lasting about twenty seconds, while the longest period recorded lasted 36 seconds. Figure 5d shows several minutes of respiratory record at T~=35 ~ Initially the animal was in SWS and respiration was regular with a frequency of 140 breaths-min -1. The animal then passed into PS and f decreased to about 35 breaths 9min 1. The record shows a ten second apnoea during this period9 The animal then passed back into SWS a n d f r o s e to 200 breaths, min- 1. Figure 6 shows
245
plots of the respiratory variables, f, VT and I)E against Ta, with IkE and f data shown as semi-log plots. As VT appeared to decrease with increasing Ta, straight lines were fitted to these data by the method of least squares. It was found that the relationships between both l o g f a n d Ta and log I)E and T~ were best approximated by two intersecting straight lines. Most points between 29 and 32 ~ were included in both regression lines, although those readings in this temperature range in which there was a significant increase in f o y e r an earlier reading, i.e. a clear panting response, were included in the 29-45 ~ lines only. Details of these regression lines are shown in Table 1, and the lines for SWS and PS are shown in Fig. 6. The devils woke up at the high and low temperature extremes and generally slept at intermediate temperatures. As a result there are only a small number of unevenly distributed points from alert animals. There is little chance of obtaining a meaningful regression line through these points, so lines for alert animals are not shown in the figure. VT decreases with increasing T, during SWS, PS and W. The slopes of the VT-Ta lines for SWS and W do not differ significantly (F=0.04, D F I = I , DF2=85, P>0.8) but during PS there is less change in VT with changing Ta. During SWS at ambient temperatures below the thermoneutral zone f, and hence I)E, increases as Ta becomes lower9 This response is completely absent during PS. Although there are only six data points from alert animals, the l)E - Ta lines for W and SWS are virtually identical9 VT tends to be greater during SWS (F values for difference between adjusted VT means during SWS and W=4.7, D F I = I , DF2=86, P
