Net energetic and thermoregulatory efficiency during panting in the sheep

Comp. B&hem. Physiol., 1974, Vol. 49A, pp. 413 to 422. Pergamon Press. Pn’nted in Great Britain

NET ENERGETIC AND THERMOREGULATORY EFFICIENCY DURING PANTING IN THE SHEEP J. R. S. HALES C.S.I.R.O.,

and G. D. BROWN

Division of Animal Physiology, Ian Clunies Ross Animal Research Laboratory, Prospect, N.S.W., Australia (Received

6 September 1973)

Abstract-l. The total heat production and that proportion attributable to panting, together with the total body and respiratory heat loss of shorn Merino sheep, were studied during exposure to various combinations of air temperature and humidity. 2. While exposure to moderately hot environments resulted in panting with mean respiratory frequencies of up to 270 breaths min-‘, the total heat production was not significantly higher than that in a thermoneutral environment and therefore the heat produced by panting appeared to be zero. 3. The mean maximum heat loss through panting was approximately 60 per cent of the total heat loss and 56 per cent of the total heat production; this was due entirely to the evaporation of moisture. 4. The results indicate that the sheep relies heavily on panting for heat dissipation and that in moderately hot environments the thermoregulatory efficiency of panting is high. 5. It is concluded that, in the light of more recent observations, the method used here and in previous studies cannot be used to provide an estimate of the energy expenditure due to increased respiratory activity; rather, an estimate of the net change in metabolic rate is obtained.

INTRODUCTION

ENERGY is expended in the act of breathing, and in man in a comfortable thermal environment, this energy expenditure increases with increasing respiratory ventilation (Otis, 1954). In mammals which exhibit thermally induced panting, respiratory minute volume increases during panting (Findlay, 1957; Albers, 1961a; Hales & Webster, 1967) and it is likely that energy expenditure will also increase, adding to the heat load of the animal. It is common practice to estimate the energy cost of breathing by measuring the increase in total energy expenditure which occurs when respiratory ventilation is increased by some stimulus. This approach has been adopted in obtaining estimates of the energy cost of thermally induced panting in the dog (Albers, 1961b; Thiele & Albers, 1963; Siemon et al., 1966; Spaich et al., 1968), the ox (Whittow & Findlay, 1963; Hales, 1968; Hales & Findlay, 1968) and the pig (Ingram & Legge, 1969). A similar technique has been employed to estimate the I5

413

414

G. D. BROWN

J. R. S. HALES AND

energy cost of muscular activity, e.g. during exercise, and if simultaneous measurements of the work done are made, the efficiency of muscular activity can be calculated on the basis of energy expenditure and work done. The “efficiency” of panting in a thermoregulatory sense can be estimated by comparing simultaneous measurements of heat loss and heat production of an animal in a hot environment while panting and in a thermoneutral environment. The only estimates of the thermoregulatory efficiency of thermally induced panting are those of Thiele & Albers (1963) for the dog. In this work, the efficiency was taken as the difference between respiratory heat loss and the increment in heat production during panting compared with that in a thermoneutral environment, expressed as a percentage of the total respiratory heat loss during panting. In the present study, the energy cost and “efficiency” of thermally induced panting has been examined by the method outlined above. It should, however, be emphasized that while this method allows the determination of the net efficiency of respiratory heat dissipation as a part of the total thermoregulatory process during exposure to heat loads, it does not provide a measure of the efficiency of the panting process itself; this distinction will be discussed later. MATERIALS

AND

METHODS

Four castrated male adult Merino sheep about 5 years old and weighing 47-61 kg were used; they were shorn to leave a fleece depth of S-IO mm. Each animal consumed 500-700 g/day of a mixture of equal parts by weight of oat grain and lucerne chaff, but feed and water were not available during the period of observations and for about 3 hr beforehand. The animals were trained to stand quietly in individual pens during experimental periods, and lived in the climatic room for approximately 6 weeks until all experiments had been completed. Between experiments, ambient dry bulb temperature (Tab) was maintained at approximately 25°C. Observations were made with animals each exposed once to the following conditions at random: T,, (water vapour pressure, P, mm Hg), 5 (4), I5 (lo), 25 (IO and 20), 35 (lo,20 and 30) and 40 (IO, 20 and 30). The animal was exposed to a given dry bulb temperature for at least 4 hr before an observation period of 20-40 min. Two of the sheep were also exposed to 40°C and 49 mm Hg. Oxygen consumption (Vo,, ml min-‘) and carbon dioxide output ( VCOa, ml min-l) (S.T.P.D.) were monitored continuously by means of a ventilated face mask and respiratory circuit essentially as described previously (Hales & Hutchinson, 1971), except that air flow through the mask was varied between approximately 50 and 120 1. min-’ depending upon the intensity of panting. Total heat production (n/rth,, Watt) was calculated as described by Brouwer (1965) :

M = [(3.866po,+

1*2voo,)

x 60 x 1~163]/1000.

In most experiments, changes in rectal temperature during the 20-40 min period of observations were no more than f O.l”C and thus total body heat loss (&,,& was taken as equal to the heat production. Slightly greater increases in rectal temperature occurred during the observation periods in the warmer environments (Results and Table I) and body heat storage (S, Watt) was calculated as S = AT,, where mb is the body kg-’ ‘C-l.

weight

set-’

in kg, and 3475

x mb x 3475,

is the specific

heat of the body

tissues

in J

ENERGETIC EFFICIENCY

DURING PANTING

415

In these experiments, total heat loss was taken as the total heat production less the heat storage. Although the calculation of heat storage was based on rectal rather than mean body temperature, the error is likely to be small, since at air temperatures of 35X, skin and rectal temperatures differ by less than 1.5% and at Tdb of 4O”C, the difference is usually less than 0~5°C (J. W. Bennett, unpublished; Hales, 1973b). Because the gradient between skin surface and rectal temperature at these elevated air temperatures is so small, the difference in the temperature increment between mean body and rectal temperature during the 20-40 min observation period will be insignificant. For these reasons, the error in estimating heat storage on the basis of rectal temperature will be extremely small. Respiratory water loss was monitored continuously as the difference between water content of air entering and leaving the face mask, by including two lithium chloride dew cells in the respiratory circuit. Respiratory evaporative heat loss (E,x) was calculated by multiplying the respiratory water loss by the change in latent heat content of the air ventilating the mask. Total respiratory heat loss (Hmt,) was calculated as the sum of the changes in latent heat content and sensible heat content of air ventilating the mask. The Steam Tables (Weast & Selby, 1966) were employed in these calculations. Rectal temperature was measured with a 38-s.w.g. copper-constantan thermocouple mounted in the tip of a plastic tube O-5 cm o.d. and inserted 10 cm into the rectum. Respiratory frequency (f) was measured by recording external body movements. The efficiency (%) of panting was estimated as Efficiency =

H

Tt - %mt x 100,

mmt where MDBntis the heat production attributed to panting. RESULTS

The detailed results of experiments, excluding exposure to 40°C T,, with 49 mm Hg P,, are given in Table 1. Values for oxygen consumption (ml min-l) are included to simplify comparison with previous work on this topic. Animals were exposed to the lower range of environmental temperatures primarily to establish the environment in which heat production and respiratory frequency were minimal; this was 25°C and 10 mm Hg, and therefore values for the various functions in this environment were taken as thermoneutral or control values. Eflects of exposure to mild environmental conditions Rectal temperature. Exposure to environmental conditions of 5°C (4 mm Hg), 15, 25 and 35°C (10 mm Hg) caused no significant variation in T,,. In 35°C (20 mm Hg) T,, was maintained at a steady level 0.3°C above the control level, but T,, continued to increase at a rate of 0.2°C hr-l in 35°C (30 mm Hg) and 40°C (10 and 20 mm Hg), and 0.6”C hr-l in 40°C (30 mm Hg). The maximum mean T,, for an experimental period was 40-l + 0.1°C in 40°C (30 mm Hg). Heat production. Compared with the environment of 25°C (10 mm Hg), which was selected as “thermoneutral”, there was no significant variation in total heat production when the sheep were exposed to 25°C (20 mm Hg), 35°C (10, 20 and 30 mm Hg) or 40°C (10 and 20 mm Hg); there was a 6 per cent increase in 40°C (30 mm Hg), and increases amounting to 16 and 34 per cent in the 15 and 5°C environments respectively. The heat production due to panting has been

I-RECTAL

IO

4

Rectaltemperature 38.9kO.l 38-850.1 Respiratory frequency 18+1 16+_1 (breaths min-‘) Oxygen consumption 308i21 287&S (ml min-‘) Total heat production (W) 114.8 t 2.0 100.1 + I.8 Panting heat production (W) Total heat loss (W) 121*9+3,5 100.1 +I.8 Panting heat loss (W) Evaporative 4.3 20.4 3*0+_0.2 Sensible 3.050.5 2.3 + 0.4 Total 7.3 5.3 Non-panting heat loss (W) 114.6 94-8 Panting efficiency (“/“)

15

5

IO

39.310.2 170+1 252+5 87.9k3.9 -1.1 78.224.3

10

38.9eO.l 108212 239+9 83.8f2.9 -2.8 83,8+2’9 36.7k3.9 0*7+_0.1 37.4 46.4 100

38.8+_0*1 Is+2 244+14 s5,9+4*9 -

7.2rfl.3 1.4kO.l 8.6 77.3 -

85954.9

IO

48.9tll.6 -2.4e0.4 46.5 31.7 100

40

25

35

7.322.2 1*9+0.5 9.2 77.7 -

86.9i2.9 86.9k2.9

250+8

38.8kO.l 27+9

20

25

14 88.2 + 4.8 -2.8 76.1+ 4.9

25lk

39.6kO.2 247 +_28

20

40

44.7 &-2.9 42.4k2.7 I.1 +0.1 - 2.3 + 0.2 45.8 40.1 36.0 39.1 100 100

84.9+3.1 -2.8 84‘9+3.1

241-18

39.1 kO.1 161+12

20

3s

90*9+5.1 -3.2 66.6k3.5

253 + 14

40.1 +O.l 270+15

30

40

22-3 4 2.3 22.8 rf:3.1 2.3kO.3 -1.910.2 24.6 20.9 51.0 45.7 100 100

85.9k4.7 - 5.0 75.6.&3‘4

243513

39.6kO.4 21222

30

35

TE~PE~TURE,~SPIRATORY FREQUENCY, HEAT PRODUCTION AND HEAT LOSS IN THE SHEEP DURING EXPOSURETOVARIOUSENVIRONMENTAL CONDITIONS. FOUR ANIMALS EACH EXPOSED ONCE TO EACH ENVIRONMENT (MI3ANfS.E.)

Ambient dry bulb temperature('C) Ambientwatervapour pressure(mm Hg)

TABLE

ENERGETIC EFFICIENCY DURING PANTING

417

estimated by calculating the change in total heat production due to a direct Q10 effect on tissue metabolic rate, subtracting this from the total heat production during heat exposure, and determining the difference between this and the total heat production of the non-panting animal. The Qn, effect was calculated as described by Brody (1945) assuming Q i0 = 2, which is generally accepted for ungulates (Brody, 1945). It may be seen in Table 1 that the values for panting heat production so obtained are slightly negative. Respiratory frequency. There was no significant effect on respiratory frequency of exposure to the 15 and 5°C environments (Table 1). A maximum respiratory frequency of fifteen times the control value (270 + 15 breaths min-l) was attained in the environment of 40°C (30 mm Hg). There was a linear increase in respiratory frequency with increasing Tdb and constant P,, but with increasing P,, respiratory frequency also increased. Heat loss. Besides the values given in Table 1, the relationship between total heat loss, respiratory heat loss and total heat production is illustrated in Fig. 1. Total heat loss was equal to heat production in the 15, 25 and 35°C (10 and 20 mm

100-

g

jj

eo-

s K

z: 60-

S b b

40-

8

s2 c

ZO-

o’

5 7-

15

25

35 40 10 Dry bulb trmperature PC) /

25

35 20

Water vapaur pressure (mmtlg)

FIG. 1. The partition of the different channels of heat loss as a percentage of heat production. Mean results from four sheep each exposed to the environmental conditions shown. 0, Total heat loss ; n , respiratory evaporative heat loss; n , respiratory sensible heat loss. The level of total respiratory heat loss is indicated by a thick black bar, and it should be noted that this is less than the respiratory evaporative heat loss when there is a gain of sensible heat through the respiratory tract.

418

J. R. S. HALES AND G.

D.

BROWN

Hg) environments. In 35°C (30 mm Hg) and 40°C (10, 20 and 30 mm Hg) heat loss was 88, 89, 86 and 73 per cent of heat production. Total respiratory heat loss increased from 10 per cent of the total heat loss in the thermoneutral environment to 59 per cent in 40°C (10 mm Hg), and declined to 31 per cent in 40°C (30 mm Hg). Sensible, or non-evaporative, heat loss from the respiratory tract was small during panting, 80-100 per cent of the total respiratory heat loss being through evaporation. The non-evaporative heat loss more than doubled in the cooler environments, and became negative with an ambient T,, of 40°C. Eficiency of panting. As would be expected, since the heat production attributable to panting (MD& was zero, the efficiency of panting was 100 per cent (Table 1). Effects of severe heat stress Two animals were exposed once to environmental conditions of 40°C (49 mm Hg). Z’,, increased at an approximately uniform rate from 39.7 to 41*8”C in 48 min. Rapid shallow panting attained a peak after about 12 min and then gave way to panting of a slower deeper form. The results are given in Table 2, summarized in terms of these two phases of the respiratory response. Total heat production increased by only 9.5 per cent during the first phase but then increased by 54.9 per cent during the second phase, while that attributed to panting was initially only 5.1 per cent of the total heat production but ultimately increased to 25.3 per cent. TABLE 2-EFFECTS

OF SEVEREHEAT STRESS ON RECTAL TEMPERATURE, RESPIRATORY FREQUENCY

AND HEAT PRODUCTION.

MEAN

RESULTS FROM ONE EXPERIMENT ON EACH OF TWO SHEEP

of

Peak Thermoneutral Rectal temperature Respiratory

(“C)

frequency

39.7

(breaths

shallow

rapid

Maximal

panting

deeper

39.8

slower panting

41.8

21

331

166

(ml min-r)

353

376

558

(W)

127.1

139.2

196.9

min-‘) Oxygen Total

consumption

heat production

Panting

heat production

(W)

-

7.2

49.9

DISCUSSION

At air temperatures above 25”C, respiratory frequency increased with increases in both Tdb and P,, but changes in rectal temperature were relatively small over the range of air temperatures used. These observations are similar to those reported in earlier laboratory studies of sheep (Lee & Robinson, 1941), cattle (Beakley & Findlay, 1955) and dogs (Kappey & Albers, 1963). Further, these experiments (Table 1 and Fig. 1) have confirmed that panting is an extremely important avenue of heat loss in sheep exposed to elevated temperatures and humidities, and

ENERGETIC EFFICIFNCY

DURING PANTING

419

that almost all of this heat loss is due to evaporation. Total respiratory heat loss accounted for up to a mean maximum of 60 per cent of the total heat dissipated by the sheep when exposed to air temperatures above 25°C; this could be as high as 80 per cent for individual sheep. These results confirm earlier studies of evaporative coolinginsheep(Brockwayet al., 1965 ; Hofmeyr et al., 1969). The greater contribution of respiratory compared with non-respiratory heat loss in sheep is the converse to the situation in heat-stressed cattle (McLean, 1963). It should also be noted that the maximum respiratory heat loss did not coincide with the maximum respiratory frequency, thus illustrating the significance of water vapour content of the ambient air in determining heat loss by panting. At an air temperature of 4O”C, rectal and skin surface temperatures are also close to 40°C (Hales, 1973b) and therefore all the heat loss would be due to evaporation of moisture. Assuming a surface area of about 1.25 m2 (Bennett, 1973) it can be shown that the mean non-respiratory heat loss for the environment of 40°C and 30 mm Hg is equivalent to a cutaneous moisture loss of 59 g rnw2 hr- l. This value is almost identical to rates of cutaneous moisture loss obtained using the desiccating capsule technique on sheep (Brook & Short, 1960) or using a whole body respiratory chamber in studies on lambs (Alexander & Williams, 1962). The maximum proportion of the total heat production lost through the respiratory tract was a mean of 56 per cent (82 per cent in an individual animal). This may not represent the maximum capacity of the sheep, but compares favourably with values of 40 and 65 per cent reported for two dogs (Thiele & Albers, 1963) and a mean maximum of 70 per cent for five cats (Adams et al., 1970). However, respiratory heat dissipation in some desert birds approaches 190 per cent of the total heat production (Dawson & Bennett, 1973); this enhanced effectiveness of respiratory heat dissipation may be a reflection of adaptations to an arid environment and perhaps also to specialized requirements for flying. Since heat balance of the sheep depends considerably on heat loss by panting, thermoregulation would be more efficient if panting could be performed at a low energy cost. In fact, as shown in Table 1, the total heat production changed little, despite marked panting, and therefore it has not been possible to attribute any increase in heat production to panting. The slightly negative values calculated for the change in heat production during panting probably result from the decline in total body heat production which often occurs during moderate heat stress and is probably due to a variation in the relative metabolic rate of the various body tissues (Hales, 1973b); the assumed Ql,, value of two has no significant influence under these conditions. Such an apparently low energy cost of panting has previously been reported in cattle subjected to mild heat stress (McLean, 1963 ; Hales & Findlay, 1968; Whittow & Findlay, 1968) and was indicated by the changes in respiratory activity and oxygen consumption which followed scrotal heating in the ram (Hales & Hutchinson, 1971). It appears that the energy cost of panting is low in the cat, as total metabolic rate changes little (Adams et al., 1970), but high in the goat, as oxygen consumption is approximately doubled on exposure to 40°C T,, (Heisey et al., 1971), although

420

J. R. S. HALES AND G. D. BROWN

available data make direct quantitative comparison with the above species difficult. For the dog, Hammel et al. (1958) concluded that the energy cost of panting was very low but, in contrast, the studies by Albers and co-workers (Albers, 1961b; Thiele & Albers, 1963; Siemon et al., 1966; Spaich et al., 1968) have indicated a much higher energy cost. Since the former report attributed the observed increases whereas the latter in energy expenditure to a Q10 effect of assumed magnitude, workers employed a much lower, experimentally determined Qis coefficient, the higher values for energy cost of panting in dogs is considered to be more likely. This is surprising in view of the fact that the dog often pants at a frequency approximating the resonant frequency of its respiratory system (Hull & Long, 1961; Crawford, 1962). The higher energy cost of panting in the dog than in the sheep and ox appears to reflect a genuine species difference. Panting involves a much greater increase in alveolar ventilation in the dog than in the sheep and ox, increased alveolar ventilation being more demanding of energy than increases in ventilation of the upper respiratory tract (Hales & Findlay, 1968; Hales, 1973a). The energy cost of panting in the pig (Ingram & Legge, 1969) approximates that in the dog. Comparative data concerning the energy cost of panting have been summarized by Spaich et al. (1968) and Hales (1973a). The few observations on the effects of severe heat stress (Table 2) were performed to obtain results directly comparable with previous work on cattle (Hales, 1968 ; Hales & Findlay, 1968 ; Whittow & Findlay, 1968), providing an indication of the energy cost of maximal panting activity. The changes in oxygen consumption in the sheep were somewhat less than those reported for cattle, viz. a 7 per cent increase at the peak of rapid shallow panting and a total increase with maximal slower deeper panting of 58 per cent, compared with 22 and 65 per cent respectively in cattle. However, the proportion of the total heat production attributed to panting in the two species was almost identical, viz. approximately 5 per cent at the peak of rapid shallow panting and 25 per cent during maximal slower deeper panting. No additional energy expenditure could be attributed to panting in the sheep subjected to moderate heat stress and therefore the net energetic efficiency and thermoregulatory efficiency was very high, viz. 100 per cent. In these experiments, respiratory frequencies were from 100 to 270 breaths mini. At similar respiratory frequencies in the dog, the efficiency is approximately 60 per cent (Thiele & Albers, 1963). This high net efficiency in the sheep is at first difficult to reconcile with the energy expenditure which must be associated with the work done by the respiratory muscles in order to bring about the two- to five-fold increase in respiratory minute volume associated with thermally induced panting (Hales & Webster, 1967). It seems probable that the effect of an increase in metabolic rate of the respiratory muscles during heat stress on total heat production is offset by a corresponding decrease in the metabolic rate of other tissues. This suggestion is strongly supported by recent measurements of the regional distribution of capillary blood flow during heat stress which have shown very marked increases in blood flow to respiratory muscles while flow in some other tissues decreases (Hales, 1973b, c).

ENERGETICEFFICIENCYDURINGPANTING

421

In view of such changes, the method used here and previously for estimating the energy cost of panting is invalid in so far as it does not provide an estimate of the energy expenditure due to increased respiratory activity. Rather, an estimate of net change in metabolic rate is obtained which, nevertheless, indicates that the efficiency of the combined physiological adjustments during thermally induced panting is high with respect to energy expenditure by the entire animal. Acknowledgements-The authors are grateful to Messrs. A. A. Fawcett and W. D. Herrmann for their technical assistance, and to Mr. J. W. Bennett for his helpful discussions. NOTE

ADDED

IN PROOF

The results of recent measurements of regional tissue blood flow in the dog have shown that while capillary blood flow to respiratory muscles increases during heat stress, the concurrent decrease in the blood flow of many other tissues is less than that seen in the sheep. If these changes in capillary blood flow reflect changes in the metabolic rate of tissues relative to one another, these observations could provide an explanation for the difference in apparent energetic efficiency of panting between sheep and dog. (J. R. S. Hales & R. A. L. Dampney, manuscript in preparation.) REFERENCES ADAMST., MORGANM. L., HUNTERW. S. & HOLMESK. R. (1970) Temperature regulation of the unanesthetized cat during mild cold and severe heat stress. J. appl. Physiol. 29, 852-858. ALBERTC. (1961a) Der Mechanismus des WSirmehechelns beim Hund-I. Die Ventilation und die arteriellen Blutgase wZihrend des Warmehechelns. Pfftigers Arch. ges. Physiol. 274,125-147. ALBER~ C. (1961b) Der Mechanismus des Wgrmehechelns beim Hund-II. Der respiratorische Stoffwechsel wiihrend des Wlirmehechelns. PjWge~s Arch. ges. Physiol. 274, 148-165. ALEXANDERG. & WILLIAMSD. (1962) Temperature regulation in the new-born lamb-VI. Heat exchanges in lambs in a hot environment. Aust. J. agxric. Res. 13, 122-143. BEAKLEY W. R. Sz FINDLAY J. D. (1955) The effect of environmental temperature and humidity on the respiration rate of Ayrshire calves. J. agric. Sci. Camb. 45, 452-460. BENNETTJ. W. (1973) Regional body surface area of sheep. J. agric. Sci. Camb. 81,429-432. BROCKWAY J. M., MCDONALDJ. D. & PULLARJ. D. (1965) Evaporative heat loss mechanisms in sheep. J. Physiol., Lond. 179, 554-568. BRODYS. (1945) Bioenergetics and Growth, p. 268. Reinhold, New York. BROOKA. H. & SHORTB. F. (1960) Sweating in sheep. Aust. J. agric. Res. 11, 557-569. BROUWERE. (1965) Report of sub-committee on constants and factors. In Energy Metabolism (Edited by BLAXTERK. L.), pp. 441-443. Academic Press, London. CRAWFORDE. C. (1962) Mechanical aspects of panting in dogs. J. appl. Physiol. 17, 249251. DAWSONW. R. & BENNETTA. F. (1973) Roles of metabolic level and temperature regulation in the adjustment of western plumed pigeons (Lophophapsferruginea) to desert conditions. Comp. Biochem. Physiol. UA, 249-266. FINDLAY J. D. (1957) The respiratory activity of calves subjected to thermal stress. J. Physiol., Lond. 136, 300-309. HALESJ. R. S. (1968) The oxygen cost of hyperventilation in the ox. _7; Physiol., Lond. 194, 24-25P. HALESJ. R. S. (1969) Changes in respiratory activity and body temperature of the severely heat-stressed ox and sheep. Comp. Biochem. Physiol. 31, 975-985.

422

J. R. S. HALES AND G. D. BROWN

HALES J. R. S. (1973a) Physiological responses to heat. In MTP International Reviezv of Science, Physiology Series 1, Vol. 7 (Edited by ROBERTSHAWD.), pp. 107-162. Butterworths, London. HALES J. R. S. (1973b) Effects of exposure to hot environments on the regional distribution of blood flow and on cardiorespiratory function in sheep. Pjliigers Arch. 344, 133-148. HALES J. R. S. (1973~) Effects of heat stress on blood flow in respiratory and non-respiratory muscles. Pfliigers Arch. 345, 123-130. HALES J. R. S. & FINDLAY J. D. (1968) The oxygen cost of thermally-induced and CO,induced hyperventilation in the ox. Resp. Physiol. 4, 353-362. HALES J. R. S. & HUTCHINSONJ. C. D. (1971) Metabolic, respiratory and vasomotor responses to heating the scrotum of the ram. J. Physiol., Lond. 212, 353-37.5. HALES J. R. S. & WEBSTER M. E. D. (1967) Respiratory function during thermal tachypnoea in sheep. J. Physiol., Lond. 190, 241-260. HAMMELH. T., WYNDHAMC. H. & HARDYJ. D. (1958) Heat production and heat loss in the dog at 836°C environmental temperature. Am.J. Physiol. 194, 99-108. HEISEY S. R., ADAMST., HOFMANW. & RIEGLE G. (1971) Thermally induced respiratory responses of the unanesthetized goat. Resp. Physiol. 11,145-151. HOFMEYR H. S., GUIDRY A. J. & WALTZ F. A. (1969) Effects of temperature and wool length on surface and respiratory evaporative losses of sheep. r. appl. Physiol. 26, 517523. HULL W. E. & LONG E. C. (1961) Respiratory impedance and volume flow at high frequency in dogs. J. appl. Physiol. 16, 439-443. INGRAMD. L. & LEGGE K. F. (1969) The effect of environmental temperature on respiratory ventilation in the pig. Resp. Physiol. 8, I-12. KAPPEY F. & ALBERS C. (1963) Der Einfluss der relativen Feuchte auf die Auslosung des Hechelns beim wachen Hund. Pjfiigers Arch. ges. Physiol. 278,262-272. LEE D. H. K. & ROBINSONK. W. (1941) Reactions of the sheep to hot atmospheres. R. Sot. Queensland Proc. 53, 189-200. MCLEAN J. A. (1963) The partition of insensible losses of body weight and heat from cattle under various climatic conditions. J. Physiol., Lond. 167, 427-447. OTIS A. B. (1954) The work of breathing. Physiol. Rev. 34, 449-458. SIEMON G., PLESCHKAK. & ALBERS C. (1966) D’le alveolar-arterielle Sauerstoffdifferenz (AaDO,) und die alveolare Ventilation beim wachen Hund in AbhHngigkeit von der Umgebungstemperatur. PfEigers Arch. ges. Physiol. 289, 255-266. SPAICH P., USINGER W. & ALBERS C. (1968) Oxygen cost of panting in anaesthetized dogs. Resp. Physiol. 5, 302-314. THIELE P. & ALBERS C. (1963) Die Wasserdampfabgabe durch die Atemwege und der Wirkungsgrad des Wlrmehechelns beim wachen Hund. Pfliigers Arch. ges. Physiol. 278, 316-324. WEAST R. C. & SELBY S. M. (1966) Handbook of Chemistry andphysics. Chemical Rubber, Ohio. WHITTOW G. C. & FINDLAY J. D. (1968) Oxygen cost of thermal panting. Am.J. Physiol. 214,94-99. Key Word Index-Sheep; panting; respiratory heat loss; non-respiratory production; heat stress ; thermoregulation.

heat loss; heat