Respiration and metabolism in the giraffe

141

Respiration Physiology (1982) 50, 141-152 Elsevier Biomedical Press

R E S P I R A T I O N A N D M E T A B O L I S M IN T H E GIRAFFE

V.A. LANGMAW,

O.S. B A M F O R D ; and G. M. O. M A L O I Y 1

1Department of Veterinary Physiology, University of Nairobi, Nairobi, Kenya, and 2Nuffield Institute for Medical Physiology, University of Oxford, Oxford, U.K.

Abstract. Measurements have been made on respiration of three resting unstressed adult giraffe under normal conditions. Tracheal dimensions and body dimensions have also been measured in a large number of giraffe and other mammals. The results indicate that contrary to statements in the literature the giraffe does not have an abnormally large dead space, though the trachea is abnormally long and narrow. The respiratory measurements indicate that the giraffe breathes as predicted by published scaling equations, and at rest shows no abnormalities of rate or depth. The respiratory evaporative water loss is very small. Body temperature is labile with a range of at least 3.3 °C, and oxygen consumption, respiratory frequency, minute volume and respiratory evaporative water loss are all strongly correlated with body temperature. Body temperature Dead space Energy metabolism

Scaling equations Ungulates Ventilation

The giraffe has been described as an "anomaly of nature" (Warren, 1974) and its ,,~usual shape has led to some wild speculations about its physiology. Experimental data, however, are more difficult to find. Most of the published work has concentrated on cardiovascular physiology, and has considered the hydrostatic problems associated with head level that can vary by some two meters above and below the heart level (Patterson et al., 1965). Less attention has been paid to respiratory problems, though it has been generally assumed that the long neck contains an abnormally large dead space and that some respiratory compensation exists for this factor. The data published so far on the subject tend to be contradictory. For example, Hugh-Jones et al. (1978) maintained that respiration was slow because of a high tracheal resistance. Robin et al. (1960) also reported that respiration was slow but attributed this to an abnormally large dead space, whereas Warren (1974) suggested that the giraffe has to hyperventilate Accepted for publication 5 August 1982 0034-5687/82/0000-0000/$02.75 © 1982 Elsevier Biomedical Press

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to compensate for its increased dead space, and reported high respiratory rates. Patterson et al. (1965) reported resting respiratory rates of up to 58/rain, though these authors admit their measured rates were elevated, and were lower in resting undisturbed animals. The study reported here was concerned with two main questions: 1. Does the giraffe really have a large dead space ? 2. If so, does this affect pulmonary ventilation? To answer these questions it was necessary to have a valid basis for comparison. The mean weight of the three giraffe used in this study was just under 600 kg, and measurements on other mammals in this weight range are rare. We therefore used the allometric scaling equations calculated by Stahl (1967) which appears to be the most extensive available for respiratory and cardiovascular parameters. Clearly the values derived for 600 kg are in most cases extrapolations outside the available data but are probably more valid than using single values from animals of different morphology. We were able to use three adult healthy giraffe that had been in captivity for two years in the same enclosure at the time of the experiments, and were being handled regularly in the course of a long-term heat balance study being performed by VAL. These experimental data therefore represent an approximation to normal animals in a resting unstressed state, and are the first to do so. We were also fortunate in having access to a large volume of necropsy data obtained from culling operations. We were therefore able to make comparisons of tracheal dimensions between giraffe and a large sample of other wild mammals from similar habitats.

Methods Three captive adult masai giraffe were used in this study, two females of 570 and 640 kg and one male of 580 kg. They were kept in an enclosure at an altitude of about 1500 m close to their site of capture, and shade, "food (lucerne hay with mineral licks) and water were available at all times. At the time of these experiments the giraffe had been in captivity for about two years and were accustomed to daily handling. Respiratory measurements were made with the animals confined in a crush but otherwise unrestrained. Animals walked into the crush from the enclosure, and tolerated confinement with no apparent distress.

Respiratory data Respiratory data were collected as follows : a light close-fitting mask made from a 5-L polythene bottle was fitted over the head extending from just forward of the eyes to beyond the muzzle. The mask was sealed to the head by a soft rubber collar

RESPIRATION AND METABOLISM IN THE GIRAFFE

143

padded with foam polyurethane, and lined with a thin polythene sheet, which allowed the mask to slip over the muzzle easily and also acted as a flap valve preventing leakage of exhaled air: The air inlet was through two 22 mm disc valves (Warren Collins Inc.) set into the mask just above the nostrils, and the outlet was through a single 32 mm diameter disc valve into a 38 mm flexible air hose which conducted the exhaled air through a desiccant canister and thence to a Douglas bag. All three giraffe tolerated the apparatus well and would wear it for long periods with no apparent distress. Three-way valves allowed exhaled air to be collected or vented to the atmosphere and also sealed the desiccant from the atmosphere until required. Normally 25 breaths were collected for analysis. At the end of an expiration, valves were operated to start collecting expired air and a stop-watch was started. Breaths were counted by watching flank movements and by listening to the disc valves closing, and results accepted only if the two counts agreed. After 25 breaths the bag and canister were sealed and the watch stopped. Bag contents were passed through a Parkinson-Cowan dry gas volume meter into a second Douglas bag. Oxygen content of samples of exhaled air from the second bag was measured using a Taylor Servomex OA 272 paramagnetic oxygen analyser. Rectal and shade air temperatures, and relative humidity, were measured. No attempt was made to apply artificial heat or cooling, but by using the diurnal temperature cycle, measurements were made at ambient temperatures between 10 and 32 °C. Respiratory variables were calculated as follows: f VT ~" Vo2

= = = =

breaths counted divided by time total volume in bag divided by breaths counted, corrected to BTPS. total volume in bag divided by elapsed time, corrected to BTPS. bag volume x (20.93~ - bag oxygen ~), corrected to STPD. elapsed time Utilisation = oxygen consumption 0.2093 x bag volume The calibration of the volume meter was checked periodically by the nitrogen dilution method, using a small flowmeter which was itself checked directly using a Brooks Vol-U-Meter of 3 L capacity. The oxygen analyser was calibrated before and after each determination using nitrogen and room air. Respiratory evaporative water loss (RWL) was measured by weighing the desiccant canister before and after the 25-breath run (w 1 and w2), passing the bag contents through the canister a second time and re-weighing (w3) and finally passing a volume o f ambient air equal to the bag volume through the canister (w4). The evaporative water loss was taken as (2 x w3) - w 4 -w~. The difference between w2 and w3 was rarely more than 10~, indicating that the exhaled air was almost completely dried on a single pass through the desiccant. Water loss was calculated per unit time.

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et al.

ANATOMICAL STUDIES N e c r o p s i e s were p e r f o r m e d in the field o n 88 i n d i v i d u a l s f r o m 16 species o f wild m a m m a l s . 31 i n d i v i d u a l s were giraffe. A s t a n d a r d p r o c e d u r e was used in which 90 s e p a r a t e b o d y m e a s u r e m e n t s were m a d e i n c l u d i n g t r a c h e a l d i a m e t e r at 4 p o i n t s (in two p e r p e n d i c u l a r directions, j u s t b e l o w the l a r y n x a n d j u s t a b o v e the t r a c h e a l bifurcations), t r a c h e a l length f r o m glottis to t r a c h e a l b i f u r c a t i o n , t o t a l b o d y length f r o m nose to tip o f tail (L) a n d b o d y girth b e h i n d the f o r e l i m b s (G). M c C u l l o c h a n d T a l b o t (1965) d e r i v e d regression e q u a t i o n s for weight on L × G 2 for m a n y A f r i c a n m a m m a l s a n d where r e g r e s s i o n lines were significant they were close together, i m p l y i n g a s t r o n g s i m i l a r i t y in the w e i g h t / d i m e n s i o n r a t i o in a n i m a l s as m o r p h o l o g i c a l l y diverse as gazelle a n d h y a e n a . T h e m e a s u r e d values o f L x C~ were t h e r e f o r e used as a n i n d e x o f weight as it was n o t technically feasible to o b t a i n m o s t b o d y weights in the field. Values for t r a c h e a l d i m e n s i o n s were then p l o t t e d a g a i n s t (L x C~) for giraffe a n d for the o t h e r species s a m p l e d .

Results RESPIRATORY MEASUREMENTS T a b l e 1 shows m e a n s , s t a n d a r d errors, m a x i m a a n d m i n i m a for all v a r i a b l e s m e a s u r e d a n d . c a l c u l a t e d . Several o f these v a r i a b l e s p r o v e d to be s t r o n g l y c o r r e l a t e d with b o d y t e m p e r a t u r e a n d as the l a t t e r was f o u n d to v a r y b y at least 3 °C d u r i n g the course o f a day, regression e q u a t i o n s o f the v a r i a b l e on b o d y t e m p e r a t u r e gave a m o r e valid d e s c r i p t i o n t h a n overall means. C a l c u l a t e d regressions a r e given in t a b l e 2, t o g e t h e r with the significance level for the regression. B o d y t e m p e r a t u r e d u r i n g the o b s e r v a t i o n s was f o u n d to v a r y between 35.7 a n d

TABLE 1 Measured and calculated values for respiratory variables in three giraffe. Between 14 and 18 determinations were made on each animal, but not all variables were successfully measured on each occasion. The three giraffe had body weights of 570, 580 and 640 kg

Body temp. Minute volume, BTPS Oxygen consumption,

Units

Mean _+SE

Maximum

Minimum

n

°C ml. min -1 • kg -1 ml • rain -1 • kg -1

37.33 + 0.121 108.77 _+4.191 2.61 _+0.099

39.0 176.50 4.71

35.7 62.7 1.18

51 51 50

9.13 + 0.59 11.68 + 0.34 0.964 + 0.043 17.28 _+0.426

14.39 15.96 2.58 20.6

5.43 8.76 0.001 12.1

50 50 48 50

STPD

Respiratory frequency Tidal volume, BTPS Respiratory water loss Utilisation

min -1 ml - kg -1 g. min 1 /o°r

RESPIRATION AND METABOLISM IN THE GIRAFFE

145

TABLE 2 Calculated regression equations for some respiratory variables on body temperatures (y = a + bx) y

x

a + SE

b + SE

r

Significance level?

Respiratory frequency (min -1) Oxygen consumption (ml. kg - 1 min'-1,

body temp. (oc) body temp. (°C)

-62.37 4- 6.12

1.92 +_0.16

0.87

< 0.1~

-15.8 +_4.72

0.493 + 0.0025

0.65

< 0.1~

-831.59 _+107.03

25.17 + 2.87

0.78

< 0.1~o

-13547.42 + 3180.77

391.12+_85.48

0.56

< 0.1~o

.

STPD) Minute' Volume (ml. kg - 1, BTPS) Respiratory water loss (mg. rain - 1)

body temp. (°C) body temp. (°C)

38.8 °C with a m e a n of 37.2 °C. This v a r i a t i o n has been s h o w n using c o n t i n u o u s r a d i o t e l e m e t r y to have a 24 h p e r i o d a n d to follow the daily a m b i e n t t e m p e r a t u r e fluctuations. T h e o b s e r v a t i o n s o f b o d y t e m p e r a t u r e m a d e in this study showed a strong c o r r e l a t i o n with a m b i e n t t e m p e r a t u r e (r = 0.79, P < 0.01) (fig. 1), t h o u g h the m o r e extensive r a d i o t e l e m e t r y data indicated a phase lag o f a p p r o x i m a t e l y 2 h b e t w e e n changes in the two t e m p e r a t u r e s and, if this a d j u s t m e n t is made, the c o r r e l a t i o n is c o n s i d e r a b l y i m p r o v e d ( L a n g r n a n , in p r e p a r a t i o n ) . Relative h u m i d i t y ( R H ) was m e a s u r e d r o u t i n e l y using a wet a n d dry b u l b t h e r m o m e t e r . R H a n d a m b i e n t t e m p e r a t u r e were f o u n d to be strongly negatively correlated (r = - 0 . 9 4 , n = 50). T h e regression e q u a t i o n was R H = 156 - 3.98 T a m b where R H is a percentage a n d t e m p e r a t u r e is in °C. As a c o n s e q u e n c e o f this correlation, high b o d y t e m p e r a t u r e was associated with low R H . M e a n f was 8.95 = 1.86 m i n -1 with a range o f 5.43-13.37. This variable was 39

%

38

•

%

ee

•

37

36

mb

•

/

*

r :0.86

I Tamb 351 tl I I I I I I I I I I 10 12 I/~ 16 18 20 22 24 26 2B 30 32 a

Fig. 1. Regression of rectal temperature Tb on ambient temperature in three resting giraffe in the open. Ambient temperature variations were normal diurnal changes, and no attempt was made to apply artificial heat or cooling.

V.A. LANGMAN et al.

146

Respiratory 14

frequency

• -1 rnln

12

10

•

i

./

Rectal I 36

I 37

temperature I 38

I 39 ° C

Fig. 2. Regression of respiratory frequency against rectal temperature in three resting giraffe. Changes in rectal temperature followed changes in ambient temperature (see fig. 1).

strongly correlated with rectal temperature (r = 0.87, P < 0.1%) (fig. 2) so that a meaningful value for resting f can be given only for a defined body temperature. The mean rectal temperature was 37.2 °C and the corresponding value for f calculated from the regression equation was 9.02 min -1.

Tidal volume. VT values were highly variable and showed no significant correlation with body temperature (r = + 0.08). Mean VT was 7.00 L at BTPS with a range of 2.25-9.58 L. VT was unrelated to any of the environmental parameters measured and from our data the variations observed in VT cannot readily be explained or predicted. Ventilatory minute volume. Observations of ~" showed considerable scatter but were correlated with body temperature (r = 0.78, P < 0.01%). Mean observed value for V was 64.8 L • rain-1 (BTPS). Since the three animals differed slightly in weight the values for VT and ~? have been expressed as ml -kg -~ so that the data from all three animals could be fitted on the same plot (fig. 3). Oxygen consumption (~?o2). As might be expected, %?o2 was correlated with body temperature (r = 0.65, P < 0.1%). Conditions were not such as to give truly basal metabolism and this presumably accounts for a lot o f the scatter. Despite this, the correlation was significant, and over the observed body temperature range of 36-39°C there was a marked rise in ~?o2 (fig. 4). The mean observed value of Vo2 was 2.61 m l - k g -~ • rain -~, or 1.57 L - r a i n -~ for a 600 kg animal. The calculated

RESPIRATION AND METABOLISM IN THE GIRAFFE

147

Oxygen consumption 0.30

l.kg!hr I

0.25

0.20

~

i

0.15 • o.,o

Rectal temperature

3'6

' 37

3'8

39' o C

Fig. 3. Regression of respiratory minute volume on rectal temperature in three resting giraffe. Data are expressed as ml. kg -1 at BTPSto allow pooling.

Oxygen consumption i t ml'kg-1 rain -1

3

•=

|

• O o ~ • ~ ~ o° °

°

oe•

•

Rectal temperature 1

'

36

=

37

I

38

39 o C

Fig. 4. Regression of oxygen uptake (L. kg -1. rain-l, STEP) on rectal temperature in three resting giraffe.

value at a b o d y temperature o f 37.2 °C was 2.54 m l . kg ~ :min -l, or 1.522 L .min -l for a 600 kg animal. The observed Q~0 over the range 36-39 °C was 2.5.

Respiratory water loss (RWL) was surprisingly small, and was strongly correlated with b o d y temperature (r = 0.56, P < 0.1 ~ ) . Over the range examined the relationship a p p e a r e d to be linear, with a slope o f nearly 400 m g - min -l • °C -1, so that a

v.A. LANGMANet

148

al.

2.0 -Respiratorywater loss g.min-1

1.5

1.0

e

~

~

•

00

•

0.5

0

1

36

Rectal temperature I I 37 38 39 o C

I

Fig. 5. Regressionof respiratorywaterlosson rectaltemperaturein threerestinggiraffe. temperature rise of 3 °C caused almost a fourfold increase in R W L (fig. 5). However, the absolute amount of water lost in this way was very small. The calculated value for R W L at a body temperature of 37.2 °C is only 1.00 g - min-1 for a 600 kg giraffe, corresponding to 1.44 L in 24 h. This was of course obtained under resting conditions and an exercising giraffe would have a much higher rate o f RWL.

Util&ation varied between 12.1% and 22.8%, with an observed mean of 17.5%. There was no significant correlation between utilisation and body temperature. However, there was a significant positive correlation between utilisation and ~'o2 (r = 0.43, P < 1%).

ANATOMICALSTUDIES Tracheal volume was calculated in 36 giraffe from measurements of diameter and length. The results were then compared with those from other mammals using log-log plots of tracheal volume against L × G 2 (fig. 6) for giraffe and for the other species studied. There was no significant difference between these two lines and it must be concluded that the relationship between body weight and tracheal volume in giraffe is not significantly different from that found in other mammals, so that giraffe do not have unusually large dead space. Tracheal length. Log-log plots of tracheal length against L × G 2 give straight lines for giraffe ~/nd for the other mammals, but the relationships are significantly different

R E S P I R A T I O N A N D M E T A B O L I S M IN T H E G I R A F F E

deadspace(mr) 1 ~ ~ ~ s -

10000 1000

149

.~giraffe otherspp.

100 10 1 I

1

1

10

I

100 LxG 2

Fig. 6. Log-log plot of tracheal dead space (ml) against the weight-related quantity (length x body girth 2) for giraffe and other species. This quantity is a linear function of weight. See text for details.

100 - Length(cm) giraffe 10 -

~

1

~

I

,,,

10

I

100LxG2

Fig. 7. Log-log plot of tracheal length (cm) against the weight-related quantity (length x body girth2), for giraffe and other species, (fig. 7). The length of the trachea is greater in giraffe than in most mammals by a factor that increases with increasing size, so that a very large giraffe would have a trachea over twice as long as expected on the basis of body weight. As there is no difference in volume, clearly the giraffe has an unusually narrow trachea, and the ratio between length and diameter increases with body size.

Discussion The observed values for all respiratory variables are within the ranges predicted for 600 kg mammals by the equations of Stahl (1967). Table 3 gives predicted and observed values for some of the respiratory variables examined. These i:esults are clearly inconsistent with some statements reported in the literature, particularly as regards the rate and depth of ventilation. The inconsistency may be due partly to the fact that previous studies have all used animals that were to some extent stressed. One animal in the study by Patterson et al. (1965). collapsed and died during measurements, and it is likely that their practice of blindfolding the animal and tying it to a scaffolding seriously affected the results. The report of Hugh-Jones et al. (1978) is based on measurements made

150

V.A. L A N G M A N et al. TABLE 3 Comparison of predicted and measured values for respiratory variables

Variable

Respiratory frequency Tidal volume Minute volume Oxygen consumption

Units

min-1 L, BTPS L . rain -1, BTPS L • min -1, STPD

Prediction for 600 kg animal, mean ± SE

Measured mean ___SE

Range

Value at 37°C

10.14 5.94 63.06 1.50

9.13 7.01 64.84 1.57

5.43 5.25 37.56 0.71

8.67 7.01 59.82 1.46

± 4.05 +_ 2.67 _+ 28.38 _+ 0.45

___0.59 _+_+0.13 ___2.51 ___0.06

- 14.39 -- 9.50 -- 105.90 -- 2.83

on a single unhealthy giraffe, and the animal's condition probably significantly affected its ventilation. Some previous studies have also used inappropriate animals for comparison. Warren (1974) uses the term "hyperventilation" to mean "breathing more deeply and rapidly than man". We believe that the only valid basis for comparison is a statistical prediction based on a large sample of other mammals. With this method, and when using healthy unstressed animals, giraffe ventilation was in all respects as expected for a 600 kg animal. Furthermore, the anatomical evidence shows that the respiratory dead space is not abnormally large, so no special behaviour is required to compensate for it. On the other hand, the trachea is abnormally long and narrow. This would be expected to increase the work of breathing, but the effect is apparently not large enough to increase the oxygen consumption above that predicted, at least while the animal is at rest. It is possible that the resistance does become significant during exercise, and it may be that as suggested by Schroter (1978), aerodynamic effects of oscillating flow in a 10ng narrow tube limit the usefulness of a rise in respiratory rate, so limiting the giraffe's ability to run. However, anecdotal evidence and personal experience indicate that giraffe can run at 60 km/h for at least 5 rain, with no obvious signs of distress. It is noteworthy that over the small range studied, increases in minute volume were brought about by increasing respiratory frequency and not tidal volume. The labile body temperature of the giraffe has considerable effects on many of the measured variables. This is not surprising in view o f the close correlation between body temperature and Vo:, which would cause secondary changes in ventilation. Over the observed range of body temperature, f, Vo2 and V varied by a factor of about 2. This amount of variation means that the value of a respiratory variable has to be defined for a particular body temperature. The data in table 3 are therefore calculated for a temperature of 37.2 °C, the mean of all observations. Clearly this strong temperature dependence has important ecological consequences for food and water requirements. The savings in water resulting from a fluctuating body

RESPIRATION AND METABOLISM IN THE GIRAFFE

151

temperature have been described by Schmidt-Nielsen et al. (1957) and labile body temperatures have been shown in a number of East African mammals (Taylor, 1969, 1970; Maloiy, 1973). The ability to survive a high body temperature depends on maintaining brain-body temperature difference, usually with the aid of the carotid rete-cavernous sinus system, (Goetz and Keen, 1957; Taylor and Lyman, 1972) using the cool venous blood from the nasal mucosa. Goetz and Keen (1957) have reported a carotid rete in the giraffe and it seems likely that this method of water conservation is used. Recently Langman et al. (1979) have shown that cooling of the exhaled air by heat exchange in the nasal mucosa conserves about half the water that would be lost if air were exhaled at body temperature. The giraffe thus uses water very economically, a fact reflected in the low values for evaporative water loss. Sparing use of water is obviously important for an animal which is at its most vulnerable when drinking and which inhabits arid savannah. Oxygen utilisation by our giraffe did not vary significantly with body temperature, unlike that of eland (Taylor, 1969) in which utilisation increased at low body temperature. Taylor points out the usefulness of this response to an animal since it can reduce ventilation volume and hence respiratory water loss with no change in oxygen consumption. It could be argued that a high utilisation is equally useful whatever the body temperature, and there is little advantage in reducing it at high temperatures, through low utilisation may indicate increased deadspace ventilation in a panting animal. It should be noted that our giraffe did not pant at the temperatures reached in this study. The range of values measured in our study was similar to that reported by Taylor for both the eland and zebu steer. It appears that despite its unusual appearance, the giraffe has a respiratory physiology which is in most ways normal. Respiratory variables are all within predicted limits for an animal of this size, and so is the volume of the anatomical dead space. The only abnormal feature is the long narrow trachea, and there is at present no evidence that this has any effect on the ability of the giraffe to ventilate its lungs.

Acknowledgments This work was supported by grants from the University of Nairobi. Permits for capture and holding of giraffe were granted by the Kenyan Ministry of Tourism and Wildlife, for whose co-operation we are grateful.

References Goetz, R. H. and E. N. Keen (1957). Some aspects of the cardiovascular systemin the giraffe. Angiology 8 : 542-564. Hugh-Jones, P., C.E. Barter, J.M. Hime and M.M. Rusbridge (1978). Dead space and tidal volume of the giraffe compared with some other mammals. Respir. Physiol. 35 : 53-58.

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Langman, V.A., G. M. O. Maloiy, K. Schmidt-Nielsen and R. C. Schroter (1979). Nasal heat exchange in the giraffe and other large mammals. Respir. Physiol. 37: 325-333. Maloiy, G.M.O. (1973). The water metabolism of a small East African Antelope, the dik-dik. Proc. Roy. Soc. Lond. Ser. B 184: 167-178. McCulloch, J. S. G. and L. M. Talbot (1965). Comparison of weight estimation methods for wild animals and domestic livestock. J. Appl. Ecol. 2: 59-69. Patterson, J.L., R.H. Goetz, J.T. Doyle, J.V. Warren, O.H. Gaver, D.K. Detweiler, S.I. Said, H. Hsernicke, M. McGregor, E.N. Keen, M.H. Smith, E.L. Hardie, M. Reynolds, W.P. Flatt and D.R. Waldo (1965). Cardio-respiratory dynamics in the ox and giraffe, with comparative observations on man and other mammals. Ann. N.Y. Acad. Sci. 127: 393-413. Robin E. D., J.M. Corson and G. J. Dammin (1960). The respiratory dead space o f the giraffe. Nature (London) 186: 24-26. Schmidt-Nielsen, K., B. Schmidt,Nielsen, S.A. Jarnum and T.R. Houpt (1957). Body temperature of the camel and its relation to water economy. Am. J. Physiol. 188:103-112. Schroter, R.C. (1978). Convective flows in mammalian lungs. In: Comparative Physiology: Water, Ions and Fluid Mechanics, edited by K. Schmidt-Nielsen, L. Bolis and S.H.P. Maddrell. Cambridge University Press, pp. 303-325. Stahl, W. R. (1967). Scaling of respiratoJ:y variables in mammals. J. Appl. Physiol. 22: 453460. T,ay!or, C . R . (1969). Metabolism, respiratory changes and water balance of an antelope, the eland. Am. J. PhysioL 217: 317-320. Taylor, C. R. (1970). Strategies of temperature regulation: effect on evaporation in East African ungulates. Am. J. Physiol, 219: 1131-1135. Taylor, C.R. and C.P. Lyman (1972). Heat storage in running antelopes: independence of brain and body temperatures. Am. J. Physiol. 222:114-117. Warren, J.V. (1974). The physiology of the giraffe. Sci. Am. 231 : 96-105.