Camp. Biochem. PhysioJ. Vol. SlA, No. 2, pp. 335-340, 1985 0300-9629/85 $3.00 + 0.00 Printed in Great Britain 0 1985 Pergamon Press Ltd

THERMOREGULATION AND HEAT BALANCE IN THE DTK-DIK ANTELOPE (RHYNCHOTRAGUS KIRKI):

A FIELD AND LABORATORY STUDY

J. M. Z. KAMAU and G. M. 0. MALOIY

Comparative Animal Physiology Research Unit, Department of Animal Physiology, University of Nairobi, Kenya

(Received 5 October 1984)

Abstract-l. Experiments were conducted in the field to study the physiological responses of dik-dik antelope to direct solar radiation and shade. The results were compared to those obtained in the laboratory.

2. The rates of metabolic heat production when the animals were exposed either to the sun or the shade were identical.

3. Dik-dik antelopes lost about 50% more heat evaporatively when exposed to the sun compared to the shade at an ambient temperature (T,) of 28°C or a T, of 40°C in a climatic chamber.

4. Heat storage in the laboratory at ?,4O”C or at T, 28% in the shade accounted for between 30 and 35% of the total heat production. The corresponding value in the sun was 5.5%.

5. The net rate of heat gain under the sun was four times greater than under shade at 28°C or in the laboratory at 40°C.

6. Behavioural mechanisms for avoidance of high insolation must constitute important adaptations that the dik-dik uses to avoid dehydration and dependence on drinking water in their natural environment.

INTRODUCTION

Most East African wild and domestic ungulates are inhabitants of arid and semi-arid areas, where they are exposed to intense solar heat load and high temperatures during the day. Few physiological stud- ies on these bovids have been carried out in the field. Physiological studies on thermoregulatory processes have mainly been carried out in the laboratory where ambient temperature and relative humidity are the only major input used to elicit physiological re- sponses. This is not surprising since ambient tem- perature is such an easily controlled variable. Al- though the use of air temperature continues in thermoregulatory studies, it is recognized that one cannot extrapolate laboratory findings directly to what actually happens in the outdoor environment without making serious errors in interpretation.

Studies on the energy budget analysis by assessing components of heat fluxes to and away from an animal in the field (Porter and Gates, 1969; Finch, 1972, 1976) have been useful especially when dealing with very large animals like cattle and giraffes but the variables and constants involved, to use the words of Bakken (1980) “impede intuitive understanding” of the basic problem to be tackled. Studies on heat exchange in wild and domestic goats (Borut et al., 1979; Finch et al., 1980) have indicated that the use of the heat flux analysis over-estimated the mag- nitude of heat gained from the desert environment and the method was not as simple and accurate as an alternative method, the “heat balance” method (Finch et al., 1980). The use of these two methods and also that for estimating the standard operative tem- perature (Gagge, 1940; Bakken, 1976, 1980) may, when extensively tested, provide the best way to

enable the effects of the complex outdoor environ- ment on thermoregulation and heat balance to be properly quantified.

The dik-dik antelopes are small ungulates inhabit- ing arid, semi-arid and bush country in East, Central and South-West Africa. They are reported to survive where drinking water is unavailable (Tinley, 1969). They encounter intensive solar radiation, particularly during the hot seasons of the year. Their adaptive strategies have been studied (Maloiy, 1973; Musewe et al., 1976; Hoppe et al., 1975; Maskrey and Hoppe, 1979) in laboratory experiments.

No physiological studies have been conducted in the field to assess the effects of solar heat loads on this small antelope. This study sought answers to the following questions:

(a) What are the physiological responses of dik- dik antelopes exposed to direct solar radiation and shade in their natural habitats?

(b) How do these responses compare with those obtained in the laboratory at thermoneutrality and after exposure to high T,?

(c) What are the possible reasons for the simi- larities and differences observed?

To answer the above questions three measurements were made: (i) fur, skin and rectal temperatures; (ii) rate of metabolic heat production, respiratory fre- quencies and total evaporative water loss; (iii) heat balance profile. While those measurements were be- ing made on the animals, the following meteoro- logical data was collected at the site of the experi- ment: air temperature, wind speeds, solar radiation, ground temperature and relative humidity.

A brief report of this work has already been published (Kamau and Maloiy, 1981).

335

336 J. M. Z. KAMAU and G. M. 0. MALQIY

MATERIALS AND METHODS

Animals

Three adult male dik-diks were moved from the labora- tory in Nairobi to the field station and accommodated in a 50 m2 chain-link covered free run with enclosed accommo- dation for the night. The enclosure was strong enough to keep away predators. Experiments started after two weeks, the intervening period being allowed for the animals to get used to the area and the meteorological measurements to be taken to determine the most suitable time for conducting the experiment during the day. The field station was situated 40 km south of Nairobi (Isenya-Kajiado, Lat. l”50’ S, Long. 36”40’ E).

Procedure

The adopted daily routine during the experiment was to take the rectal temperature of the experimental animals on a particular day at 11 a.m. The animal to be experimented upon was then weighed and placed in an experimental area consisting of a round chain-link enclosure 1.5 m in diameter. To provide shade, a sack was placed 2 m over the enclosure. Each day one animal in turn was used in the experiments. A single experimental run consisted of six 15-min periods during which rectal, skin and fur temperatures of the animal were taken in that order, followed by measurement of oxygen uptake. During each of these periods ground tem- perature, air temperature, wind speed, relative humidity and solar radiation were recorded. If there were too many clouds on any particular day, or part of the day, experiments were stopped. Each animal participated for at least 3 days in the shade and 3 days in the sun.

Measurements on the animal

Rectal (T,), fur (T,,) and skin (Tskin) temperatures were measured with YSI Telethermometer ModePTD using ap- propriate thermistor probes previously calibrated in oil against a mercury thermometer. T, was taken 8 cm deep. Tskin and T,, were measured on the flank on the side facing the sun. Total evaporative water loss (TEWL) was deter- mined by taking hourly differences in weight loss from the animals, using a top loading pan balance (Sartorius Type 2255) with a capacity of 7 kg and capable of weighing to the nearest 0.1 g. Respiratory frequencies were measured visu- ally by watching the movement of the flank for short periods and timing with a stopwatch. To measure metabolic rate, an open flow system (Withers, 1977) was used. The animals wore face masks, which were ventilated at the rate of 800-900 I/hr. A portion of the ex-current air was delivered to a portable oxygen analyser (Taylor Servomex Model A0.024) calibrated between 16 and 21% with pure nitrogen and dried air as standard gases. The rate of oxygen con- sumption (voz) was calculated using the equation:

po2 ml 0, hr-’ = VE (Fio, - FeoJ

1 - Fio, + RQ (Fi,,) Where VE = rate of air flow through the mask, Fi,, = fractional concentration of oxygen going into the mask and Fe,, = fractional concentration of oxygen leaving the mask. RQ = respiratory quotient. vo’,, values were con- verted to rate metabolic heat production (Ei,,,,) by as- suming an RQ of 0.86 and that when 1 litre of oxygen is used in oxidative metabolism, 5.56 watts are liberated. Similar methods were applied in the laboratory measurement at controlled T, between 14 and 42°C.

Meteorological measurements

Air, ground temperatures, relative humidity, solar radi- ation and wind speeds were measured at 15 min intervals during the experimental period. Air temperature was mea- sured with a mercury thermometer placed in a Stevenson’s screen which also housed the minimum and maximum thermometers. Relative humidity was measured by a whirl-

ing psychrometer, while wind speed was recorded at 30-min intervals using a Ccup anemometer raised 2m above the ground. Diffuse and direct solar radiation and also radiation from the ground was measured using a Solarimeter (Kipp and Zonan) mounted 40 cm above the ground. These instru- ments were checked and calibrated by the Kenya Meteoro- logical Department before and after the experiments.

Heat balance

Details will be found in Finch et al. (1980). The essential steps will be explained. An animal in its natural environment gains heat through metabolic heat production (Ijmetab) and absorption from the external environment (&,). The ani- mal will at the same time be losing heat by evaporation (ri,,,,), convection (&,,,) and by radiation (I-i,,). The temperature of the body core may then remain steady or change when heat is gained or lost (k &,,). I-i,,,, was calculated according to Taylor et al. (1971) and assuming specific heat capacity of tissues of 0.96 W kg-’ “C-i. In equation form:

(1)

Ijgain = i?_& - fi& - fi_.

Substituting equation (2) into equation (1):

(2)

I-i,in = fievap + Hstoi,,,, - Eimetab (4)

By measuring the three simple components of this equation, metabolism, evaporation and heat storage, the magnitude of the heat load from the external environment could be assessed. It is important to note here that avenues of heat gain or loss by radiation and the losses by convection are pooled together, thus making it difficult to directly assess the radiative component which is the greatest heat input in the equation. However, for a small animal like the dik-dik, the avenue of heat loss by convection is perhaps minimal or negligible considering that wind velocity at a height of 30 cm above the ground (shoulder height) may be dismal (Monteith, 1973).

RESULTS

The environment

Table 1 depicts the prevailing environmental condi- tions at the field station during the five weeks of experimentation. “Sun” or “Shade” indicate the pre- vailing experimental conditions during the various experiments. T, variation during the day from 11.00 a.m. to 3.30 p.m. local time are also shown (Fig. 1). No significant differences were observed in Ta during the execution of the experiments under the sun or shade.

Rectal and surface temperatures

Figure 2 depicts the mean T, achieved during the experiments with the animals in the sun or under the shade. The animals started with an average T, of 38.7”C at 9.00 a.m. Exposure to the sun led to a rise in T,, which quickly reached 40.6”C and remained elevated for the rest of the experimental period. The daily range recorded during the experiments was 39.542”C. Experiments conducted with the animals under the shade showed similar patterns-a rapid rise in T, between 9.00 and 11 .OO a.m. with maintenance of T,, of 39.9”C during the rest of the day.

Thermoregulation and heat balance in the dik-dik 331

Table 1. Ambient temperature, solar radiation, wind speeds and relative humidity (mean rt SD, ranges shown in brackets) at the field station during the experimental periods with the animals standing

under the shade or in direct sunlight

Ambient environmental Animals standing in position conditions SUII Shade

Ambient temperature (“C) 27.8 f 0.2 27.4 + 0.5 (24-31.5) (22-31.0)

Wind speed (m see-‘) 0.41 & 0.1 0.36 + 1 (0.06-l) (0.06-l)

Relative humidity (%) 36 f 3 34+4 (20-50) (20-50)

Solar radiation (Wm-*) 978 5 20 974 + 22 (900-1050) (900-1050)

T,, and Tskin are also shown in Fig. 2. In the sun, large variations were noted in both Tskin and T,,. However, T,, was on the average 2-3°C above Tskin. In the shade, the observed Tskin and T,, changes were identical and subject to less variations than in the sun. In the sun and under the shade T, was found to be higher than Tskin. But when the animals were exposed to the sun, T,, was always higher than T,,.

Total evaporative water loss (TEWL)

This, like Tskinr increased linearly with increasing respiratory frequency (Fig. 3). The vertical intercept, in case of TEWL, at ‘zero’ respiratory rate indicates the non-respiratory contribution to the total amount of evaporative water loss.

Heat balance

Figure 4 shows the measured components of the heat balance equation for the animals standing in the sun or shade and also results of laboratory studies on the same animals at T, 28 and 40°C. fimetab was similar whether the animals stood in the sun or under the shade, 3.02 vs 3.06 W kg-’ respectively. hPi, in the sun was, however, four times more than in the

42

38

36 -

Local time (hr)

Fig. 2. In the sun large variations in Tskin (e---O) and T,, (a-0) were evident as shown by the very large standard deviation. Mean rectal temperatures (a---A) were stable and always between T,, and T,,,. In the shade T,, and T,, closely followed each other. Mean rectal temperatures were stable and on average 5-9°C above T,,

and T,,.

I I I I

100 200 300 400

Resp. rate (min-’ )

Local time (hr) Fig. 3. Total evaporative water loss (TEWL) ghr-’ and skin temperatures are plotted against changes in respiratory

Fig. 1. Ambient temperature (T,) at the field station be- tween 11 .OO a.m. and 3.00 P.m. local time (mean i SD)

frequency (R,,) for both “shade” and “sun” experiments. The equations describing the linear relationship are: TEWL

during the periods when the experiments were conducted ghr-r = 10 + 0.08 with the animals under the shade or in direct sunlight.

R,,,, N = 30, r = 0.89 and R,, min-’ = 34.38 Tskin - 1095.7, N = 50, r = 0.80.

338

4

2

6 Y YI E

z 4

2

.O r Laboratory

1 O I Lab (28°C)

J. M. Z. KAMAU and G. M. 0. MALOIY

Field

lade (28°C)

Fig. 4. Heat balance profile for the animals in the field (under shade or sun at T, of 28°C or in the laboratory at T, 28 or 40°C). The measured parameters, metabolic rate (M) and evaporative heat loss (E) are shown with their standard deviations. The calculated components, non- evaporative heat loss (NE), heat gain (G) and heat storage

(S) are also indicated.

shade at 28°C. In the sun, dik-diks lost 50-60x more heat by evaporation as compared to the shade or laboratory at a T, of 40°C. In the laboratory at T, 40°C and under the shade at T, 28°C 3&35x of lljmetab was stored. The corresponding value in the sun was about 55%. In the laboratory at 28°C Eimetab was around one-third lower than in the sun or under the shade. No heat was stored but the animal lost 50% of its total heat production non-evaporatively. A net negative rate of heat gain of 1 .OO W kg-’ was evident compared with a net gain of 0.85 W kg-’ at a T, of 40°C.

DISCUSSION

Air temperatures between 24 and 32°C were recorded in the field experiments. This is within the range where the oxygen uptake was shown to be minimum (Maskrey and Hoppe, 1979) under labora- tory conditions. The term “thermoneutrality” needs to be applied with caution for, in the field experiment at 28°C the dik-dik did not only have a higher metabolism and rectal temperature, but also had increased rates of evaporative water loss. This is evident from our results on the heat balance (Fig. 4).

One of the important but unresolved problems in thermoregulation is how to extrapolate laboratory findings to the actual conditions prevailing or en- countered in outdoor environments. We suggest here that the physiological responses of a dik-dik antelope

under various environmental field conditions and controlled laboratory environments would indicate the ‘equivalent’ temperature under these conditions. To illustrate this, we observed in laboratory experi- ments respiratory frequencies of about 480 breaths min-’ after exposing dik-diks to a T, of 44°C for over 90min (Kamau and Maloiy, in preparation). Under these circumstances, T,,, averaged 40.8”C. In the field at midday, respiratory frequencies of nearly 450 breaths mm’ and rectal temperatures of 40.5”C were achieved at a T, of 27°C and Tskin of 38°C (Figs 1 and 2). Changes in T,, and respiratory frequencies at a i”a of 44°C in the laboratory elicited nearly the same physiological responses to heat as T* of 27°C plus intense solar radiation in the field. The two environ- mental heat loads were, in this respect, ‘equivalent’.

One important finding that arises from this study is that the observed physiological changes are not being elicited by air temperature per se. What are the thermoregulatory and heat balance features that are common both to the field and laboratory environ- ment? In the laboratory at a T, of 44°C the tem- perature of the skin over the trunk was 38°C (Kamau and Maloiy, in preparation). The same skin tem- perature was measured in the field when the air temperature was only 27°C. Thus, the air tem- perature in the laboratory that evoked a similar physiological heat loss response in the field was 17°C higher within the Ta ranges given.

That a dik-dik should respond physiologically in the same manner due to completely different ambient temperatures may be explained by an examination of Fig. 2. In the field under the sun, at 12.30p.m., the temperature of the fur coat may be on average as high as 44°C while that of the skin and rectum are only 39 and 40.8”C respectively. The air temperature is about 28°C. One would intuitively expect the large tem- perature gradient between the fur coat and/or skin to be of some use in dissipating heat from the animal to the much cooler environment, but the situation is somewhat different; heat should flow from the fur coat towards the skin and the environment and from the core to the skin (Fig. 5). We see no reason for the skin temperature to change unless the temperature of the fur coat or the body core changes (fur tem- perature may well change by connective means). At an air temperature of around 28°C the animal stand- ing in the sun will be surrounded by air trapped between the fur. This would seem to be the tem- perature which evokes physiological defences against heat in the laboratory at 44°C as well as in the field. Under such conditions, if the animal does not sweat, then it must use the respiratory system efficiently, as is clearly demonstrated in this study. The present study supports that by Finch (1972) in her studies on two East African antelopes, the hartebeest and the eland. She stated that “evaporative thermoregulatory responses to heat conducted to the animal appear to vary in relation to changes in skin temperature and not in relation to the changes in body temperature”. It is important to point out here that the two studies were carried out in the same ecological zone. The thermal behaviour of the fur coat of the dik-dik seems to differ from that of the awassi, merino sheep and zebu cattle (Macfarlane, 1968). Despite the fact that the experiments were conducted at T, of 40°C the

~e~o~guiation and heat balance in the dik-dik 339

Core-40.8”C

(a) Sun (b) Shade

Fig. 5. Temperature characteristics of the fur coat, skin and core of the dik-dik when exposed to the sun and the shade. The temperature trapped in between the hairs seems to evoke physiological defences against beat in the field and

!aboratory.

skin temperatures were always higher than the core temperatures.

Experiments conducted with the dik-dik under the shade showed that Tskin was approximately equal to T,,. At 1.00 p.m. Tsk,” and T,, were 34°C when Ta was 28°C. Similar surface temperatures were found at i”, of 28°C in the iaboratory (Kamau and Maioiy, in preparation). Under these en~ronment~ conditions, however, T,, was quite different with T, recorded in the laboratory being 1.&1.5”C lower than those in the field. Our findings support those of Finch (1972), even though her study was carried out on a larger antelope, the hartebeest. The differences in core tem- perature in the laboratory and under the shade reflect reradiated insolation from the surrounding environ- ment which seems to be more than the loss to the immediate environment and the clear sky. This point is illustrated clearly by the heat balance profile (Fig, 4), where the heat balance at 28°C in the shade is similar to that at 40°C in the laboratory. However, one major difference noted here is in the method of heat dissipation. Whereas in the laboratory heat loss by evaporation was the most important avenue of heat loss, in the field with the animals shaded most of the heat was lost non-evaporatively because of the favourable temperature gradient between the skin and the environment. At 40°C in the laboratory this temperature gradient was almost completely abol- ished.

From the foregoing account and also from studies by Finch (1972) on the two larger antelopes, the eland and hartebeest, it is evident that the temperature of the skin largely drives the physiological responses of these wild ungulates against solar heat loads. What single factor could best indicate the integrated effects of solar radiation, air temperature and wind speed? The best and simplest microclimatic measurement seems to be ground temperature (Fig. 6). A very high correlation between ground and Tskin over the tem- perature ranges recorded at the experimentai site was evident. This observation has been made before in

Fig. 6. Skin temperature (Tskin) varied directly with ground temperature Tgnd ranging from 34 to 50°C. The two param- eters had strong Iinear relationship as evident from the equation:

Tskin = 11.31 + 0.66 Tend, N = 52, P = 0.73.

gulls (Bartholonew and Dawson, 1979) and also in ground squirrels (Chappell and Bartholomew, 1981). The latter researchers stated that “ground tem- perature most closely tracked standard operative temperature”.

Our observation that the heat balance under the shade at 28°C was similar to that in the laboratory at a T, of 40°C was surprising and only helped to ~ghlight the danger of extrapolating laboratory data to field situations. Under field conditions dik-diks may not, after all, be as highly adapted to their harsh environment as suggested by several laboratory stud- ies. They must depend on behavioural thermo- regulation by seeking shade. With the increasing human population and accelerated a~icultural activ- ities in the semi-arid areas there may soon be no shade for the dik-dik, as more of them will be pushed to more unfavourable habitats.

Acknowledgements-We wish to thank the Director, the Department of Wildlife Conservation and Management (Kenya) for providing us with the necessary permits, Mr Muchemi of the Meterorologic~ Department (Kenya) for loaning and checking of some of the meteorological instru- ments, Messrs S. K. Kamau and P. Githaka for taking care of the animals in the field, and Mrs Fay Frost for typing.

This study received financial support from the Dean’s Committee, University of Nairobi, to J. M. Z. Kamau and Leverhulme Trust, London, to G. M. 0. Maloiy.

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