Muguga, P.O. Kabete, Kenya, and Museum of Comparative
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1 J. Physiol. (1969), 23, pp With 3 text-figurew Printed in Great Britain A COMPARISON OF SWEAT GLAND ACTIVITY IN EIGHT SPECIES OF EAST AFRICAN BOVIDS BY D. ROBERTSHAW* AND C. R. TAYLORt From the East African Veterinary Research Organization, Muguga, P.O. Kabete, Kenya, and Museum of Comparative Zoology, Harvard University, U.S.A. (Received 3 December 1968) SUMMARY 1. The pattern and control of the sweat glands of eight species of wild bovids has been studied. 2. Heat exposure resulted in changes in cutaneous moisture loss which showed considerable species variation. Duiker, Grant's gazelle, Thomson's gazelle and oryx all demonstrated periodic discharges of moisture on to the surface of the skin. Defassa waterbuck and eland exhibited discharges which were accompanied by a gradual rise in basal level. Buffalo showed an immediate large increase which was sustained during the period of heat exposure. Three wildebeest displayed small fluctuations whilst a fourth animal showed a step-wise increment in cutaneous moisture loss. 3. The intravenous infusion of adrenaline into the buffalo and one wildebeest caused an increase in cutaneous moisture loss, the magnitude of which was directly related to the size of the dose administered. In three other wildebeest, and all other animals tested, a single injection of adrenaline was necessary to cause a discharge of moisture on to the surface of the skin. Noradrenaline was without effect. 4. Heat-induced but not adrenaline-induced sweating was inhibited by the intravenous administration of an adrenergic neurone blocking agent, bethanidine. 5. It is concluded that the sweat glands of the wild bovids studied are under adrenergic neurone control, in common with the domestic bovids previously studied, and that there is no correlation between the pattern of sweating and the phylogenetic position of the species. * Present address: Department of Veterinary Physiology and Biochemistry, University College Nairobi, Box 3197, Nairobi. t Present address: Department of Zoology, Duke University, Durham, North Carolina Box 2776, U.S.A.
2 136 D. ROBERTSHA W AND C. R. TA YLOR INTRODUCTION Domestic ruminants exhibit two patterns of sweat gland activity upon heat exposure. Cattle show a step-wise increase in cutaneous moisture loss until a continuous output is achieved (McLean, 1963a), and in this species it is known that cutaneous moisture loss is the major avenue of evaporative cooling (McLean, 1963b). Sheep and goats show discrete discharges of moisture on to the surface of the skin (Bligh, 1961; Waites & Voglmayr, 1963; Robertshaw, 1968), and it appears that evaporative cooling from the skin is negligible in these species (Robertshaw, 1968). Although the sweat glands of domestic ruminants exhibit different patterns of activity they are all controlled by adrenergic sympathetic nerves (Findlay & Robertshaw, 1965; Robertshaw, 1968). Simpson (1945) divides the family Bovidae into six subfamilies. Cattle belong to the subfamily Bovinae while sheep and goats belong to the subfamily Caprinae. Representatives of the remaining subfamilies were investigated in the present study. All of the species examined possess sweat glands (D. McEwan Jenkinson, personal communication) and all are indigenous to equatorial Africa. The present experiments were designed to examine (1) the response of sweat glands to heat exposure, (2) the control of the sweat glands, and (3) a possible relationship between sweat gland activity and the phylogenetic position of the species. A brief report of this work has already been published (Robertshaw & Taylor, 1968). METHODS Two animals of each of the following species were used: duiker (Silvicapra grimmia, mean wt. 6-8 kg), Thomson's gazelle (Gazella thomsonii, mean wt kg), Grant's gazelle (G. granti, mean wt. 25 kg), Defassa waterbuck (KobW8 defa8sa, mean wt. 1 kg), oryx (Oryx bewia, mean wt. 11 kg), eland (Taurotragu8 oryx, mean wt. 21 kg), and buffalo (Synceru8 caffer, mean wt. 24 kg). Four wildebeest (Connochaetes taurinws, mean wt. 15 kg) were also used. Animals wvere exposed to various ambient temperatures in the temperature controlled room described by Taylor & Lyman (1967). Changes in cutaneous moisture loss were detected by means of a ventilated capsule (McLean, 1963 c) placed on an area of shaved skin overlying the 8th or 9th ribs, approximately midway between the thoracic spinous processes and the sternum. Air was drawn through the capsule at a rate of 1 1./min. Results were expressed as the difference in wet bulb temperature of lte capsule and room air (A' C) which was continuously recorded on a recording potentiometer. Cutaneous moisture loss was quantitatively measured from a similar position on the other side of the animal using a desiccant capsule as described by Taylor & Lyman (1967). Drugs were administered through a cannula made of polyvinyl chloride (Portex Ltd, Hythe, Kent, Bore 1-19 mm, external diameter 1-7 mm) inserted aseptically, under local anaesthesia into the jugular vein on the day before the experiment. The drugs used during these experiments were adrenaline hydrochloride, noradrenaline bitartrate, and bethanidine sulphate.
3 SWEATING OF BOVIDS 137 RESULTS Effect of heat exposure. All animals showed some degree of sweat gland activity when exposed to ambient conditions of 4 C (dry bulb), 23 C (wet bulb). Buffalo increased cutaneous moisture loss suddenly and a constant level with small and occasionally large changes in amplitude was rapidly attained (Fig. 1). The buffalo had the highest cutaneous moisture Buffalo (mean wt. 24 kg) Eland (mean wt. 21 kg) Waterbuck (mean wt. 1 kg) Oryx (mean wt. 11 kg) Thomson's gazelle (mean wt kg) Grant's gazelle (mean wt. 25 kg) Duiker (mean wt. 6-8 kg) 6 F U 4- <12t U 4 -<2L <2 L r k 2 - L<2, 12 _ Cutaneous moisture loss (g/m2 hr) Time (min) Fig. 1. Records of cutaneous moisture loss at the onset of sweating made with a ventilated capsule and measurements of cutaneous moisture loss using a desiccant capsule of various East African bovids exposed to ambient conditions of 4 C (dry bulb), 23 C (wet bulb). loss when equilibrated at 4 C of any of the species studied (about 25 g/m2.hr). Eland and waterbuck increased cutaneous evaporation in small 'steps' (Fig. 1). Fluctuations in moisture loss were still present when sweating had reached a constant level (at about 2 g/m2. hr in the eland and about 1 g/m2.hr in the waterbuck). The oryx sweated in small bursts at a frequency of 12-27/hr (Fig. 1). Cutaneous evaporation decreased to nearly the initial level between each discharge, however, its sweat rate was about the same as that of the waterbuck (1 g/m2.hr). The Thomson's gazelle, Grant's gazelle and duiker also sweated in small bursts (Fig. 1).
4 138 D. ROBERTSHAW AND C. R. TAYLOR The frequency of discharge, however, was only 6-9/hr and the amplitude of the individual discharges was less than that observed in the oryx. At 4 C cutaneous moisture loss from these three species was approximately half of that observed from the oryx (Fig. 1). One wildebeest showed definite sweat gland activity with a stepwise increase in moisture loss similar to that observed in the eland and waterbuck (Fig. 2). This wildebeest had a mean cutaneous moisture loss of about 12 g/m2.hr. Three other wildebeest showed only small oscillations in cutaneous moisture loss (Fig. 2). These animals had a mean cutaneous moisture loss of only about 6 g/m2. hr. Wildebeest I Wildebeest 2, 3 and 4 U Z ~ ~ L l IlI I l Cutaneous moisture loss Time (min) (g/m2. hr) Fig. 2. Records of cutaneous moisture loss at the onset of sweating made with a ventilated capsule, etc., from two groups of wildebeest exposed to ambient conditions of 4 C (dry bulb), 23 C (wet bulb). Effects of adrenaline or noradrenaline administration. All animals sweated in response to intravenous adrenaline administration when equilibrated at an ambient temperature of 3C. Infusions of 8,jg adrenaline/kg. min induced sweating in the buffalo. Further increases in the rate of infusion produced additional increases in cutaneous moisture loss. The single wildebeest which sweated in response to heat sweated when adrenaline was infused at a rate of -25,zg/kg. min and the rate of sweating was increased at higher rates of infusion (Fig. 3). The remaining three wildebeest, the duiker, the Thomson's gazelle, the Grant's gazelle, the oryx, the Defassa waterbuck, and the eland did not sweat when adrenaline was infused at rates up to 1 ug/kg. min. Single injections of 5,sg adrenaline/kg, however, always produced a large increase in cutaneous moisture loss (Fig. 3). This rapidly returned to the pre-injection level in all species except the eland. The moisture loss from the eland remained elevated for at least 3 min after the injection. None of the animals showed any change in cutaneous moisture loss after the administration of noradrenaline at infusion rates up to 1 /tg/kg. min or single injections of 5,tg/kg body -weight.
5 SWEATING OF BOVIDS 139 Effects of bethanidine administration. Intravenous administration of 2 mg bethanidine/kg body wt. to the buffalo and 1 mg/kg to all other animals effectively inhibited any sweat gland activity caused by exposure to an ambient temperature of 4 C. The small oscillations in cutaneous moisture loss observed in wildebeest nos. 2, 3 and 4 upon heat exposure (Fig. 2) were also inhibited. Adrenaline administered in the manner described above was still an effective sudomotor stimulus in animals which had received bethanidine. Noradrenaline administration produced no change in cutaneous moisture loss whether given by infusion or single injection. iv. adrenaline infusion i 25,ug/kg.min O5#g/kg. * 4 Wildebeest I min a2 Wildebeest 2, 3 and 4 Adrenaline 5 fug/kg a Time (min) Fig. 3. Records of cutaneous moisture loss from the same wildebeest as in Fig. 2 exposed to ambient conditions of 3 C (dry bulb), 2 C (wet bulb). DISCUSSION While all the bovids investigated sweat in the heat, there are differences both in magnitude and pattern of sweating. At 4 C cutaneous evaporation from the buffalo is almost eight times that from the duiker. The pattern also varies from the sudden large increase observed in the buffalo to the small bursts observed in the duiker. High rates of cutaneous moisture loss are usually associated with a continuous high level of evaporation with small oscillations. This was observed in buffalo, eland, waterbuck, and one wildebeest (Fig. 1). This is similar to what has been previously described for the ox (McLean, 1963a). Bligh (1967) has proposed that the pattern of cutaneous moisture loss seen in cattle is due to myoepithelial contractions superimposed on a greatly increased sweat secretion. Thus in an animal
6 14 D. ROBERTSHA W AND C. R. TA YLOR equilibrated in the heat, the sweat gland leaks moisture onto the skin surface continuously. The myoepithelial contractions then cause small oscillations in sweat rate. Such an explanation could explain the pattern of sweating observed in the buffalo, eland, defassa waterbuck, and one wildebeest. Bligh also proposed that the pattern of sweat gland activity seen in sheep is due to synchronous contractions of the myoepithelium producing periodic discharges of luminal fluid onto the surface of the skin. These discharges, however, are not accompanied by any large increase in sweat secretion and there is no leakage of sweat onto the skin between contractions. This explanation could also apply to the observations on oryx, Thomson's gazelle, Grant's gazelle and duiker. The oryx, however, achieves the same rate of cutaneous moisture loss as the waterbuck while having a pattern similar to that described in sheep and goats (Robertshaw, 1968) and that observed here in the gazelles and duiker. Using Bligh's hypothesis the differences between the oryx and the cattle type of sweating would have to be explained either by a more complete contraction of the myoepithelium or a larger sweat gland lumen in the oryx, since frequency of bursts in the oryx is approximately the same as the frequency of oscillations in cattle. Heat-induced sweating in all of the species investigated appears to be under adrenergic neural control since it is inhibited by the adrenergic neurone blocking agent, bethanidine. It has been shown previously that the heat-induced sweating of domestic ruminants is also blocked by bethanidine administration (Findlay & Robertshaw, 1965; Robertshaw, 1968). These authors demonstrated that bethanidine administration simulates the effect of sympathectomy and concluded from this evidence that the sweat glands of the ox are controlled by adrenergic nerves. Bethanidine does not prevent the release of adrenaline by the adrenal medulla (Boura & Green, 1963) and since intravenous adrenaline administration is still an effective sudomotor stimulus after bethanidine administration it may be assumed that the adrenal medulla does not make any significant contribution to normal thermal sweating. Findlay & Robertshaw (1965) and Robertshaw (1968) came to similar conclusions with respect to the sweat glands of domestic bovids. Since the oscillations in cutaneous moisture loss observed in the three wildebeest which did not appreciably increase their rate of cutaneous moisture loss in the heat were abolished by bethanidine administration, it would appear that these oscillations are due to sweat gland activity controlled by adrenergic nerves. One object of this study was to investigate a possible correlation between the pattern and magnitude of sweating and the phylogenetic position of a species within the family Bovidae. Table 1 divides the species
7 m O SWEATING OF BOVIDS - -Qe C Reso In ~ t. To d >- 4.o Z ED 4-'3aco *6 E m 3 X4 C).; L Er s!_>x 141 E- a p I"- O
8 142 D. ROBERTSHA W AND C. R. TAYLOR which were investigated into the subfamilies of the family Bovidae according to Simpson (1945). No correlation between phylogenetic position and pattern of sweating is present. For example, within the subfamily Hippotraginae, the waterbuck sweats in a manner similar to cattle, the oryx sweats in discrete bursts, and individual wildebeest sweat in different ways. A correlation exists, however, between cutaneous moisture loss/m2. hr at 4 C and the adult size of an animal (Fig. 1). The smaller animals dissipate most of their excess heat through the respiratory tract while the larger animals dissipate most of their excess heat through cutaneous evaporation (C. R. Taylor, in preparation). Not enough information is available to devise a suitable scheme which explains the relationship between rate of sweating and the adult body mass of a bovid. However, at an ambient temperature of 4 C, the surface where evaporation takes place must be cooler than body temperature for an animal to maintain a constant body temperature. The skin of an animal which sweats must, therefore, be considerably cooler than the temperature of the environment. The skin of an animal that pants, however, could equal or possibly exceed that of the environment. Thus, the environmental heat load would be less for an animal if it dissipated all its heat by panting rather than by sweating. It has often been stated that panting involves a greater expenditure of energy than sweating and thus additional metabolic heat is generated which must be dissipated by evaporation. Two recent studies by Whittow & Findlay (1968) and Hales & Findlay (1968), however, have demonstrated that the cost of panting in cattle is so low that it cannot be measured accurately. Crawford (1962) has shown that dogs pant at the natural resonant frequency of the respiratory system and has suggested that this may account for the high efficiency of panting. It is possible from the data of McLean (1963) to calculate the respiratory frequency which would be required to dissipate all of the heat from the respiratory tract of an ox weighing about 12 kg. These calculations indicate that an ox would have to pant at a frequency of approximately 5 respirations/min if alveolar ventilation were not to be increased. It seems possible that this high respiratory rate exceeds the resonant frequency of the thoracic cavity of the ox and would involve a large expenditure of energy. However, such measurements of the resonant frequency and the degree to which it can be changed by adjusting the elasticity of the thoracic cavity need to be made before this explanation of why large animals sweat can be evaluated. In conclusion it is clear that all of the bovids which have been investigated to date possess functional sweat glands which respond to heat and which are controlled by adrenergic neurones; and that the pattern and magnitude of sweating is correlated better with the size of an animal than
9 SWEATING OF BOVIDS 143 it is with its phylogenetic position. One is left with the interesting problem of why this correlation between rate of sweating and size exists. This work was supported in part by Grant No. 652 from the Rockefeller Foundation to the East African Community (formerly the East African Common Services Organization) and the Faculty of Veterinary Science, University of East Africa, and in part by the National Institutes of Health Grant No. GM 11, The authors are grateful to Dr A. F. Green of Burroughs Wellcome and Co. for supplies of bethanidine. REFERENCES BLIGH, J. (1961). The synchronous discharge of apocrine glands of the Welsh Mountain sheep. Nature, Lond. 189, BLIGH, J. (1967). A thesis concerning the processes of secretion and discharge of sweat. Environ. Re8. 1, BOURA, A. L. A. & GREEN, A. F. (1963). Adrenergic neurone blockade and other acute effects caused by N-benzyl-N'N' dimethylguanidine and its ortho chloro derivative. Br. J. Pharmac. Chemother. 2, CRAWFORD, E. C. (1962). Mechanical aspects of panting in dogs. J. apple. Phy8iol. 17, FINDLAY, J. D. & ROBERTSHAW, D. (1965). The role of the sympatho-adrenal system in the control of sweating in the ox (Bo8 tauru8). J. Phy8iol. 179, HALES, J. R. S. & FINDLAY, J. D. (1968). The oxygen cost of thermally induced and CO2- induced hyperventilation in the ox. Re8p. Phy8iol. 4, McLEAN, J. A. (1963a). The regional distribution of cutaneous moisture vaporization in the Ayrshire calf. J. agric. Sci., Camb. 61, McLEAN, J. A. (1963b). The partition ofinsensible losses of body weight and heat from cattle under various climatic conditions. J. Physiol. 167, McLEAN, J. A. (1963 c). Measurement of cutaneous moisture vaporization from cattle by ventilated capsules. J. Physiol. 167, ROBERTsHAW, D. (1968). The pattern and control of sweating in the sheep and the goat. J. Physiol. 198, ROBERTSHAW, D. & TAYLOR, C. R. (1968). The pattern and control ofsweat discharge in some East African bovidae. J. Physiol. 198, 89-9P. SIMPsON, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mu8. nat. Hi8t. 85, TAYLOR, C. R. & LYMAN, C. P. (1967). A comparative study of the environmental physiology of an East African antelope, the eland, and the Hereford steer. Phy8iol. Zool. 4, WAITES, G. M. H. & VOGLMAYR, J. K. (1963). The functional activity and control of the apocrine sweat glands of the scrotum of the ram. Aust. J. aqric. Re8. 14, WHITTOW, G. C. & FINDLAY, J. D. (1968). Oxygen cost of thermal panting. Am. J. Phyaiol. 214,
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