Blood gas changes during panting East African antelope, the dik-dik M. MASKREY, P. P. HOPPE, AND 0. S. BAMFORD Department of Animal Physiology, University of Nairobi,

MASKREY, M., P. P, E~~PPE,AND 0. S. BAMFORLBZOO~ gas changes during panting in a small East African antelope, the dik-dik. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 44(4): 534-537, 1978. -Five adult male dik-dik (Madoqua kirkii) were exposed in a climatic chamber to an air temperature of 45°C. Measurements were made of rectal temperature (T,,) and respiratory frequency (f) and arterial blood samples taken before and during heat exposure were analyzed for pH, Pco2 and PO,. During exposure, T,, and f increased in all animals, In the first 80 min dik-dik displayed thermal tachypnea and minor changes in blood gases. Continued exposure lead to hyperpnea accompanied by a fall in Pacoz and a rise in pH. Pace, at first fell and then increased toward or above control levels. The dik-dik did not display second phase breathing. This observation confirms that second phase breathing is not essential to the development of respiratory alkalosis. The main conclusion of the study is that the dikdik, unlike another heat-adapted antelope, the wildebeest (Taylor, Robertshaw, and Hofmann. Am. J. Physiol. 217: 907910, 1969), is unable to resist alkalosis during heat stress. arterial oxygen pH,; respiratory ventilation

pressure; arterial carbon dioxide pressure; alkalosis; thermal hyperpnea; dead space

IS A STRATEGY employed by many mammals to maximize the loss of heat by evaporation from the upper respiratory tract. During prolonged and severe heat stress, panting may influence respiratory gas exchange, leading to the development, of respiratory alkalosis. This is usually associated with the presence of so-called second phase breathing (3). Heat-induced respiratory alkalosis has been reported to occur in a number of domestic species including the ox (2, 4, lo), the sheep (ll), the goat (12), and the dog (9, 13). However, few studies have been made on nondomesticated species that live in hot climates. Taylor, Robertshaw, and Hofmann (20) compared panting in zebu cattle and wildebeest. They reported that, under conditions in which cutaneous evaporative heat loss was prevented, the wildebeest was resistant to the development of alkalosis at ambient temperatures where cattle become severely alkalotic. Dawson and Rose (6) reported only a moderate alkalosis in the tammar wallaby when severely heat stressed. The present study set out to determine whether, as a general rule, animals living in hot climates show a tendency not to become severely alkalotic when exposed to heat. Experiments were performed on the dik-dik, PANTING

534

in a small

Nairobi,

Kenya

Mudoqua kirk& which is a small antelope inhabiting much of east and southern Africa. The dik-dik has been shown to be well adapted to a hot arid environment (14) and employs panting as its only controlled means of losing heat by evaporation (16). METHODS

The study involved five adult male dik-diks weighing between 3.4 and 4.6 kg (mean 3.95 kg). Between experiments, they were housed singly in metabolism cages and fed on alfalfa hay supplemented with green leaves -from plants frequently browsed by dik-diks in the wild. Food and water were continually available. The ambient temperature at which they were kept was not controlled and varied between 14 and 23°C. Animals were tested singly within a climatic chamber preset to an ambient temperature (T,) of 45*C and a relative humidity of 23%. Prior to testing, a polyethylene cannula was surgically implanted into a femoral artery and fitted with a three-way tap to allow anaerobic withdrawal of arterial blood during the experiment. Venous blood samples were obtained from a jugular vein. The dik-diks were trained to become accustomed to a harness and were suspended in this during heat exposure, Rectal temperature (T,,) was measured using a polyethylene sheathed copper/constantan thermocouple inserted approximately 10 cm into the rectum and recorded, together with wet and dry bulb temperatures, on a Honeywell Electronic 16 recorder. Respiratory frequency (f) was measured using a stethograph belt secured around the thorax and the pressure changes transferred via a tambour and writing level to a kymograph*

Heat exposure was continued either until T,, reached 42°C or the animals became restless. Exposure consequently lasted for between 90 and 140 min during which time from three to five Z-ml arterial blood samples were taken. Control values were obtained from blood samples taken while the animals remained quietly in their cages prior to heat exposure. Venous blood samples were obtained from a jugular vein while the animals were resting and again at the termination of heat exposure. All blood samples were analyzed for Paz, Pcoz, and pH using an Instrumentation Laboratories meter (pH and blood gas analyzer) model 113-S. The pH, Pcoz, and PO* values were corrected for body temperature (5 3 18) Experiments and measurements were conducted m l

002L8987/78/0000-0000$01.25

Copyright

0 1978 the American

Physiological

Society

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Nairobi which has an elevation of 1,660 m. The average barometric pressure was approximately 625 Torr.

TABLE 1. Responses of dik-dik exposed to 45°C Minutes Parameter

O-20

Rectal temperature increased throughout the period of heat exposure, the rate of rise being greatest during the early part of exposure. With regard to the respiratory responses, the exposure period could be conveniently divided into three parts. Up to 50 min heat exposure, f increased rapidly. Between 50 and 80 min f reached a maximum of between 400 and 500 breaths/ min. At this stage the dik-diks shifted from closedmouth to open-mouth panting. Eighty minutes after the exposure had begun there was little or no further increase in f. However, it was clear from the stethograph record and from visual observation that the depth of breathing was increasing at this time. The changes of T,, and f with time are shown in Fig. 1. Table 1 shows the changes in blood gases and pH of arterial blood in relation to changes in T,, and f during heat exposure. It also shows values for venous blood before and immediately after exposure. A small change in pH, and Pace, occurs during the first 80 min of exposure. As heating continues there is a fall in Pace, and a corresponding rise in pff a, Paoz falls during the early part of the trial then increases to be near or a little above the control value. The venous values suggest similar trends and are included here mainly for comparison. Figure 2 shows the results from heat exposure on one dik-dik in which the measurements obtained are graphed against exposure time.

38.8 (38.6-39.2) 32 (18-48) 7.44 (7.41-7.47) 7.38 (7.34-7.41) 32.3 (29-34) 39.7 (37-42) 78 (71-84.5) 46 (40-U)

‘be, “C f, breaths/ min PK P% Pa,,,

Torr

Pvco,,

Torr

Pa,, , Torr Pvo2, Torr Values

of Exposure

Control 20-50

50-80

39.2 (38.8-40.0) 93 (35-155) 7.51 (7.48-7.53)

40.2 (39.6-41.1) 284 (170-450) 7.52 (7.50-7.55)

40.95 (40.4-41.6) 436 (380-510) 7.56 (7.53-7.58)

30.3 (27.5-34.5)

29.2 (26-32)

27.6 (25.5-31.5)

RESULTS

are means with

0

20

79 (73-83.5)

the ranges

40

below

60

71.5 (63-78 j

>80 41.4 (40.8-42.0) 471 (415-540) 7.65 (7.56-7.77) 7.52 (7.44-7.58) 20.8 (13-26) 30.6 (25.5-34.5) 81.5 (68.5-95.5) 49.5 (44-62)

66.5 (55-73)

them in parentheses.

80

100

120

uo

Time (mind FIG. 2. Changes in rectal temperature, and blood gases of a single dik-dik exposed

respiratory to T, 45°C.

frequency,

DISCUSSION

39 0

20

40

60

80

100

I20

110

Time (mins)’ FIG, 1. Changes in rectal temperature and respiratory in dik-dik exposed to T, 45°C. Each symbol represents vertical lines indicate standard deviations. Number symbol indicates n.

frequency the mean; below each

The present study shows that the dik-dik does become alkalotic during heat stress, this alkalosis resulting from hyperpnea during the latter part of heat exposure. Initial thermal tachypnea which involves an increase in dead space ventilation gives way with continued heating to an increased tidal volume and thus increased alveolar ventilation. Unfortunately tidal volume could not be measured in the present study and therefore these changes can only be inferred, However, the occur-

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536

MASKREY,

rence of thermal hyperpnea at increased body temperature would be consistent with findings in other species (17) Taylor et al. (20) have suggested that the wildebeest does not normally become alkalotic during heat exposure because it is able to increase tidal volume without increasing alveolar ventilation. The wildebeest increases its dead space during panting by ventilating its large paranasal sinuses. The fact that the dik-dik more readily becomes alkalotic suggests that it does not have a similar strategy open to it. This is surprising in view of the fact that the dik-dik does possess an elongated snout comprising infiatable tissue which could conceivably be used to increase dead space during panting. Although T,, is employed here as a representative core temperature, its value per se may be of little importance with regard to the thermoregulatory responses of the animal. It has been demonstrated that there is a very poor correlation between T,, and respiratory activity (8). Indeed, as the present study, like all previous studies, is investigating a transient rather than a steady-state phenomenon, the absence of such a correlation is not unusual. It must also be borne in mind that many species are able to maintain a brain temperature considerably lower than that of the general body core by possessing a carotid rete which allows heat exchange to take place between carotid blood and the venous drainage from the nasal region This is the case in the Thomson’s gazelle (19) and is probably also true in the dik-dik. Without a measurement of brain temperature it is diffxcult to obtain a true estimate of thermal stress There would appear to be major species differences in the degree to which blood gases are disrupted during panting. Thus, whereas the cat, due to effective plasma buffering, is relatively resistant to the development of alkalosis (E), the goat shows increased alveolar ventilation following even small increases in T, (12). The dog (9), ox (lo), sheep (ll), and dik-dik (this report) appear to lie between these two extremes. It would seem then that the cat and the wildebeest are more resistant to the development of respiratory alkalosis. But could it not also be suggested that the goat for instance was more tolerant to the development of alkalosis? This is a difficult question to answer from our present knowledge and it will require carefully designed experiments in order to answer it. In some species, if the heat exposure is severe and l

HOPPE,

AND

BAMFURD

prolonged, rapid shallow -panting is superceded by slower, deeper respiratory movements which have been termed second phase breathing (3). This has been shown to occur in the ox (l), the sheep (ll), and the dog (9). In the ox (IO) and the sheep (II) it is only during second phase breathing that respiratory alkalosis develops. The dog differs in that alkalosis may set in during shallow panting (9). In the dik-dik, we were never able to identify second phase breathing. Once f had risen to a maximum of 400-500 breaths/min this maximum was maintained for as long as the animal was able to withstand the conditions. It may be that second phase breathing is confined to larger animals as it has not so far been reliably demonstrated in smaller species (17). Nevertheless, the present study shows conclusively that second phase breathing is not an essential prerequisite to the development of respiratory alkalosis. One surprising aspect of the present study is the biphasic change in Pao,. Previous reports have indicated a rise in oxygen content of the blood during continued exposure to heat. This has been accredited to a rise in cardiac output coupled with an increased peripheral blood flow (7, 13). To clarify this point it would be necessary to make measurements of cardiovascular parameters in the dik-dik during heat stress. In conclusion, it can be stated that resistance to the development of alkalosis is not necessarily a general feature among animals adapted to hot climates. On the other hand, the dik-dik, which is small enough to find shelter during the hottest part of the day, may not require the protection from increased alveolar ventilation which a plains dweller such as the wildebeest might need. It is important for a proper understanding of these differences that the blood gas changes during heat exposure be measured for a range of nondomesticated species in the same way that thermoregulatory changes have been monitored. In this way it may be possible to determine whether specific adaptations occur which either enable the animal to resist the development of alkalosis or enable it to tolerate alkalosis should it be forced upon it, The authors are grateful to the staff of the Intensive Care Unit, Kenyatta Hospital, Nairobi for analyses of the blood samples. Present address M. Maskrey: Dept. of Physiology, University of Tasmania, Hobart, Tasmania 7001, Australia. Recedved

for publication

26 September

1977.

REFERENCES W. R., AND 9. D. FINDLAY. The effect of environmental temperature and humidity on the respiration of Ayrshire calves. J. Agr. Sci. 45: 452-460, 1955. 2. BIANCA, W. The effect of thermal stress on the acid-base balance of the Ayrshire calf. J. Agr. Sci. 45: 428-430, 1955. 3. BIANCA, W. The relation between respiratory rate and heart rate in the calf subjected to severe heat stress. L Agr. Sci. 51: 321-324, 1958. 4. BIANCA, W., AND J. D. FINDLAY. The effect of thermally-induced hyperpnoea on the acid-base status of the blood of calves. Res. Vet. Sci. 3: 38-49, 1962. 5. BRADLEY, A. F., M. STUPFEL, AND J. W. SEVERINGHAUS. Effect of temperature of Pco2 and Paz of blood in vitro. J. Appl. Physiol. 1. BEAKLEY,

9:201-204,1956.

6.

DAWSON, T. J., AND R. W. ROSE. Influence of the respiratory response to moderate and severe heat on the blood gas values of a macropodid marsupial (Macropus eugenii). Comp. B&hem. Physiol. 37A: 59-66, 1970. 7. FINDLAY, J. D., AND G. C. WHITTOW. The role of arterial oxygen tension in the respiratory response to localized heating of the hypothalamus and to hyperthermia. J. Physiol., London 186: 333-346, 1966. 8. HALES, J. R. S. Changes in respiratory activity and body temperature of the severely heat-stressed ox and sheep. Comp. Biochem. PhysioZ. 31: 975-985, 1969. 9. HALES, J. R. S., AND J. BLIGH. Respiratory responses of the conscious dog to severe heat stress. Experientia 25: 818-819, 1969,

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GASES

IN

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PANTING

DIK-DIK

10. HALES, J. R. S., AND J. D. FINDLAY. Respiration of the ox: normal values and the effects of exposure to hot environments. Respiration. PhysioZ. 4: 333-352, 1968. 11. HALES, J. R. S., AND M. E. D. WEBSTER. Respiratory function during thermal tachypnoea in sheep. J. Physiol., London 190: 241-260, 1967. 12. HEISEY, S. R., T. ADAMS, W. HOFMANN, AND G. RIEGLE. Thermally induced respiratory responses of the unanaesthetised goat. Respiration Physiol. 11: 145-151, 1971. 13. HIGGINS, E. A., AND P. F. IAMPIETRO. Thermal panting and the initiation of respiratory alkalosis. Can. J. Physiol. PharmacoZ. 45: 1-12, 1967. 14. HOPPE, P. P. How to survive heat and aridity: ecophysiology of the dikdik antelope. Vet. Med. Rev., Buyer 1: 77-86, 1977. 15. MORGAN, M. L., AND T. ADAMS. Respiratory acid-base balance in the unanaesthetised cat during acute heat stress (Abstract).

537 PhysioZogist 15: 221, 1.972. 16. MUSEWE, V. O., G. M. 0. MALOIY, AND J. K. KANJA. Evaporative water loss in two small African antelopes: the Dikdik and the Suni. Comp. Biochem. Physiol. 53~: 17-18, 1976. 17. NICOL, S. C., AND M. MASKREY. Panting in small mammals: a comparison of two marsupials and the laboratory rabbit. J. AppZ. Physiol. : Respirat . Environ. Exercise Physiol. 42 : 537-544, 1977. 18. ROSENTHAL, T. B. The effect of temperature on the pH of blood and plasma in uitro. J. Biol. Chem. 173: 25-30, 1948. 19. TAYLOR, C. R., AND C. P. LYMAN. Heat storage in running antelopes: independence of brain and body temperatures. Am. J. Physiol. 222: 114-117, 1972. 20. TAYLOR, C. R., D. ROBERTSHAW, AND R. HOFMANN. Thermal panting: a comparison of wildebeest and zebu cattle. Am. J. Physiol. 217: 907-910, 1969.

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Blood gas changes during panting in a small East African antelope, the dik-dik.

Blood gas changes during panting East African antelope, the dik-dik M. MASKREY, P. P. HOPPE, AND 0. S. BAMFORD Department of Animal Physiology, Univer...
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