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Blood Gas Tensions and Acid-Base Regulation in the Salt-Water Crocodile, Crocodylus Porosus, at Rest and After Exhaustive Exercise

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Blood Gas Tensions and Acid-Base Regulation in the Salt-Water Crocodile, Crocodylus Porosus, at Rest and After Exhaustive Exercise exp. Bwl. 118, 143-159 (1965) minted in Great Britain 0 The Company of Biologists Limited' 1985 BLOOD GAS TENSIONS AND ACID-BASE REGULATION IN THE SALT-WATER CROCODILE, CROCODYLUS POROSUS, AT REST AND AFTER EXHAUSTIVE EXERCISE BY R. S. SEYMOUR, A. F. BENNETT* AND D. F. BRADFORD Department of Zoology, University of Adelaide, Adelaide, S.A. 5001, Australia Accepted 27 February 1985 SUMMARY 1. Salt-water crocodiles, Crocodylus porosus Schneider, were catheter- ized and Po,, Pco,, pH and lactate concentration ([lactate]) were measured in arterial blood during rest and after forced exhaustive activity at 30°C. 2. Gas exchange ratio (R), calculated from blood Po, and Pco,, decreased from about 1.0 to 0.3 during resting voluntary breath-holding and indicated CO2 sequestration in the body fluids. The mean value for R in undisturbed animals was 0.6, which substantiates the hypothesis that some COa excretion is extrapulmonary. 3. In vitro buffer value of true plasma was -23.5+1-9mmol HC03- 1-'pH-'. In vivo buffer value, determined by short-term self titration with metabolic CO2, was - 12.2 k4.7 mmol HC03- I-' pH-'. 4. Exhaustive activity for 5min in laboratory animals resulted in pronounced metabolic lactacidosis: pH decreased approximately from 7-43 to 7-11 while lactate concentration increased from 1.2 to 20-30 mmoll-'. The acidosis was reduced by respiratory compensation during the first hour of recovery and by metabolic adjustments that were practically complete after the third hour. Greater acidosis (pH down to 6.4) in larger field-captured animals was resolved over a longer period. 5. During recovery, lactate and proton fluxes between the blood and other tissue were uncoupled. 6. The virtual absence of the fixed-acid Bohr effect in C. porosus blood is adaptive in large individuals because it facilitates continued 02uptake from the lung into blood which may be acidified by as much as 1 pH unit as a result of physical activity. INTRODUCTION Much crocodilian behaviour is slow and peaceful. Like other aquatic reptiles, resting crocodilians usually have ventilatory periods separated by longer periods "Present address: School of Biological Sciences, University of California, Irvine, California 9271 7, U.S.A. Key words: Blood gases, acid-base regulation, exercise, reptile. 144 R. S. SEYMOUR,A. F. BENNETTAND D. F. BRADFO of apnoea (Naifeh et al. 1970). Gas exchange in diving reptiles has been termed 'cyclic' because the patterns of COz excretion and 02 uptake are temporally distinct (Ackerman & White, 1979; Burggren & Shelton, 1979). Whereas 02is recruited from the lung more or less constantly, most of the CO2 accumulates in the bicarbonate buffer system of the body fluids during apnoea and is released during the ventilatory period. This phenomenon has been demonstrated in the alligator, Alligator mississippiensis (Andersen, 1961) and in the Nile crocodile, Crocodylus niloticus (Glass & Johansen, 1979), and we have studied it in the salt- water crocodile, Crocodylus porosus. The languid existence of crocodiles, however, can be punctuated by fierce activity during predation, defence and escape. Crocodiles often feed' on large terrestrial animals that they pull into the water and drown (Guggisberg, 1972). Thus, they must be capable of powerful physical activity and they must also be adequate divers. Both intense activity and diving behaviour promote a reliance on anaerobic metabolism. The magnitude of anaerobiosis in reptiles may exceed that of any other animal group and the build-up of lactate and protons in muscle and blood can lead to severe acid-base disturbance (Bennett, 1978, 1982). The dynamics of metabolite appearance and disappearance in blood following exercise has been studied in various animal groups, but the reptiles deserve more attention because of their extreme anaerobic capacity. Crocodilians, in particular, are of interest because of the severity of the acidosis produced by relatively short bouts of intense exercise (Coulson & Hernandez, 1979; Bennett, Seymour, Bradford & Webb, 1985). We examined acid-base regulation in C. porosus during voluntarv diving and following provoked activity in the laboratory and field. MATERIAL AND METHODS Animals Seven Crocodylus porosus (mean mass = 2.74 kg; range = 0.43-7.0 kg) were cap- tured in the Adelaide River region, near Darwin, in the Northern Territory during November 1983. They were collected by standard methods (Webb & Messel, 1977) under permit No. SL41/83 issued by the Conservation Commis- sion of the Northern Territory. Captive crocodiles were held in large concrete bins (Webb, Buckworth & Manolis, 1983) at approximately 30°C for a few days until they were used. They were not fed but were released in good condition within a week. Blood sampling The right exterior carotid artery was occlusively catheterized in six animals under cold anaesthesia (McDonald, 1976). Animals were placed in an ice-water bath with only their heads held out of water. The latter precaution was taken as previous observations on tropical snakes indicated that death could result from head submersion in cold water. Animals were submersed until rectal temperature fell to approximately 5 "C, when they became completely unresponsive to external %&; fR:QBCs? Exercise in crocodiles 143 stimuli. They were then transferred to a bed of ice which was manipulated to keep body temperature constant. Catheters, fashioned from polyvinyl chloride tubing (0.58 x 0.96 mm or 1.0 x 2.0 mm and 1.0-1.5 m long) and filled with heparinized saline (250 i.u. ml-', were implanted via a small ventral incision and exteriorized the dorsal side of the neck. After surgery, the crocodiles were artificially rentilated during post-operative warming until spontaneous ventilation was ~med.They recovered for at least 18 h in isolation before measurements were :aken. Crocodiles are notoriously sensitive to disturbance, which may alter their heart rate and ventilatory pattern (Gaunt & Gans, 1969; Gans & Clark, 1976). To neasure completely resting animals, we placed each individual in shallow water ).Of l.O°C) in containers of sufficient size to permit them to submerge and move around. The only restraint was a cord securing the jaws together; this cord -. .d not impede normal ventilation. So that the animals were not disturbed by the investigators, the containers were covered and the measurements were carried out quietly. Ventilation rate was observed in isolated animals, by impedance plethys- mography (Parks Model 270 Plethysmograph). Experimental protocol All measurements were made from 10.00 to 18.00 h local time. A series of blood samples was withdrawn from catheterized crocodiles under three experimental conditions. First, samples were obtained from isolated animals during normal ventilatory cycles, including voluntary apnoea. Second, the top of the container was removed and the animal was allowed to view a person. The crocodiles responded by changing their ventilatory pattern, often undergoing longer periods of voluntary apnoea. We refer to this treatment as 'intimidation'. Finally, they were gently held under water until they began to struggle and then were permitted to surface. The next day, each catheterized crocodile was exercised and permitted to recover from the bout of activity. Blood samples were first taken from a resting animal prior to activity. Then it was placed in a bathtub half full of water and prodded by hand on the tail and limbs for 5 min. The crocodile responded with intense bouts of struggling and rolling for the first 1-2min, but the level of activity diminished thereafter. It was then returned to its covered container to rest undisturbed during the recovery period. Blood samples were taken as soon as possible after the cessation of activity (approx. 2-3 min) and at 10, 20, 30 min and 1, 2, 3 h of recovery. Additional blood samples were obtained by heart puncture from crocodiles exercised to exhaustion in the field (Bennett et al. 1985). Sample analysis Blood from catheterized crocodiles was obtained according to the methods described by Seymour & Webster (1975), in which gas tensions are measured in samples subsequently returned to the animal to avoid depletion of blood volume. Blood was aspirated into a Radiometer model BMS 3 Mk 2 blood microsystem connected to a model PHM72 acid-base analyser, maintained at 30-Of 1-O°C. Several times the volume of the catheter tubing and electrode cell were flushed through the system before gas tension was read at prevailing blood pressure. The Poz electrode was calibrated with Radiometer Po, zero solution and water equilibrated with air, accounting for water vapour pressure. After determining the difference in electrode readings of air and water with the same Po,, the electrode was routinely calibrated with gas from a Radiometer GMA 2 gas mixing apparatus. Reported Pco, has been increased 7 % to account for the approximate difference between the electrode's responses to blood and water (Heitmann, Buckles & Laver, 1967). The PCO,electrode was calibrated with the GMA 2 and the pH electrode with precision buffers. The barometric pressure varied less than f2 Torr during the experiments and was assumed to be ccinstant at 758 Torr. In vitro blood buffer values were measured by equilibrating approximately 0.4ml samples of whole blood to each of the humidified gases supplied by the GMA 2 (Pco, = 27.3 and 54.8 Torr). Samples were rotated in a tonometer consist- ing of two, 2-ml glass vials thermostatted to pH electrode temperature. Equilibra- tion occurred within 10min and after that time the samples were aspirated into the pH electrode. Plasma [HC03-] was calculated with the Henderson-Hassel- balch equation. To deal with blood pH values as low as 6.4, the pK' was calculated from a second order polynomial equation fitted to data at 30°C from Severinghaus (1 965); the equation (pK' = 5.2493 + 0.2953 pH -0.0238 pH2) accounts for pH dependence and yields a value within 0.004 units of that calculated at pH = 7.4 by Reeves (1 976).
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