RESPIRATORY FUNCTION OF THE SWIM-BLADDERS OF THE PRIMITIVE FISH POLYPTERUS SENEGALUS

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1 J. Exp. Biol. (1970), 5a, With 4 text-figures Printed in Great Britain ESPIATOY FUNCTION OF THE SWIM-BADDES OF THE PIMITIVE FISH POYPTEUS SENEGAUS BY A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED Department of Zoology, Faculty of Science, and Department of Physiology, Faculty of Medicine, University of Khartoum, Sudan (eceived 16 April 1969) INTODUCTION Anatomical, physiological, and ecological studies of fishes which have survived since Devonian times not only contribute to the better understanding of primitive vertebrate patterns but also extend our knowledge of the evolution of existing vertebrate mechanisms. In particular, they provide a valuable basis for speculation about the adaptations of these fishes in relation to the conditions prevailing in earlier times. One of the outstanding differences between these primitive fishes and modern forms which can be studied in the living representatives lies in their mode of respiration. It has already been shown that Polypterus senegalus surfaces to inhale air whenever the aquatic oxygen content is low, or during periods of activity, and it has been concluded that the inhaled air is passed to the swim-bladders (Abdel Magid, 1966). It has further been shown that the swim-bladders are richly vascularized and lined with respiratory epithelium. The unique circulation of Polypterus, together with other anatomical findings and ecological observations, lead to the conclusion that the blood flowing through the pulmonary vessels must become loaded with oxygen from the swim-bladders unless it has already been saturated when passing through the gills (Abdel Magid, 1967). The present investigation was carried out to find out for certain whether the swimbladders of Polypterus actually do contribute to respiration as suggested above. MATEIA AND METHODS The fish used throughout this investigation were obtained from the White Nile in the vicinity of Khartoum or else from Jebel Awlia area some 30 miles to the south. Sixteen specimens of Polypterus senegalus (weighing g.) were investigated in 23 expts. Gas samples from both left and right swim-bladders were obtained from unrestricted fishes through hypodermic needles (sizes 14-20) introduced through the body-wall into the bladders andfixedwith rubber bands round the body. These needles were connected to plastic tubes approximately 40 cm. in length and 0-3 mm. inner diameter. Ten cm. of this tubing had a volume of only ml. Two techniques were used for gas sampling and gas analysis: (a) to establish the pattern of the changes of gas composition in the swim-bladders, 1 ml. samples were drawn into the syringes before and after inspiration of air. Before taking an actual sample the dead space of the tubes and syringes (approximately 0-2 ml.) was flushed

2 28 A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED by repeatedly drawing and pushing back i ml. of the gas in the bladder. The gas samples were then analysed for their oxygen and carbon dioxide contents with a Scholander microanalyzer (Scholander, 1947). By this technique it was possible only to analyse a limited number of samples, as each sample diminished substantially the volume of gas in the swim-bladder; (b) to investigate the dynamics of the changes if B _dtx Fig. i. Diagram to illustrate method of semicontinuous measurement of oxygen tension. A = 3 ml. syringe; B, C, D = Perspex connectors; E = P Ol electrode; F, G, = hypodermic needles for cannulation; H = inlet for calibration and measurement of oxygen tension of water; t = clamps. in the gas composition within the bladders a semicontinuous technique for determination of the oxygen tension, previously developed by one of us (Vokac & Macholda, 1966), was adapted to this purpose (Fig. 1). Oxygen tension was measured with a thermostated adiometer P Ot electrode Type E 5044 connected through a Gas Monitor PHA 927 to a ph-meter 27. Calibration. The measuring equipment was calibrated by pushing first an oxygenfree solution and then atmospheric air of known oxygen tension by way of the horizontal

3 Function of swim-bladders of primitive fish 29 hole in the central four-way Perspex connector through the electrode up to the syringe. During this procedure the vertical outlets of the central connector were clamped. Sampling. The horizontal outlets of the central connector were clamped and the vertical passage was left open. After repeated flushing of the sampling dead space, a 1 ml. sample was drawn into the syringe from one of the swim-bladders bypassing the electrode. During this time the tube leading to the other bladder remained clamped. The exact time at which each sample was withdrawn was recorded. Measurement. The horizontal tube leading from the four-way connector to the electrode was undamped, and the vertical tube leading to the syringe was clamped. The sample was then pushed through the electrode (total dead space 0-17 ml.) back into the swim-bladder and the oxygen tension of the sample recorded. If the difference between two successive samples was not greater than mm. Hg, the response time of the measuring instrument was below 1 min. The sampling and measurement could then be repeated either from the same bladder or else from the other one. This method had the advantage of allowing semicontinuous gas analysis at intervals of 1-2 min. At the same time, because the sample was returned via the oxygen electrode back to the swim-bladder, the analysis did not diminish the volume of air in the swim-bladder and could be repeated as many times as necessary. Accuracy of measurement. Zero drift never exceeded + 1 mm. Hg even after 4-5 hr. The equipment could easily be re-standardized during the experiment via the horizontal hole in the central connector. The same route was also used to measure the oxygen tension of the surrounding water during the experiment. By miniaturizing all the connectors and tubes, including those leading to the fish, dead space was kept as low as 0-27 ml. epeated mixing before taking samples only flushed back o-i ml. of the previous sample, an amount which is almost negligible. The other 0-17 ml. of the previous sample which remained temporarily in the electrode circuit was flushed out by the subsequent sample. Only the last non-contaminated portion of the sample was used for the next measurement. In this way the accuracy of analysis was not appreciably affected even when there were comparatively large differences between the oxygen tensions of successive samples. ESUTS Basic pattern of gas changes The basic pattern of changes occurring in the gas composition of the swim-bladders of Polypterus in relation to the inhalation of atmospheric air was investigated. The results were fairly uniform and a typical pattern can be seen in the data of an experiment represented graphically in Fig. 2. Both swim-bladders of a fish weighing 184 g. were cannulated. Gas samples were obtained from the left bladder by means of a hypodermic needle inserted at a position immediately posterior to the communication of the left bladder with the right one. Samples from the right bladder were obtained by inserting a hypodermic needle on the right side of the fish immediately anterior to the vent. Soon after cannulation the fish was transferred to a plastic container filled with about of tap water. The initial oxygen tension of the water was 140 mm. Hg, the temperature 26 C, and the oxygen content 7^3 mg./l.

4 30 A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED Gas samples from both swim-bladders were drawn simultaneously into a pair of syringes before the fish visited the surface. Imminent surfacing was often indicated by deep ventilatory movements accompanied by sudden beating of the pectoral fins. Shortly after the fish had surfaced, another pair of samples was withdrawn. The same procedure was repeated before and after the second inhalation of air, and again before the third surfacing. The samples were then analysed M E E Minutes Fig. 2. Changes in the tension of oxygen and carbon dioxide in the left bladder (O O) and in the posterior end of the right bladder ( ) of Polypterus senegalus. Arrows indicate surfacing and the inhalation of atmospheric air. Figure z shows a sharp increase in oxygen tension immediately after inhalation. This was markedly higher in gas from the left bladder than from the right one. It was followed by a decrease which continued until the next inhalation. Changes in carbon dioxide tension during the period were much less pronounced. Sixty-four samples were obtained in a similar way in 12 expts. with 10fishes. The results are summarized in Table 1 which shows their averages and variation. The mean changes in oxygen and carbon dioxide tension correspond closely with those found in the experiment described above (Fig. 2). On account of technical difficulties connected with cannulation of the swim-bladders it was not always possible to draw samples simultaneously from both bladders. Nor was it always possible to draw samples from the same bladder before and immediately after inhalation of air. The averages in Table 1 are, therefore, not strictly comparable and the table represents the variation of all our findings. In four of the experiments with four different fishes we were able, however, to draw simultaneous pairs of interrelated samples before and immediately after the

5 Function of swim-bladders of primitive fish 31 inhalation of air. The results of these are given in full in Table 2. They emphasize not only the uniformity of the general pattern but also quantitative differences between the right and left swim-bladder under strictly comparable conditions. Statistical evaluation confirmed the fact that the oxygen tension increased significantly and Table 1. Averages of oxygen and carbon dioxide tension and their variation in 64 samples from both swim-bladders eft bladder ight bladder P Oj (mm. Hg) P COi (mm. Hg) N Mean 3.D. Minimal Maximal Mean S.D. Minimal Maximal Before inhalation IO-I 22-8 After inhalation I2-I Before inhalation " '4 n After inhalation Table 2. Oxygen and carbon dioxide tensions in samples drawn simultaneously from both the left () and right () swim-bladders before and after inhalation (The time intervals between sampling and inhalation, and between inhalation and sampling, are given). Weight (g.) Mean S.D. Side Time interval (sec.) DO 60 IO 9O , Before inhalation Po, (mm. Hg) io-i 17-1 Poo, (mm. Hg) IO-I 2O n-8 n I2'O l6' H Time interval (sec.) fin uu '5 45 IO 367 _, 2I'o Q After inhalation Po, (mm. Hg) ioo ' 15-5 io-6 Pco, (mm. Hg) ' " ' carbon dioxide tension decreased significantly after inhalation in both bladders (P < o*o 1). On the other hand, when the respective tensions in the left and right bladders were compared only the difference in oxygen tensions after inhalation of air was significant (P = o-oi).

6 32 A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED Dynamics of oxygen uptake Further information was obtained about oxygen uptake from the swim-bladders by semicontinuous determination of oxygen tension. An experiment, the results of which are plotted in Fig. 3, may serve as a typical example. The same fish which had been used in the first experiment was again cannulated 6 weeks later in the same places. Soon afterwards it was transferred to tap water with an initial oxygen tension of 140 mm. Hg, a temperature of 3O C. and an oxygen content of 6-9 mg./l. 1S Minutes Fig. 3. Semicontinuous measurement of oxygen tension in the left swim-bladder (O) and in the posterior end of the right bladder (#) of Polypterus senegalus. Arrows indicate surfacing and inhalation of atmospheric air. The pattern of the changes of oxygen tension in the respective bladders was always the same. A large instantaneous increase of oxygen tension occurred in the left bladder after each inhalation. The peak tension was always markedly lower in the posterior region of the right bladder and was reached only after a considerable time lag. In both bladders this was followed by a steady decrease of oxygen tension until the next inhalation, when the pattern was again repeated. epeated findings of differences between the oxygen tension at the posterior end of the right bladder and in the left bladder after inhalation were tentatively attributed to incomplete mixing of the inspired air. This presumption was verified by the following experiment (Fig. 4). The right bladder of a fish weighing 240 g. was cannulated at the posterior as well as at the anterior end opposite to the junction with the left swim-bladder. This fish was then transferred to tap water with an initial oxygen tension of 140 mm. Hg. The temperature of the water was 21 C. and its oxygen content

7 Function of swim-bladders of primitive fish o mg./l. The results were nearly identical with those of the previous experiment (Fig. 3). An instantaneous increase of oxygen tension in the anterior region of the bladder after inhalation was regularly accompanied by a much slower rise at the posterior end. There was a marked difference in peak concentrations (Fig. 4). This difference can be regarded as reliable evidence of incomplete mixing of the inhaled and residual air in the right swim-bladder E E Minutes Fig. 4. Semicontinuous measurement of oxygen tension in the anterior (O) and posterior ( ) ends of the right swim-bladder of Polypterus senegalus. Arrows indicate surfacing and the inhalation of atmospheric air. Of specific interest in this experiment were the rates of oxygen uptake by blood. The fall in the concentration of oxygen was much quicker in the anterior than in the posterior part of the right bladder. Only when the interval between two inhalations was very long did the two curves eventually meet. The mixing of the contents of the bladder by diffusion, possibly enhanced by peristalsis, may have played a role in diminishing the initial difference in concentration up to the point where the curves crossed. From then on the differences in the rate of oxygen uptake were most probably due only to differences in the flow of blood in the anterior and posterior ends of the bladder. The presence of a higher density of capillaries in the anterior end as compared with the posterior end points to such a possibility. Further conclusions pertaining to the incomplete mixing of inspired gas in the right swim-bladder can be reached by quantitative evaluation of the data in Table 2. The inhaled atmospheric air dilutes the residual gas mixture in the bladders. The resulting changes of the composition of the bladder contents represent, therefore, the ratio of the residual volume to the inhaled volume. Even if we do not know the actual 3 E X B 52

8 34 A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED residual volume, the relative volume of inhaled air expressed as a percentage of the unknown residual volume can be calculated from the degree of dilution. A modification of the formula used for the estimation of the volume of different body cavities by gas dilution technique can be applied to this purpose (Vokac & Macholda, 1966). (a) elative volume of inhaled air as a percentage of the residual volume as calculated from changes of oxygen tension (V Ot ): (P y -P x ) 100 F (I) ' " P.-P* where P x = P o, before inhalation; P y = P Ol after inhalation; P z = P Oj of inhaled air (on the average, 147 mm. Hg). (b) elative volume of inhaled air as a percentage of the residual volume, as calculated from changes in the carbon dioxide tension (Poo,) : _ (P x -P u ) 100, v K oo, p _p» v z / where P x = P OOl before inhalation; P v = P COi after inhalation; P z = P COi of inhaled air (0-2 mm. Hg). Table 3 represents the average relative volumes of inhaled air expressed as a percentage of the respective residual volumes. These were calculated from the data in Table 2 from both oxygen and carbon dioxide tension changes, and separately for Table 3. elative volumes of inhaled air (V Ot, Pco,) expressed as percentage of the residual volume in the left () and right () bladders V Ot N Mean S.D P < o-oi 6 S P = O'l the right and left bladders. When calculated from the increase of oxygen tension, the relative volume of atmospheric air diluting the residual volume of the left bladder (Po ) was found to be significantly larger (P < o-oi) than that on the right side (Po, )- On the average a volume unit of the left bladder was diluted by inhaled air about three times more effectively (162% 153 %) than a volume unit of the air in the posterior end of the right bladder. This finding can be regarded as further evidence of uneven distribution of inhaled air in the right bladder. Similar differences between the relative volumes of the air inhaled can be seen when these volumes are calculated from change in the oxygen and carbon dioxide tensions of the gases within the same bladder, for example if V o% is compared with Po^, and Po, with ^00, (Table 3). The volumes calculated from the figures of oxygen tension are markedly larger than those calculated from figures of carbon dioxide tension: 162 against 67% in the left bladder and 53 against 37% in the right bladder. The differences are statistically significant (P 0-05).

9 Function of swim-bladders of primitive fish 35 To explain this discrepancy we have to assume that, in one and the same bladder, the initial degree of dilution of residual oxygen and carbon dioxide by the inhaled air must have been the same. But the withdrawal of the samples after the inhalation was delayed by sec. (Table 2). However, because of the high rate of diffusion of carbon dioxide (Bartels et al. 1963), its tension rose sharply even during this short period. The differences in carbon dioxide tension assessed before and after the inhalation of air, are therefore misleadingly low. Consequently the value calculated for the proportion of air inhaled is also low. DISCUSSION It has long been assumed that the swim-bladders of Polypterus take part in gaseous exchange (Brown, 1957). Until now, in spite of ecological and anatomical observations supporting this assumption, no experimental work has yet been carried out to substantiate the hypothesis. The present investigation, however, provides data which demonstrate conclusively the role of the swim-bladders as accessory respiratory organs and their function as lungs. A sharp increase of oxygen tension in both bladders immediately after surfacing proves that atmospheric air is actually inspired (Fig. 2). The rate at which the oxygen subsequently disappears from the bladders is high (Figs. 3, 4). This high rate proves that the oxygen must be taken up from the swim-bladders by blood circulating through their walls. Conclusions can also be drawn concerning the mechanics of air breathing. During the periods between inhalations, the changes in the volume of the bladders due to variations in their carbon dioxide content are negligible. The reduction in the volume of the bladders through the uptake of oxygen is also small, as can be seen from the following example. If we assume that the oxygen tension after inhalation reaches 100 mm. Hg (F Ot about 14%) and subsequently falls to 15 mm. Hg (F o, 2%), the volume of the bladder would be diminished only by 12%. However, we always observed a marked rise in oxygen tension after inhalation. This would only have been possible if a comparatively large volume of atmospheric air had been added to the residual volume. From the degree of dilution that was measured in the left bladder it was calculated that the tidal volume of air inhaled was, on the average, about one and a half times greater than the residual volume (Table 3). This means that the volume of the bladder must have been reduced, by expiration, to about 40% before the inhalation took place, otherwise hyperinflation of the bladder would have occurred. It follows, therefore, that not only inspiration, but also expiration, must take part in the exchange of gases between the bladder and the atmosphere. The degree by which the carbon dioxide in the swim-bladder was diluted by the inhaled air was always lower than that of the oxygen (Table 3). The quick rise of carbon dioxide tension in the bladders after initial dilution can be attributed to the high rate of diffusion of this gas. The differences between calculated dilutions of oxygen and carbon dioxide show that carbon dioxide is equilibrated between the bladder and the blood much more quickly than oxygen is. In spite of this, the amount of carbon dioxide eliminated by expiration was very small in comparison with the oxygen taken up from the bladders. It seems, therefore, that aquatic respiration is sufficient 3-2

10 36 A. M. ABDE MAGID, Z. VOKAC AND NAS E DIN AHMED under normal conditions to eliminate carbon dioxide from the blood, mainly because its diffusion rate is more than twenty times higher than that of oxygen. The uptake of oxygen from the swim-bladders is reflected in the regulation of aquatic breathing even under normal conditions when the oxygen tension of the water is higher than that in the bladders after inhalation. A temporary adduction of the opercula was observed immediately after inspiration of air. This was followed by a noticeable reduction in respiratory frequency and depth, which gradually increased until the next inspiration. To explain fully the differences between the oxygen tensions of the two bladders and within different regions of the right bladder, anatomical findings must be taken into consideration. The right bladder is about twice as long as the left, and extends the whole length of the body cavity. It is more or less cylindrical in shape and is attached dorsally to the body wall. This is in contrast to the left bladder which is spindle-shaped, with its tapering end loosely situated in the body cavity. The long and narrow form of the right swim-bladder causes grossly uneven distribution of inhaled air within it. The shapes of the two bladders, as expressed by their different lengthwidth ratios, must account for differences in the rate of mixing gases within them and influence considerably the mixing of the air inhaled with the residual. SUMMAY 1. The respiratory function of the swim-bladders of Polypterus senegalus was investigated. Experiments were carried out in tap water with an oxygen tension of about 140 mm. Hg. 2. Both swim-bladders were cannulated through the body-walls of the unrestricted fish. Gas samples were analysed for their oxygen and carbon dioxide content before and after the fish visited the surface. 3. A sharp increase in oxygen and a decrease in carbon dioxide tension was always observed after inhalation. This proves that atmospheric air is actually inspired into the bladders. 4. After inspiration, the amount of oxygen in the bladders decreased rapidly. This shows that oxygen is taken up by the blood, even when the oxygen content of the water is normal. 5. Inspiration of air is preceded by expiration which, on the average, reduces the volume of the bladders to about 40%. 6. The uneven distribution of inhaled air in the right bladder is shown to be due to anatomical configuration. The authors are indebted to Professor Ali Khogali, Head of the Department of Physiology, Faculty of Medicine, and to Professor J.. Cloudsley-Thompson, Head of the Department of Zoology, Faculty of Science, University of Khartoum for offering departmental facilities. We are also grateful to the latter for reading the draft manuscript.

11 Function of swim-bladders of primitive fish 37 EFEENCES ABDE MAGID, A. M. (1966). Breathing and function of the spiracles in Polypterus senegalus. Anim. Behav. 14, ABDE MAGID, A. M. (1967). espiration of air by the primitive fish Polypterus senegalus. Nature, and. 315, BATES, H., BUCHE, E., HETZ, C. W., ODEWAD, G. & SCHWAB, M. (1963). Methods in Pulmonary Physiology. New York-ondon: Hafner Publishing Company Inc. BOWN, M. E. (Edit.) (1957). The Physiology of Fishes, vol. 1. New York: Academic Press Inc. SCHOANDE, P. F. (1947). Analyzer for accurate estimation of respiratory gases in one-half cubic centimeter samples. J. biol. Chem. 167, VOKAC, Z. & MACHODA, F. (1966). Determination of the volume of the pneumothoracic cavity and of the blood gas diffusion rate through its walls. Cs. Fysiol. 15, 73 4 (in Czech).

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