The Exchange of Oxygen and Carbon Dioxide Across the Gills of Rainbow Trout

Hughes & Shelton (1962), Hughes (1964) and Rahn (1966) have analysed gas exchange in animals in an aquatic environment, particularly fish, from a theoretical viewpoint. These authors provide equations which permit a quantitative analysis of the gas-exchange process. From these, it is possible to determine the relative effectiveness of the exchange process (Hughes & Shelton, 1962) in a single animal under a variety of conditions, or to compare gas exchange in different animals, independent of the environment in which they live, whether it be aquatic or aerial.

Much of the present information on the circulatory and respiratory systems of fishes is of a fragmentary nature encompassing fish of widely differing habitat, habit and species. This has limited any analysis of gas exchange in fish, as well as any comparison between fish and air-breathing mammals. An effort has been made, however, to measure many of the factors affecting gas exchange across the gills of fish in a simultaneous and integrated manner by Holeton & Randall (1967 a, b) and by Stevens & Randall (1967 a, b). These experiments were carried out on intact, unanaesthetized, unrestrained rainbow trout (Salmo gairdneri) subjected to two conditions: first, hypoxia (Holeton & Randall, 1967 a, b), and secondly, moderate exercise (Stevens & Randall, 1967a, b). This data is sufficiently extensive to permit an analysis of gas exchange across the gills of a single species of fish.

The symbols employed are somewhat different from those used by Hughes & Shelton (1962) and Hughes (1964), but are generally those used in mammalian respiration as described in Ruch & Patton (1965), p. 769, and employed by Rahn (1966). The terms used are :

Hughes & Shelton (1962) and Hughes (1964) have compared gas exchange at the gills with known relationships derived from studies upon compact heat exchangers. They show how several heat-exchanger relationships are of use in analysing gasexchange systems. One such relationship is the effectiveness of transfer. Effectiveness (Hughes & Shelton, 1962) is the ratio of the actual gas transfer (⁠ etc.) to the maximum rate of gas transfer possible, expressed as a percentage.

The effectiveness of oxygen uptake by the blood is expressed by the following equation :

Maximum oxygen uptake will occur if the blood leaving the gills is at the same partial pressure of oxygen as the inspired water.

The solubility of oxygen in the blood is not constant but varies with the slope of the oxygen dissociation curve of the blood.

The same form of equation can be used to determine the effectiveness of oxygen removal from water, the effectiveness of carbon dioxide uptake by the water, and the effectiveness of carbon dioxide removal from the blood.

These equations were applied to data reported by Holeton & Randall (1967 a, b) and Stevens & Randall (1967 a, b). These data were obtained from rainbow trout (Salmo gairdneri) in fresh water. The experiments of Holeton & Randall (1967) were carried out at 15 ± 1i° C., whereas those of Stevens & Randall (1967 b) were at 4-8° C. The solubility of oxygen in blood was determined from oxygen dissociation curves constructed in this laboratory (Randall, Beaumont & Holeton, unpublished) unless otherwise stated.

Changes in the effectiveness of gas exchange, capacity-rate ratio of blood and water, and the oxygen transfer factor, during hypoxia and during moderate exercise, were calculated.

The effectiveness of blood oxygenation is very near 100 % in the resting rainbow trout at environmental temperatures of approximately 5 and 15° C. Moderate exercise produced only slight decrease in effectiveness (Fig. 1); but a reduction in the oxygen content of the water resulted in a marked decrease in effectiveness, reaching values of 30-40% at environmental of 40 mm. Hg (Fig. 2). Removal of oxygen was 30% effective in experiments carried out at approximately 15° C. (Fig. 2) but was only 11% at temperatures of 5-8° C. (Fig. 1). Hypoxia and moderate exercise had very little effect on the effectiveness of oxygen removal from the water.

These results illustrate the very high effectiveness of gas exchange across the gills of fishes. Only during hypoxia did the effectiveness of loading the blood with oxygen fall much below 95-100 %.

The differences in the effectiveness of oxygen removal from the water, in the resting fish, reported in Figs. 1 and 2 are probably related to differences in the velocity of water flow. The calculated values reported in Fig. 1 were obtained from data collected from fish exposed to water velocities of about 7 cm./sec. whereas the calculated values reported in Fig. 2 were from fish exposed to water velocities of 2 cm./sec.

The capacity-rate ratio of blood to water at the gills is between 0·2 and 0·3 in the resting rainbow trout (Figs. 3 and 4). Moderate exercise resulted in a small increase, whereas hypoxia produced a doubling of capacity-rate ratio. As Hughes & Shelton (1962) have pointed out, the capacity-rate ratio can have a strong influence upon effectiveness. During hypoxia the capacity-rate ratio increased and as might be expected the effectiveness of gas transfer decreased. The increase in the capacity rate for blood during hypoxia must be related to an increased solubility of oxygen in blood, because cardiac output does not alter appreciably (Holeton & Randall, 1967b). The changes in the solubility of oxygen in blood are described by the oxygen dissociation curve, which in turn is dependent upon the characteristics of haemoglobin. The decrease in effectiveness during hypoxia is related therefore to the nature of the oxygen dissociation curve of the blood. A carp, having a haemoglobin with a very high affinity for oxygen (Black, 1940) should be able to maintain a high level of effectiveness of gas transfer even at very low environmental oxygen levels. This presumably confers an advantage to the carp over other fishes, in a hypoxic environment.

There is a marked increase in the transfer factor of the gills of trout in response to hypoxic conditions in the environment (Fig. 5); during exercise the transfer factor increased almost fivefold (Fig. 3), indicating that during both hypoxia and exercise there is an increase in the effective exchange area, or a decrease in diffusion distance, or both.

The effectiveness of carbon dioxide removal from the blood did not change markedly during exercise, and was of the order of 50 % (Fig. 1). The carbon dioxide content of blood afferent and efferent to the gills was estimated using the data of Stevens & Randall (1967b) and a carbon dioxide dissociation curve was constructed from data on the carbon dioxide content of the blood of rainbow trout (Black, Kirkpatrick & Tucker, 1966; Ferguson & Black, 1941). The effectiveness of carbon dioxide uptake by the water varied between 4 and 7 % (Fig. 1). These values were obtained assuming a respiratory quotient of 1, and a solubility coefficient for carbon dioxide in water of 1·8 ml./I./mm. Hg ⁠. The low effectiveness of carbon dioxide uptake by the water is a result of the high capacity of water for carbon dioxide.

The ratio of diffusion coefficients for oxygen and carbon dioxide in tissues is about 1 : 20. The mean gradient driving oxygen into the blood is approximately 70 mm. Hg. One would expect, therefore, the mean gradient for carbon dioxide between blood and water to be about 3 to 4 mm. Hg. The of the arterial blood is of the order of 2· 5 mm. Hg. This is probably determined by the diffusion characteristics of the gills. Holeton & Randall (1967b) recorded slightly lower values than Stevens & Randall (1967b), (1·5 and 2·5 mm. Hg respectively). This may be a reflexion of differences in diffusion characteristics of the gills due to differences in temperature (15 ± 1° C. and 4-8° C. respectively).

An increase in venous would probably not result in an increase in dorsal aortic -The added load on the exchange system could be dealt with easily, because of the high capacity of water for carbon dioxide relative to oxygen. Thus an increase in the effectiveness of carbon dioxide removal from the blood would normally result from an increase in venous ⁠, the arterial remaining fairly constant.

A comparison of gas exchange in man and rainbow trout indicates that in both cases oxygen uptake by the blood approaches 100% effectiveness (Table 1). This is due to the presence of haemoglobin in the blood. Oxygen removal from the medium is of the same order of magnitude in both aerial and aquatic respiration (Table 1), although, as emphasized previously, the value for the effectiveness of oxygen removal from water reported here is probably minimal rather than maximal, and may approach 100% under certain environmental conditions. In general it is probably higher than that for aerial respiration.

The major difference between aerial and aquatic respiration is related to the effectiveness of carbon dioxide removal from the blood (Table 1). This results in high carbon dioxide levels in arterial blood of terrestrial animals compared with the low carbon dioxide levels recorded in fish. The low effectiveness of carbon dioxide removal from blood in man is related to the tidal nature of breathing. A second factor influencing carbon dioxide removal from blood is that equal volumes of oxygen and carbon dioxide exert the same pressure in air, whereas the ratio of their solubility coefficients in water is between 1:24 and 1:35 depending on the temperature (Rahn, 1966). As the respiratory quotient is about 1, the differences in the capacities of the two media for carbon dioxide relative to oxygen result in differences in the percentage effectiveness of carbon dioxide uptake by air and water. Effectiveness of carbon dioxide uptake in air is 60 % of maximum, whereas carbon dioxide uptake by the water is only 4-6 % of maximum. Because of the large capacity of water for carbon dioxide compared with oxygen, removal of carbon dioxide from the blood is not a problem.

In man a compromise is made between removal of carbon dioxide and water loss. Tidal ventilation is possible because of the low density and high oxygen content of air compared with water. This minimizes water loss, but reduces the percentage effectiveness of carbon dioxide removal.

In fish there are similar osmotic problems, but tidal ventilation is not practical because of the high density and low oxygen content of the medium. Those factors which increase gas exchange will augment exchange of ions and water. The uptake of water at the gills in fresh water is offset by a high blood pressure and ionic losses are reduced by special cells which actively transport ions from the water into the blood.

This investigation was supported by grants from the National Research Council of Canada and the B.C. Heart Foundation. Some of the experiments were carried out at the Biological Station, Nanaimo, B.C. and we thank Dr Brett and the Biological Station for support given to this project.