Publisher Summary This chapter discusses oxygen and carbon dioxide transfer across fish gills. The gills of fish are the major site, though not the only one, for oxygen and carbon dioxide transfer. The skin and fins may also serve in this capacity and many fish have evolved accessory air-breathing organs. These may be the modifications of the skin, buccal, pharyangeal, or gill surface, or they may be the regions of the gut or the swim bladder. In general, the gills of fish are the major pathway for oxygen and carbon dioxide transfer between the environment and the body tissues. The oxygen stores within the body, with the exception of that in the swim bladder, are small. Carbon dioxide stores in the body are large as compared with the rate of production. At resting rates of CO 2 production, it would take the animal several hours to accumulate the equivalent of the body CO 2 stores. Thus, minor changes in the magnitude of the CO 2 stores—for example, related to the acidification of the body tissues—can have a marked effect on CO 2 excretion across the gills.

5 Oxygen and Carbon Dioxide Transfer Across Fish Gills

This chapter describes the hemoglobin (Hb) structure and function in fishes. Hb of most vertebrates is a tetrameric globular protein consisting of two α and two β polypeptide chains, each having an oxygen-binding heme. The oxygen affinity of Hb varies with globin structure, giving rise to species differences that relate to differences in primary structure. The hydrogen ion equilibria of Hb are fundamental to both the structure and the physiological function of the protein. The exchange of H + between protein and solvent is important for blood CO 2 transport and it makes Hb an effective nonbicarbonate buffer that limits fluctuations in blood pH upon acid or base additions. The acidic carboxyl groups of glutamic acid and aspartic acid residues are negatively charged at physiological pH and are titrated only when pH falls below 6. Basic groups, such as the guanidyl group of arginine and the amino group of lysine side chains, are positively charged at physiological pH and release H + only when the pH exceeds above 9. It is found that the fixed acid Haldane effect is generally large in teleosts, but differs among species.

1 Hemoglobin Structure and Function

Stress from fishing capture can incite potentially lethal physiological changes in fishes. Blood acid-base status has routinely been utilized to gauge the magnitude of the stress response, which is dependent on the nature of the capture event and metabolic capacity of the species in question. The mortality induced by demersal longline capture has been shown to vary among taxonomically similar carcharhinid elasmobranchs. In this study, we aimed to: (1) quantify and compare blood acid-base disturbances associated with longline capture in five carcharhinid species; (2) examine the extent to which these disturbances correspond with reported at-vessel mortality rates; and (3) investigate how interspecific differences in the physiological stress response could relate to life history, ecology, and phylogeny. Results showed that blood acid-base disturbances from longline-capture varied between species, with relative degrees of disturbance by species proportional to previously reported at-vessel mortality rates. In addition, the degree in which metabolic and respiratory acidoses influenced relative depressions in blood pH also differed by species. The differences in blood acid-base status point to discrepancies in the aerobic and anaerobic capacities among these taxonomically similar species, and are important when considering the effects of, and possible means to mitigate deleterious consequences from, longline fishing capture.

Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks.

Control of ventilation in the hypercapnic skate Raja ocellata: I. Blood and extradural fluid.

Two major strategies are apparent for the regulation of gas transport by vertebrate blood except in the myxinoids, which seem to have little scope for such regulation. In lampreys and teleost fish, haemoglobins have low buffering capacities and large Bohr/Haldane effects. Na+/H+ exchange plays an important role in the control of haemoglobin oxygen-affinity in these vertebrate groups. The large Bohr/Haldane effect also facilitates carbon dioxide transport: the blood (or erythrocyte) pH increases upon deoxygenation, thus increasing the concentration of bicarbonate formed at a given carbon dioxide tension. In lampreys, the bicarbonate permeability of the erythrocyte membrane is low. As a consequence, extracellular acid loads cannot be buffered by haemoglobin. In contrast, teleost erythrocytes possess a functional anion exchange, allowing extracellular proton loads to be buffered by haemoglobin. However, because the buffering capacity of teleost haemoglobins is low, buffering of extracellular acid loads is less effective in teleost fish than in elasmobranch fish and in air-breathing vertebrates whose haemoglobins have a high buffering capacity. However, the high buffering capacity of the haemoglobins diminishes the possibility of regulating haemoglobin oxygen-affinity via secondarily active Na+/H+ exchange, because intracellular pH changes, caused by proton efflux, remain small.

Oxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transport.

The oxygenation-linked, allosteric interactions of erythrocytic organic phosphates and urea with the haemoglobin (Hb), and the functional significance of the Hb multiplicity, were studies in an elasmobranch, Squalus acanthias. The autochthonous red cell nucleoside triphosphates (NTP) ATP and GTP (guanosine triphosphate) strongly depress O2 affinity of the stripped (cofactor-free) Hb and increase cooperativity in O2 binding. As previously found in teleost Hbs, GTP exerts a greater effect than ATP at the same concentration. Urea, in contrast, increases O2 affinity and depresses cooperativity. It also antagonizes the modulator effectivity of NTP at physiological NTP/Hb concentration ratios. Deoxygenation of the Hb raises blood pH. This Haldane effect contrasts with earlier findings for Pacific specimens, but accords with the presence of a Bohr effect (phi = delta log P50/delta pH). S. acanthias Hb resolves into six main components (three pairs) on the basis of isoelectric point. There is no evidence for radical functional differentiation as found in teleosts with electrophoretically anodal and cathodal Hb components. The physiological implications of the findings and the possible molecular mechanisms basic to the NTP and urea effects are discussed.

R. M. Wells

Papers

Allosteric interactions governing oxygen equilibria in the haemoglobin system of the spiny dogfish, Squalus acanthias.