Role of the Swimbladder Rete of Fish in Secretion of Inert Gas and Oxygen¹

The partial pressure of oxygen and other gases dissolved in water and subjected to high hydrostatic pressure is increased. Although this was established many years ago it remains a problematical phenomenon. The review deals with some of the underlying theoretical difficulties and discusses the kinetic and environmental implications of the pressure-enhanced partial pressures.

Gas gland cells of the European eel (Anguilla anguilla) are specialized for the production and secretion of acidic metabolites. Although typically exposed to high oxygen partial pressures, they convert glucose mainly into lactate, but also produce CO₂ in the pentose phosphate shunt. Only a very small fraction of glucose is oxidized via aerobic metabolism. Although the buffer capacity of gas gland cells appears to be high, even at low extracellular pH values intracellular pH is always kept about 0.2–0.3 pH-units more acidic. Thus, under all physiological conditions proton concentration within gas gland cells is higher than in the extracellular fluid, facilitating proton extrusion. Diffusion of CO₂, Na⁺/H⁺-exchange, sodium-dependent anion exchange and a V-ATPase represent the pathways available for proton secretion. While under resting conditions the sodium-dependent pathways and diffusion of CO₂ appear to be the dominating mechanisms for acid secretion, at low intracellular pH the contribution of Na⁺/H⁺-exchange and of V-ATPase appear to increase, while sodium-dependent anion exchange becomes less important. The mechanisms regulating the activity of these acid-secreting pathways and of the metabolism responsible for the production of protons are largely unknown.

Oreochromis alcalicus grahami is a small cichlid fish that lives in shallow peripheral lagoons of Lake Magadi, Kenya. The internal surface of the air-bladder is highly vascularized, illustrating possible utilization as an accessory respiratory organ. The wall of the bladder consists of five distinct tissue layers. From the outer to the inner surfaces are: a squamous, undifferentiated epithelial cell; a collagen-elastic tissue space; a smooth muscle tissue band; an inner connective tissue space; and columnar gas-gland cells projecting into the lumen. The cell membrane over the perikarya of the gas-gland cells was sporadically broken. The disruptions were ascribed to possible physical damage by discharging gas-bubbles. Juxtaluminally, the gas-gland cells attached across tight junctions. The cells have highly euchromatic nuclei and conspicuously large intracytoplasmic secretory bodies. On the blood capillary facing (basal) aspect, the cell membrane of the gas-gland cells is highly amplified. The cells insert onto a smooth muscle tissue band. The morphological features and the topographical arrangement of the gas-gland cells in O. a. grahami are indicative of an operative exchange of materials between them and the underlying tissue components especially the blood capillaries. For a fish that subsists in hot, highly saline and alkaline water heavily invested by avian predators and where the partial pressure of oxygen diurnally shifts from virtual anoxia to hyperoxia, development of a versatile air-bladder for efficient buoyancy control conforms to the functional demands placed on it by a unique environment. Illustratively, instead of the gas-gland morphology in O. a. grahami resembling that in the freshwater fishes, the group from which the fish has evolved, it compares more closely to that of the marine fish. This similarity suggests amazing parallel evolutionary adaptation to biophysically corresponding aquatic milieus.

This chapter describes the problem of buoyancy faced at deep-sea levels and discusses the swim bladder function of fishes. Fish produce hydrodynamic lift mainly by using their pectoral fins as hydrofoils. The metabolic power needed to propel the hydrofoils through the water can be calculated from drag on the hydrofoils and speed. Another strategy to achieve neutral buoyancy is to build up and maintain a buoyancy device—that is, compensate for the high density of most tissues by including special structures or organs characterized by a very low density. In many species, the swim bladder consists of two chambers, including a thick-walled section in which gas can be deposited and a thin-walled chamber in which gas can be resorbed. In other fishes, the resorbing part of the swim bladder is reduced to a special section of the secretory bladder, called “oval,” which can be closed off by muscular activity. The reduction of the effective gas-carrying capacity of swim bladder blood is brought about by the metabolic and secretory activity of epithelial gas gland cells. The specific gravity of gas increases with gas pressure; hence, the difference between swim bladder gas density and water density decreases with increasing water depth.

This chapter focuses on the metabolism of the swimbladder tissue in fish. Many fish posses a gas-filled swimbladder as a hydrostatic organ to achieve neutral buoyancy. As a compliant bladder, it obeys Boyle's law and changes pressure and volume with changes in hydrostatic pressure—that is, with water depth. The hydrostatic pressure increases by about 1 atmosphere for every 10 m of water depth. A crucial step in the functioning of the swimbladder is the production and release of metabolites that modify the gas carrying properties of blood passing the tissue. The morphological arrangement of the various layers of swimbladder tissue provides close contact of the cells producing these metabolites—the gas gland cells—to the vascular system and also ensures the accumulation of gas molecules in the bladder and not in the surrounding tissues. The chapter presents a brief discourse on the morphology and histology of the bladder. It elaborates the metabolism of the swimbladder tissue, especially of the gas gland cells, and discusses the role of carbonic anhydrase in the swimbladder epithelium.