Countercurrent Concentration and Gas Secretion in the Fish Swim Bladder

Abstract

Many fish possess a gas-filled swim bladder, and the gas molecules enter the bladder by diffusion from its capillaries and epithelium. The high gas partial pressures necessary to drive diffusion are produced in two steps. First, in the blood perfusing the swim bladder capillaries the physical solubility of gases is reduced via the salting-out effect, and gases are released from a chemical binding site via blood acidification (e.g., Root effect for O₂; conversion of HCO₃⁻ to CO₂). These effects result in an increase in the gas partial pressure in blood. In a second step, this initial increase in partial pressure (the "single concentrating effect") is multiplied by back diffusion of gas molecules in the countercurrent system of the rete mirabile. For inert gases, the salting-out effect, induced by the release of lactic acid from the gas gland cells in the swim bladder tissue, results in a probably small reduction of solubility, while the acid-induced decrease in hemoglobin O₂-carrying capacity (Root effect) and the release of CO₂ from HCO₃ ⁻, combined with the release of anaerobically produced CO₂ from gas gland cells, result in a significant single concentrating effect for O₂ and CO₂. The relatively high permeability of the rete capillaries for gases allows for back diffusion, and thus for countercurrent concentration, of gases. The rete mirabile is, however, permeable not only for gases but also for metabolites and salt molecules, and the countercurrent concentration of solutes enhances the countercurrent concentration of gas molecules. This is particularly important for inert gases because their single concentrating effect is small. Back diffusion of CO₂ in the rete mirabile not only results in a countercurrent concentration of CO₂ but also enhances the partial pressure increase of O₂ by decreasing the hemoglobin O₂-carrying capacity within the arterial capillaries of the rete. This interdependence of O₂ and CO₂ may apply to countercurrent systems in other tissues as well, for example, to the skeletal muscle. Hence, the swim bladder rete mirabile may serve as a model tissue for studies of gas exchange and countercurrent blood flow in other organs. Furthermore, the regulation of countercurrent eficiency and gas secretion promises to be an interesting area of research, including also the regulation of metabolic activity and acid production in the gas gland cells.