The swimming physiology of the European eel under regulable hyperbaric conditions

The European eel lives as so-called yellow eel in the European freshwater system. With a process named silvering the eel prepares for the spawning migration back to the Sargasso Sea for reproduction. During this journey, which takes 4 to 6 month, the eel sexually matures, but does not feed. Within recent years a rapid decline in population size was observed, and the European eel is listed as an endangered species. Overfishing, toxicological threat and parasite infection are discussed as possible reasons for this decline. Currently it is attempted to artificially ripen eels for farming, and to obtain more detailed knowledge about the spawning migration for better protection of the species. While the attempts to artificially ripen eels were of limited success so far, swim tunnel experiments showed that the eel indeed can migrate for several months without feeding. These experiments were performed at constant atmospheric pressure (1 bar). Recent field studies, however, revealed that the migrating eel, by performing daily migrations between 200-300 m depth at nighttime and 600-800 m depth at daytime, is exposed to very high and variable hydrostatic pressures. The hydrostatic pressure directly affects pressure and volume of the swimbladder, the hydrostatic organ of the eel. Ideally, the volume of the swimbladder should be kept constant, independent of water depth, in order to reduce the energy expenditure for swimming, which appears almost impossible, according to our current knowledge about the mechanisms of gas secretion. It is therefore hypothesized that swimming at variable and high hydrostatic pressure improves gas secretion into the swimbladder and initiates the ripening process of the gonads. Furthermore, both processes are significantly impaired by toxicants and by swimbladder parasites. In order to test these hypotheses in a project called The swimming physiology of the European eel under regulable hyperbaric conditions (SPEER) a newly developed pressure controlled swim tunnel system will be used which, for the first time, allows swimming eels at variable hydrostatic pressures up to 10 bars. In the swim tunnel swimming behavior and energetics will be analyzed. By measuring gene expression and enzyme activities in swimbladder tissue the possible contribution of the swimbladder to the energetics of the spawning migration will be assessed, and the mechanisms preventing damaging effects of oxygen radicals, expected to form under the high oxygen pressures present in the swimbladder, will be determined. Furthermore, the impact of toxicants (PCB) and of swimbladder parasites on swimming performance, energetics and swimbladder function will be analyzed. Finally, by measuring gene expression in ovaries it will be determined whether migrating at high and variable hydrostatic pressure contributes to the development of sexual maturity.

During the spawning migration eels perform diurnal vertical migrations, swimming at a depth of about 200 - 300 m at night time, and 600 - 800 m during daytime. Based on model calculations it appears impossible that with the encountered rapid changes in hydrostatic pressure swimbladder volume can be kept constant in order to retain a status of neutral buoyancy. To asses the role of the swimbladder and to measure energy consumption during prolonged swimming under elevated hydrostatic pressure and to assess the effect of temperature changes we exercised eels in a swim tunnel at atmospheric pressure and at a pressure of 8 bar for several hours and up to six weeks. Analysis of gene expression at the level of mRNA suggested an activation of acid secretion in swimbladder gas gland cells, which would stimulate gas secretion into the swimbladder. It appears that, although the swimbladder cannot provide full buoyancy compensation during the vertical migrations, it shows some secretory activity and thus contributes to buoyancy regulation. Oxygen consumption in the swim tunnel was temperature dependent, and oxygen uptake was particularly elevated in the higher temperature range (15.5 - 19oC). Elevated hydrostatic pressure, however, had no significant effect on oxygen consumption. This information will be very helpful for an assessment of the energy requirements of the spawning migration, which may take 5 to 6 months, or perhaps even more than a year. We also measured oxygen consumption and acid secretion of isolated swimbladder gas gland cells in vitro, revealing that at glucose concentrations above 1.5 mmol*l-1 oxygen consumption is quite constant and can hardly be modified. Acid secretion, however, can by modified by pharmacological treatment, and the pentose phosphate shunt significantly contributed to acid production. This underlines the role CO2, produced in the pentose phosphate shunt, in swimbladder function. We also localized aquaporin in swimbladder gas gland cells and in endothelial cells of swimbladder capillaries. Aquaporins have been shown to facilitate CO2 diffusion. We therefore propose that presence of aquaporin in the swimbladder facilitates CO2 diffusion, supporting filling of the swimbladder with CO2 and supporting acidification of blood in order to reduce the oxygen carrying capacity of the haemoglobin and support oxygen secretion into the swimbladder. Analysis of gene expression in rete mirabile tissue revealed presence of many different transport proteins, transporting ions as well as metabolites. Back-diffusion of ions and metabolites in the counter current system will support the generation high gas partial pressures, and thus support swimbladder function. Our results therefore show that, although the swimbladder will not be able to provide neutral buoyancy by keeping the volume constant during vertical migrations, it will at least partially contribute to buoyancy during the spawning migration.