The transition from water breathing to air breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus
The evolutionary transition from water breathing to air breathing involved not only a change in function of the organs of respiratory gas exchange and N waste excretion, but also in the organs of ion uptake from the environment. A combination of in vivo and in vitro techniques was used to look at the relative importance of the gills versus the gut in Na+ Cl and K+ balance in two closely related erythrinid species: a facultative air breather, the jeju (Hoplerythrinus unitaeniatus) and an obligate water breather, the traira (Hopliasmalabaricus) The jeju has a well vascularized physostomous swimbladder, while that in the traira is poorly vascularized, but the gills are much larger. Both species are native to the Amazon and are common in the ion poor, acidic blackwaters of the Rio Negro. Under fasting conditions, the traira was able to maintain positive net Na+ and Cl balance in this water, and only slightly negative net K+ balance. However, the jeju was in negative net balance for all three ions and had lower plasma Na+ and Cl concentrations, despite exhibiting higher branchial Na+,K+ATPase and v type H+ATPase activities. In the intestine, activities of these same enzymes were also higher in the jeju, and in vitro measurements of net area specific rates of Na+ Cl and K+ absorption, as well as the overall intestinal absorption capacities for these three ions, were far greater than in the traira. When acutely exposed to disturbances in water O2 levels (severe hypoxia ~15 or hyperoxia ~420 saturation) gill ionoregulation was greatly perturbed in the traira but less affected in the jeju, which could "escape" the stressor by voluntarily air breathing. We suggest that a shift of ionoregulatory capacity from the gills to the gut may have occurred in the evolutionary transition to air breathing in jeju, and in consequence branchial ionoregulation, while less powerful, is also less impacted by variations in water O2 levels.
Journal of Comparative Physiology B