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

Abstract

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 (Hoplias malabaricus). 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.

Cellular oxygen consumption, ROS production and ROS defense in two different size-classes of an Amazonian obligate air-breathing fish (Arapaima gigas)

“…This suggests that, compared to water breathing teleosts, the gills of A. gigas are of reduced importance for ion uptake and ion homeostasis. This is in line with our measurements of Na + /K + -ATPase activity and also of V-ATPase activity in gill tissue and ABO, which revealed that the activity of both ATPases compared to activities recorded in water breathing fish or even the air-breathing Hoplerythrinus unitaeniatus are particularly low, pointing to a low ion exchange capacity of A. gigas gills, in small as well as in larger fish [8,27]. In accordance, the gills' oxygen uptake of A. gigas is lower compared to the water-breathing brown trout (Salmo trutta) [28].…”

“…This is in line with our measurements of Na + /K + -ATPase activity and also of V-ATPase activity in gill tissue and ABO, which revealed that the activity of both ATPases compared to activities recorded in water breathing fish or even the air-breathing Hoplerythrinus unitaeniatus are particularly low, pointing to a low ion exchange capacity of A . gigas gills, in small as well as in larger fish [ 8 , 27 ]. In accordance, the gills' oxygen uptake of A .…”

Air-breathing behavior, oxygen concentrations, and ROS defense in the swimbladders of two erythrinid fish, the facultative air-breathing jeju, and the non-air-breathing traira during normoxia, hypoxia and hyperoxia

“…Although the whole procedure was completed within 2 or 3 min, oxygen could have been removed from the bladder during this time and not replaced, resulting in lower oxygen values. In a previous study, we measured an oxygen uptake of 5.6 ± 0.6 µmol g − 1 h − 1 for jeju at a temperature of 29–32 °C (Wood et al 2016 ). Therefore, a 100 g of jeju would consume about 19 µmol of oxygen within 2 min.…”

Gills versus kidney for ionoregulation in the obligate air-breathingArapaima gigas, a fish with a kidney in its air-breathing organ

“…Rather they decrease ion fluxes and N-waste excretion rates across the gills during aquatic hypoxia by selective reductions in branchial permeability, without apparently compromising the capacity for O 2 uptake. Most importantly, a facultative air-breathing Amazonian teleost, the jeju (Hoplerythrinus unitaeniatus) was able to simply avoid the gillperturbing effects of both aquatic hypoxia and aquatic hyperoxia by resorting to air-breathing (Wood et al, 2016). Therefore, our fourth and final hypothesis was that A. gigas would be able to avoid the symptoms of the osmorespiratory compromise at the gills during aquatic and aerial hypoxia and hyperoxia.…”