Is the air-breathing organ a significant route for CO2 excretion during aquatic hypercapnia in the pirarucu, Arapaima gigas?

The pirarucu is one of the very few obligate air-breathing fish, employing a gigantic, highly vascularized air-breathing organ (ABO). Traditionally, the ABO is thought to serve mainly for O₂ uptake (ṀO₂), with the gills providing the major route for excretion of CO₂ (ṀCO₂) and N-waste. However, under aquatic hypercapnia, a common occurrence in its natural environment, branchial ṀCO₂ to the water may become impaired. Under these conditions, does the ABO become an important route of ṀCO₂ excretion to the air? We have answered this question by measuring ṀCO₂ and ṀO₂ in both air and water phases, as well as the pattern of air-breathing, in pirarucu under aquatic normocapnia and hypercapnia (3% CO₂). Indeed, ṀCO₂ to the air phase via the ABO increased 2- to 3-fold during exposure to high water PCO₂, accounting for 59-71% of the total, with no change in the dominant contribution of the ABO to ṀO₂ (71-75% of the total). These adjustments were quickly reversed upon restoration of aquatic normocapnia. During aquatic hypercapnia, ṀCO₂ via the ABO became more effective over time, and the pattern of air-breathing changed, exhibiting increased frequency and decreased breath volume. Ammonia-N excretion (86-88% of total) dominated over urea-N excretion and tended to increase during exposure to aquatic hypercapnia. We conclude that the ability of the ABO to take on the dominant role in CO₂ excretion when required may have been an important driver in the original evolution of air-breathing, as well as in the functionality of the ABO in modern air-breathing fish.