Gills and air-breathing organ in O₂ uptake, CO₂ excretion, N-waste excretion, and ionoregulation in small and large pirarucu (Arapaima gigas)

Abstract

In the pirarucu (Arapaima gigas), gill surface area and thus gas exchange capacity of the gills are reduced with proceeding development. It, therefore, is expected that A. gigas, starting as a water breather, progressively turns into an obligate air-breathing fish using an air-breathing organ (ABO) for gas exchange. We assessed the air-breathing activity, O₂ and CO₂ exchange into air and water, ammonia-N and urea-N excretion, ion flux rates, and activities of ion transport ATPases in large versus small pirarucu. We found that even very young A. gigas (4–6 g, 2–3 weeks post-hatch) with extensive gills are air-breathers (18.1 breaths*h⁻¹) and cover most (63%) of their O₂ requirements from the air whereas 600–700-g animals (about 3–4 months post-hatch), with reduced gills, obtain 75% of their O₂ from the air (10.8 breaths*h⁻¹). Accordingly, the reduction in gill surface area hardly affected O₂ uptake, but development had a significant effect on aerial CO₂ excretion, which was very low (3%) in small fish and increased to 12% in larger fish, yielding a hyper-allometric scaling coefficient (1.12) in contrast to 0.82–0.84 for aquatic and total CO₂ excretion. Mass-specific ammonia excretion decreased in approximate proportion to mass-specific O₂ consumption as the fish grew, but urea-N excretion dropped from 18% (at 4–6 g) to 8% (at 600–700 g) of total N-excretion; scaling coefficients for all these parameters were 0.70–0.80. Mass-specific sodium influx and efflux rates, as well as potassium net loss rates, departed from this pattern, being greater in larger fish; hyper-allometric scaling coefficients were > 1.0. Gill V-type H⁺ ATPase activities were greater than Na⁺, K⁺-ATPase activities, but levels were generally low and comparable in large and small fish, and similar activities were detected in the ABO. A. gigas is a carnivorous fish throughout its lifecycle, and, despite fasting, protein oxidation accounted for the major portion (61–82%) of aerobic metabolism in both large and small animals. ABO PO₂ and PCO₂ (measured in 600–700-g fish) were quite variable, and aerial hypoxia resulted in lower ABO PO₂ values. Under normoxic conditions, a positive correlation between breath volume and ABP PO₂ was detected, and on average with a single breath more than 50% of the ABO volume was exchanged. ABO PCO₂ values were in the range of 1.95–3.89 kPa, close to previously recorded blood PCO₂ levels. Aerial hypoxia (PO₂ down to 12.65 kPa) did not increase either air-breathing frequency or breath volume.