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

Abstract

In Arapaima gigas, an obligate air-breather endemic to ion-poor Amazonian waters, a large complex kidney runs through the air-breathing organ (ABO). Previous indirect evidence suggested the kidney, relative to the small gills, may be exceptionally important in ionoregulation and N-waste excretion, with support of kidney function by direct O2 supply from the air-space. We tested these ideas by continuous urine collection and gill flux measurements in ∼700g fish. ATPase activities were many-fold greater in kidney than gills. In normoxia, gill Na+ influx and efflux were in balance, with net losses of Cl− and K+. Urine flow rate (UFR, ∼11 ml kg−1 h−1) and urinary ions (< 0.2 mmol L−1) were exceptional, with [urine]/[plasma]ratios of 0.02-0.002 for K+, Na+, and Cl−, indicating strong reabsorption with negligible urinary ion losses. Urinary [ammonia] was very high (10 mmol L−1, [urine]/[plasma] ∼20) indicating strong secretion. The kidney accounted for 21 – 24% of N-excretion, with ammonia dominating (95%) over urea-N through both routes. High urinary [ammonia] was coupled to high urinary [HCO3−]. Aerial hypoxia (15.3 kPa) and aerial hyperoxia (>40.9 kPa) had no effects on UFR, but both inhibited branchial Na+ influx, revealing novel aspects of the osmo-respiratory compromise. Aquatic hypoxia (4.1 kPa), but not aquatic hyperoxia (>40.9 kPa), inhibited gill Na+ influx, UFR and branchial and urinary ammonia excretion. We conclude that the kidney is more important than gills in ionoregulation, and is significant in N-excretion. While not definitive, our results do not indicate direct O2 supply from the ABO for kidney function.