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

ABSTRACTIn 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 that the kidney, relative to the small gills, may be exceptionally important in ionoregulation and nitrogen (N) waste excretion, with support of kidney function by direct O2 supply from the airspace. We tested these ideas by continuous urine collection and gill flux measurements in ∼700 g 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] ∼17) 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 osmorespiratory 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. Although not definitive, our results do not indicate direct O2 supply from the ABO for kidney function.