Impact of ontogenetic changes in branchial morphology on gill function in Arapaima gigas

Abstract

Soon after hatching, the osteoglossid fish Arapaima gigas undergoes a rapid transition from a water breather to an obligate air breather. This is followed by a gradual disappearance of gill lamellae, which leaves smooth filaments with a reduced branchial diffusion capacity due to loss of surface area, and a fourfold increase in diffusion distance. This study evaluated the effects these changes have on gill function by examining two size classes of fish that differ in gill morphology. In comparison to smaller fish (approximately 67.5 g), which still have lamellae, larger fish (approximately 724.2 g) without lamellae took up a slightly greater percentage of O2 across the gills (30.1% vs. 23.9%), which indicates that the morphological changes do not place limitations on O2 uptake in larger fish. Both size groups excreted similar percentages of CO2 across the gills (85%-90%). However, larger fish had higher blood PCO2 (26.51.9 vs. 16.51.5 mmHg) and HCO3(-) (40.2 +/- 2.9 vs. 33.6 +/- 4.5 mmol L(-1)) concentrations and lower blood pH (7.58 +/- 0.01 vs. 7.70 +/- 0.04) than did smaller fish, despite having lower mass-specific metabolisms, suggesting a possible diffusion limitation for CO2 excretion in larger fish. With regard to ion regulation, rates of diffusive Na+ loss were about 3.5 times higher in larger fish than they were in smaller fish, despite the lowered branchial diffusion capacity, and rates of Na+ uptake were higher by about the same amount despite 40% lower activity of branchial Na+/K+-ATPase. Kinetic analysis of Na uptake revealed an extremely low-affinity (K(m) = 587.9 +/- 169.5 micromol L(-1)), low-capacity (J(max) = 265.7 +/- 56.8 nmol g(-1) h(-1)) transport system. These data may reflect a general reduction in the role of the gills in ion balance. Renal Na+/K+-ATPase activity was 5-10 times higher than Na+/K+-ATPase activity in the gills, and urine: plasma ratios for Na+ and Cl(-) were very low (0.001-0.005) relative to that of other fish, which suggested an increased role for dietary salt intake and renal salt retention and which was representative of a more "terrestrial" mode of ion regulation. Such de-emphasis of branchial ion regulation confers greatly reduced sensitivity of diffusive ion loss to low water pH. Ammonia excretion also appeared to be impacted by gill changes. Rates of ammonia excretion in larger fish were one third less than that in smaller fish, despite larger fish having blood ammonia concentrations that were twice as high.