The amphibious fish Kryptolebias marmoratus uses different strategies to maintain oxygen delivery during aquatic hypoxia and air exposure

Despite the abundance of oxygen in atmospheric air relative to water, the initial loss of respiratory surface area and accumulation of carbon dioxide in the blood of amphibious fishes during emersion may result in hypoxemia. Given that the ability to respond to low oxygen conditions predates the vertebrate invasion of land, we hypothesized that amphibious fishes maintain O-2 uptake and transport while emersed by mounting a co-opted hypoxia response. We acclimated the amphibious fish Kryptolebias marmoratus, which are able to remain active for weeks in both air and water, for 7 days to normoxic brackish water (15%, similar to 21kPa O-2; control), aquatic hypoxia (similar to 3.6kPa), normoxic air (similar to 21 kPa) or aerial hypoxia (similar to 13.6kPa). Angiogenesis in the skin and bucco-opercular chamber was pronounced in air-versus water-acclimated fish, but not in response to hypoxia. Aquatic hypoxia increased the O-2-carrying capacity of blood via a large (40%) increase in red blood cell density and a small increase in the affinity of hemoglobin for O-2 (P-50 decreased 11%). In contrast, air exposure increased the hemoglobin O-2 affinity (decreased P-50) by 25% without affecting the number of red blood cells. Acclimation to aerial hypoxia both increased the O-2-carrying capacity and decreased the hemoglobin O-2 affinity. These results suggest that O-2 transport is regulated both by O-2 availability and also, independently, by air exposure. The ability of the hematological system to respond to air exposure independent of O-2 availability may allow extant amphibious fishes, and may also have allowed primitive tetrapods to cope with the complex challenges of aerial respiration during the invasion of land.