The amphibious fish Kryptolebias marmoratus uses alternate strategies to maintain oxygen delivery during aquatic hypoxia and air exposure
Abstract 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 O2 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 7d to normoxic brackish water (15‰, ~21 kPa O2; control), aquatic hypoxia (~3.6 kPa), normoxic air (~21 kPa), or aerial hypoxia (~13.6 kPa). 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 blood O2 carrying capacity via a large (40%) increase in red blood cell density and a small increase in hemoglobin-O2 affinity (P50 decreased 11%). In contrast, air exposure increased hemoglobin-O2 affinity (decreased P50) by 25% without affecting the number of red blood cells. Acclimation to aerial hypoxia both increased O2 carrying capacity and decreased hemoglobin-O2 affinity. These results suggest that O2 transport is regulated both by O2 availability and also independently by air exposure. The ability of the hematological system to respond to air exposure independently of O2 availability may allow extant amphibious fishes and also primitive tetrapods to cope with the complex challenges of aerial respiration during the invasion of land.