Phenotypic flexibility in respiratory traits is associated with improved aerial respiration in an amphibious fish out of water

Abstract

Amphibious fishes have evolved multiple adaptive strategies for respiring out of water, but there has been less focus on reversible plasticity. We tested the hypothesis that when amphibious fishes leave water, enhanced respiratory performance on land is the result of rapid functional phenotypic flexibility of respiratory traits. We acclimated four isogenic strains of Kryptolebias marmoratus to air for 0, 1, 3 or 7 days. We compared respiratory performance out of water with traits linked to the O2 cascade. Aerial O2 consumption rate was measured over a step-wise decrease in O2 levels. There were significant differences between strains, but time out of water had the largest impact on measured parameters. K. marmoratus had improved respiratory performance (lower aerial critical oxygen tension (Pcrit), higher regulation index (RI)) after only 1 day of air exposure and these changes were strongly associated with the change in hematocrit and dorsal cutaneous angiogenesis. Additionally, we found that 1-hour of air exposure induced the expression of four angiogenesis-associated genes, vegfa, angpt2, pecam-1 and efna1 in the skin. After 7 days in air, respiratory traits were not significantly linked to the variation in either aerial Pcrit or RI. Overall, our data indicate that there are two phases involved in the enhancement of aerial respiration; an initial rapid response (1 day) and a delayed response (7 days). We found evidence for the hypothesis that respiratory performance on land in amphibious fishes is the result of rapid flexibility in both O2 uptake and O2 carrying capacity.