Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure

Abstract

Amphibious mangrove killifish, Kryptolebias marmoratus (formerly Rivulus marmoratus), are frequently exposed to aerial conditions in their natural environment. We tested the hypothesis that gill structure is plastic and that metabolic rate is maintained in response to air exposure. During air exposure, when gills are no longer functional, we predicted that gill surface area would decrease. In the first experiment, K. marmoratus were exposed to either water (control) or air for 1 h, 1 day, 1 week, or 1 week followed by a return to water for 1 week (recovery). Scanning electron micrographs (SEM) and light micrographs of gill sections were taken, and morphometric analyses of lamellar width, lamellar length and interlamellar cell mass (ILCM) height were performed. Following 1 week of air exposure, SEM indicated that there was a decrease in lamellar surface area. Morphometric analysis of light micrographs revealed that there were significant changes in the height of the ILCM, but there were no significant differences in lamellae width and length between any of the treatments. Following 1 week of recovery in water, the ILCM regressed and gill lamellae were similar to control fish, indicating that the morphological changes were reversible. In the second experiment, V(CO(2)) was measured in fish continuously over a 5-day period in air and compared with previous measurements of oxygen uptake (V(O(2))) in water. V(CO(2)) varied between 6 and 10 micromol g(-1) h(-1) and was significantly higher on days 3, 4 and 5 relative to days 1 and 2. In contrast to V(O(2)) in water, V(CO(2)) in air showed no diurnal rhythm over a 24 h period. These findings indicate that K. marmoratus remodel their gill structures in response to air exposure and that these changes are completely reversible. Furthermore, over a similar time frame, changes in V(CO(2)) indicate that metabolic rate is maintained at a rate comparable to that of fish in water, underlying the remarkable ability of K. marmoratus to thrive in both aquatic and terrestrial habitats.