Gill Remodeling in Crucian Carp during Sustained Exercise and the Effect on Subsequent Swimming Performance

Gill remodeling can be extensive in crucian carp, where up to a 7.5-fold increase in gill surface area has been observed during exposure to hypoxia through a reduction in the interlamellar cell mass (ILCM) and increased lamellar protrusion that has been hypothesized to be signaled by the need to maximize oxygen uptake under a given condition. Sustained aerobic exercise may have the greatest influence on oxygen demand in fish; however, its effect on gill remodeling in crucian carp has not been investigated. The specific objectives of this study were to determine (i) whether sustained aerobic exercise induces gill remodeling in the crucian carp, (ii) whether gill remodeling following sustained exercise affects the maximum critical swimming speed (U-crit) and maximal oxygen consumption rate (M) over dotO(2) and (iii) whether gill remodeling following sustained exercise is associated with trade-offs related to ionoregulation. We measured (M) over dotO(2) in crucian carp at each step during an initial U-crit test (U-crit1), forced them to swim at 70% of U-crit for 40 h, and then conducted a second U-crit test (U-crit2). From rest to U-crit1 (7-8 h), we observed a significant increase in protruding lamella height and area of the gills and a reduction in ILCM height and volume, likely associated with partial shedding of the ILCM, indicating that gill remodeling during exercise is rapid. Further changes were observed between U-crit1 and U-crit2, with statistically significant increases in protruding lamellar height, basal length and area, and a statistically significant reduction in protruding lamellar thickness and ILCM height and volume. Interestingly, there was no significant difference between U-crit1 and U-crit2 values, nor in maximal (M) over dotO(2) measured at U-crit1 and U-crit2. Furthermore, there was no significant difference in plasma osmolarity, [Na+], or [Cl-] in fish at rest, following U-crit1 or U-crit2. Thus, while these data support the hypothesis that the need to maximize oxygen uptake is an important signal for gill remodeling, which can occur quite rapidly (within 7 h at 15 degrees C), the physiological implications of remodeling during exercise are less clear.