Eyeless Mexican cavefish save energy by eliminating the circadian rhythm in metabolism

Abstract

The eyed surface form and eyeless cave form of the Mexican tetra Astyanax mexicanus experience stark differences in the daily periodicities of light, food and predation, factors which are likely to have a profound influence on metabolism. We measured the metabolic rate of Pachón cave and surface fish at a fixed swimming speed under light/dark and constant dark photoperiods. In constant darkness surface forms exhibited a circadian rhythm in metabolism with an increase in oxygen demand during the subjective daytime, whereas cave forms did not. The lack of circadian rhythm in metabolism leads to a 27% energy savings for Pachón cave fish compared to surface fish when comparing both forms in their natural photoperiods. When surface forms were tested under constant dark conditions they expended 38% more energy than cave forms under equivalent conditions. Elimination of the circadian rhythm in metabolism may be a general feature of animals that live in perpetually dark food-limited environments such as caves or the deep sea.

Figure 1. Schematic of the respirometer used in the study (not to scale).

Figure 2. Comparison of the metabolic rate (O_2mean) of A. mexicanus over 7 days at a set swimming speed and two photoperiods.

(A, C, E, G, I) 12:12 light:dark and (B, D, F, H, J) 24 h dark photoperiod. Grey areas represent dark conditions. A to D display the traces for all individuals with the mean superimposed. E and F display mean and 95% confidence intervals. G and H display 24 h running means, and the arrow indicates when acclimation was deemed complete. I and J display the ratio of daytime:nighttime total oxygen consumption.

Figure 3. Daily variation in the allometrically scaled metabolic rate (O_2mean) of A. mexicanus at a set swimming speed and two photoperiods.

(A–C) a 12:12 light:dark and (D–F) 24 h dark photoperiod. Grey areas represent dark conditions. Each trace represents the combined data for 5.5 days. A, B, D and E display the traces for all individuals with the mean superimposed. C and F display mean with 95% confidence intervals. Asterisks indicate time periods where means differ at P<0.05.