Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress

Temperature is a key factor that affects all levels of organization. Minute shifts away from thermal optima result in detrimental effects that impact growth, reproduction and survival. Metabolic rates of ectotherms are especially sensitive to temperature and for organisms exposed to high acute temperature changes, in particular intertidal species, energetic processes are often negatively impacted. Previous investigations exploring acute heat stress have implicated cardiac mitochondrial function in determining thermal tolerance. The brain, however, is by weight, one of the most metabolically active and arguably the most temperature sensitive organ. It is essentially aerobic and entirely reliant on oxidative phosphorylation to meet energetic demands, and as temperatures rise, mitochondria become less efficient at synthesising the amount of ATP required to meet the increasing demands. This leads to an energetic crisis. Here we used brain homogenate of three closely related triplefin fish species (Bellapiscis medius, Forsterygion lapillum, and Forsterygion varium) and measured respiration and ATP dynamics at three temperatures (15, 25 and 30 degrees C). We found that the intertidal B. medius and F. lapillum were able to maintain rates of ATP production above rates of ATP hydrolysis at high temperatures, compared to the subtidal F. varium, which showed no difference in rates at 30 degrees C. These results showed that brain mitochondria became less efficient at temperatures below their respective species thermal limits, and that energetic surplus of ATP synthesis over hydrolysis narrows. In subtidal species synthesis matches hydrolysis, leaving no scope to elevate ATP supply.

Automated summary

Temperature is a key factor affecting all levels of organization in organisms, with even minute shifts from thermal optima leading to detrimental effects on growth, reproduction, and survival. Ectotherms are particularly sensitive to temperature changes, especially intertidal species, which often experience negative impacts on energetic processes. Studies have shown that during acute heat stress, mitochondrial function in the heart plays a crucial role in determining thermal tolerance, while the brain, being one of the most metabolically active and temperature-sensitive organs, faces an energetic crisis as temperatures rise.