The influence of thermal acclimation on power production during swimming II. Mechanics of scup red muscle under in vivo conditions

We have previously shown that the power output of red muscle from warm-accl imated scup is greatly reduced when the fish swim at low temperatures. This reduction occurs primarily because, despite the slowing of muscle relaxati on rate at cold temperatures, warm-acclimated scup swim with the same tail- beat frequency and the same stimulation durations, thereby not affording th e slower-relaxing muscle any extra time to relax. We hypothesize that power output during swimming could be increased if the stimulus duration were re duced or if the relaxation rate of the red muscle were increased during col d acclimation. Scup were acclimated to 10 degreesC (cold-acclimated) and 20 degreesC (warm -acclimated) for at least 6 weeks. Cold acclimation dramatically increased the ability of scup red muscle to produce power at 10 degreesC. Power outpu t measured from cold-acclimated muscle bundles driven through in vivo condi tions measured from cold-acclinated scup swimming at 10 degreesC (i.e. work loops) was generally much greater than that from warm-acclimated muscle dr iven through its respective in vivo conditions at 10 degreesC. The magnitud e of the increase depended both on the anatomical location of the muscle an d on swimming speed. Integrated over the length of the fish, the red muscul ature from cold-acclimated fish generated 2.7, 8.9 and 5.8 times more power than the red musculature from warm-acclimated fish while swimming at 30 cm s(-1), 40 cm s(-1) and 50cms(-1), respectively. Our analysis suggests that the cold-acclimated fish should be able to swim in excess of 40 cm s(-1) w ith just their red muscle whereas the warm-acclimated fish must recruit the ir pink muscle well below this speed. Because the red muscle is more aerobi c than the pink muscle, cold acclimation may increase the sustained swimmin g speed at which scup perform their long seasonal migrations at cool temper atures. We then explored the underlying mechanisms for the increase in muscle power output in cold-acclimated fish. Contrary to our expectations, cold-acclima ted muscle did not have a faster relaxation rate; instead, it had an approx imately 50 % faster activation rate. Our work-loop studies showed that this faster activation rate, alone, can increase the mechanical power productio n during cyclical contractions to a surprising extent. By driving cold-acclimated muscle through warm- and cold-acclimated in vivo conditions, we were able to partition the improvement in power production associated with increased activation rate and the approximately 20 % reduct ion in the duration of electromyographic activity found in the accompanying study. Depending on the position and swimming speed, approximately 60 % of the increase in power output was due to the change in the red muscle's con tractile properties (i.e. faster activation); the remainder was due to the shorter stimulus duty cycle of cold-acclimated scup. Thus, by both shortening the in vivo stimulation duration and speeding up t he rate of muscle activation as part of cold-acclimation, scup achieve a ve ry large increase in the power output of their red muscle during swimming a t low temperature. This increase in power output probably results in an inc rease in muscle efficiency and, hence, a reduction in the energetic cost of swimming. This increase in power output also reduces reliance on the less aerobic and less fatigue-resistant pink muscle. Both these abilities may in crease the swimming speed at which prolonged aerobic muscle activity can oc cur and thus reduce the travel time for the long seasonal migrations in whi ch scup engage.