The influence of temperature on power production during swimming II. Mechanics of red muscle fibres in vivo

We found previously that scup (Stenotomus chrysops) reduce neither their st imulation duration nor their tail-beat frequency to compensate for the slow relaxation rates of their muscles at low swimming temperatures. To assess the impact of this 'lack of compensation' on power generation during swimmi ng, we drove red muscle bundles under their in vivo conditions and measured the resulting power output. Although these in vivo conditions were near th e optimal conditions for much of the muscle at 20 degrees C, they were far from optimal at 10 degrees C, Accordingly, in vivo power output was extreme ly low at 10 degrees C. Although at 30 cm s(-1), muscles from all regions o f the fish generated positive work, at 40 and 50 cm s(-1), only the POST re gion (70 % total length) generated positive work, and that level was low. T his led to a Q(10) of 4-14 in the POST region (depending on swimming speed) , and extremely high or indeterminate Q(10) values (if power at 10 degrees C is zero or negative, Q(10) is indeterminate) for the other regions while swimming at 40 or 50 cm s(-1). To assess whether errors in measurement of the in vivo conditions could cau se artificially reduced power measurements at 10 degrees C, we drove muscle bundles through a series of conditions in which the stimulation duration w as shortened and other parameters were made closer to optimal. This sensiti vity analysis revealed that the low power output could not be explained by realistic levels of systematic or random error. By integrating the muscle p ower output over the fish's mass and comparing it with power requirements f or swimming, we conclude that, although the fish could swim at 30 cm s(-1) with the red muscle alone, it is very unlikely that it could do so at 40 an d 50 cm s(-1), thus raising the question of how the fish powers swimming at these speeds. By integrating in vivo pink muscle power output along the le ngth of the fish, we obtained the surprising finding that, at 50 cm s(-1), the pink muscle (despite having one-third the mass) contributes six times m ore power to swimming than does the red muscle. Thus, in scup, pink muscle is crucial for powering swimming at low temperatures. This overall analysis shows that Q(10) values determined in experiments on isolated tissue under arbitrarily selected conditions can be very different from Q(10) values in vivo, and therefore that predicting whole-animal perf ormance from these isolated tissue experiments may lead to qualitatively in correct conclusions. To make a meaningful assessment of the effects of temp erature on muscle and locomotory performance, muscle performance must be st udied under the conditions at which the muscle operates in vivo.