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 stimulation 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 swimming, we drove red muscle bundles under their in vivo conditions and measured the resulting power output. Although these in vivo conditions were near the 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 extremely low at 10 degrees C. Although at 30 cm s(-)(1), muscles from all regions of the fish generated positive work, at 40 and 50 cm s(-)(1), only the POST region (70 % total length) generated positive work, and that level was low. This 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 cause artificially reduced power measurements at 10 degrees C, we drove muscle bundles through a series of conditions in which the stimulation duration was shortened and other parameters were made closer to optimal. This sensitivity analysis revealed that the low power output could not be explained by realistic levels of systematic or random error. By integrating the muscle power output over the fish's mass and comparing it with power requirements for 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 and 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 length 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 more 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 performance from these isolated tissue experiments may lead to qualitatively incorrect conclusions. To make a meaningful assessment of the effects of temperature on muscle and locomotory performance, muscle performance must be studied under the conditions at which the muscle operates in vivo.
Rome
L C
LC
Department of Biology and Department of Physiology, University of Pennsylvania, Philadelphia, PA 19104, USA. lrome@mail.sas.upenn.edu
Swank
D M
DM
Coughlin
D J
DJ
D000818:Animals; D001696:Biomechanical Phenomena; D003080:Cold Temperature; D005399:Fishes / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology*; D013550:Swimming / Q000502:physiology*