Elevating body temperature above ambient using metabolic heat is the norm among birds and mammals, but among fishes it is the exception. Two fish groups that buck the trend are tunas and lamnid sharks, and they do so using remarkably convergent adaptations for minimizing heat loss. One such adaptation for reducing heat loss across the skin is internalized oxidative swimming muscle. Most fishes swim using slow-twitch (or `red') muscle located just under the skin, but tunas and lamnids have red muscle that is much closer to their body core. One advantage of burying red muscle deep within the body is that this high metabolic rate tissue is then insulated by the large mass of fast-twitch (`white') muscle surrounding it. The consequence of this arrangement is a steep thermal gradient, from warm red muscle at the core to relatively cold white muscle just under the skin. Bernal and colleagues were interested in the consequences of this thermal gradient on muscle function in salmon sharks, a lamnid that inhabits icy Arctic waters and is believed to maintain some of the highest thermal gradients among endothermic fishes.
To measure the magnitude of the thermal gradient in salmon sharks' muscles,the investigators caught three salmon sharks in the Gulf of Alaska. They found that, at its warmest, salmon sharks' deep red muscle can be 26°C, which is about 20°C higher than ambient. The white muscle under the skin was typically only a few degrees higher than ambient, whereas the deepest white muscle was almost as warm as the red muscle. These measurements confirmed that salmon shark white muscle exhibits a dramatic thermal gradient.
The investigators also measured the effects of temperature on muscle contractile properties in live salmon sharks using a portable stimulator/transducer. They found similar twitch durations in superficial white muscle all along the body, but significantly faster twitches in deeper(warmer) white muscle. When they stimulated isolated muscle fibre bundles in vitro over a range of temperatures, they found that salmon sharks'red muscle was remarkably sensitive to temperature, with twitch speed decreasing by a factor of 3.7 for a 10°C drop in temperature. By contrast,nearby white muscle was not nearly as sensitive to temperature, decreasing only 2-fold for a 10°C drop. The investigators also measured muscle power as a function of temperature and showed that white muscle can operate well over a wide range of temperatures, but red muscle simply can't.
The authors point out that the high thermal sensitivity of red muscle underscores the fact that these animals are obligate ram ventilators; they have to swim continuously in order to keep breathing. If a salmon shark were to stop swimming, its red muscle would stop generating heat and eventually would cool. Even a small drop in red muscle temperature could compromise its function enough to send it into a downward spiral from which the animal couldn't recover. When framed this way, it seems unfortunate for salmon sharks that they are saddled with such sensitive red muscle in such a challenging thermal environment. But the other side of the coin is that salmon shark red muscle likely achieves higher power outputs when warm than it could if it were less temperature sensitive. Furthermore, salmon sharks probably exert tight control over the temperature of their red muscle, which allows them to reap the benefits and avoid the pitfalls of having red muscle more typical of a mammal than a fish.
