Mammal-like muscles power swimming in a cold-water shark

Abstract

Effects of temperature on muscle contraction and powering movement are profound, outwardly obvious, and of great consequence to survival. To cope with the effects of environmental temperature fluctuations, endothermic birds and mammals maintain a relatively warm and constant body temperature, whereas most fishes and other vertebrates are ectothermic and conform to their thermal niche, compromising performance at colder temperatures. However, within the fishes the tunas and lamnid sharks deviate from the ectothermic strategy, maintaining elevated core body temperatures that presumably confer physiological advantages for their roles as fast and continuously swimming pelagic predators. Here we show that the salmon shark, a lamnid inhabiting cold, north Pacific waters, has become so specialized for endothermy that its red, aerobic, locomotor muscles, which power continuous swimming, seem mammal-like, functioning only within a markedly elevated temperature range (20-30 degrees C). These muscles are ineffectual if exposed to the cool water temperatures, and when warmed even 10 degrees C above ambient they still produce only 25-50% of the power produced at 26 degrees C. In contrast, the white muscles, powering burst swimming, do not show such a marked thermal dependence and work well across a wide range of temperatures.

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

“…We suggest that this advantage, coupled with the previously recognized benefit of thermal niche expansion, could outweigh high energetic costs incurred by RM endothermy and, thus, has facilitated the radiation and diversification of tunas and endothermic sharks. Our analyses also indicate that fishes with RM endothermy are similar to birds and mammals in many respects, including not only high metabolic rates (2) and temperature dependence of muscle function (37), but also fast cruising speeds and the capabilities of large-scale migrations.…”

In cold blood: evidence of Pacific sleeper shark (Somniosus pacificus) predation on Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska

“…All 3 species have been documented feeding within Alaskan waters and the Bering Sea (Compagno, 1984;Benz et al, 2004;Martin, 2005). However, lamnid sharks, including the salmon shark (Smith and Rhodes, 1983;Anderson and Goldman, 2001;Goldman et al, 2004;Bernal et al, 2005) and the white shark (McCosker, 1987;Goldman, 1997), have been shown to maintain body-core and stomach temperatures consistently 6-15°C above ambient temperatures even in subarctic regions with SSTs below 5°C. Therefore, the Pacific sleeper shark emerges as the only potential predator of Steller sea lions in the North Pacific and Bering Sea region whose body-core temperatures likely remain at mid-water values.…”

Temperature effects on metabolic rate of juvenile Pacific bluefin tunaThunnus orientalis

“…Optimum frequency and power output of yellowfin tuna slow-twitch muscle are temperature dependent (Altringham and Block, 1997) and slowtwitch muscle from the endothermic salmon shark is unable to produce positive work at low temperatures (Bernal et al, 2005), raising the possibility that bluefin tuna slow-twitch muscle would be similarly impaired at cold temperatures. The decline in optimum contraction frequency at low temperature in vitro indicates that cold muscle should be least effective at high swimming speeds (Altringham and Block, 1997).…”