Enhanced thermoregulation abilities of shortfin mako sharks as the key adaptive significance of regional endothermy in fishes.

Abstract

Some large, wide-ranging teleosts and elasmobranchs are converged to have regional endothermy, retaining metabolic heat via vascular countercurrent heat exchangers. Yet, their adaptive significance remains debated. While previous studies proposed potential benefits of elevated body temperature, enhanced controllability of body temperature enabled by heat exchangers may also be important. Some endothermic teleosts (e.g. bigeye tuna) alter rates of body temperature change depending on dive phases to maximize foraging time in deep, cold waters while minimizing recovery time in shallow, warm waters. However, whether endothermic elasmobranchs possess similar abilities remains unclear. Using animal-borne tags, we recorded diving behaviours and muscle temperatures of shortfin mako sharks, a possible elasmobranch equivalent to bigeye tuna. Warming and cooling rates were estimated with a heat exchange model. Further, we conducted literature-based, phylogenetically informed comparative analyses of heat exchange rates across 25 fish species (mass range, 0.01-1600 kg). All four mako sharks repeatedly dived below the thermocline with ambient temperature changes of up to 7-14°C. On average, muscle temperatures were 1.5-3.9°C warmer than the ambient water. Two individuals dived deep (up to 286-327 m) and showed a 14-47 times higher warming rate than cooling rate, whereas the other two individuals that dived shallowly exhibited one to two times differences. One individual warmed its muscle above sea surface temperature before a deep dive, possibly preparing for the coming deep excursion using internal heat sources. Comparative analyses showed that the ratio of warming to cooling rate and its range across individuals was larger in endothermic bigeye tuna, swordfish and mako sharks than in most other fishes. Our results demonstrate that enhanced temperature controllability has convergently evolved among some endothermic teleosts and elasmobranchs that inhabit low-to-middle latitude waters with strong thermal gradients. By contrast, some other endothermic species (e.g. salmon sharks and Atlantic bluefin tuna) that migrate to subpolar waters are specialized for body temperature elevation. We propose that the controllability and elevation of body temperature have different adaptive significance, reflecting species' habitats and foraging ecology. Our findings help explain the diversity and success of endothermic fishes as apex predators across the world's pelagic oceans.