Abstract
For most animals including fishes, temperature affects the rates of physiological processes (e.g., metabolic activities) and is therefore one of the most influential abiotic factors driving fish movement patterns. A select group of active, predatory, pelagic fishes make seasonal wide ranging latitudinal migrations across broad temperature ranges; but, for most species, rapid vertical (depth) movements to the colder waters beneath the thermocline are potentially restricted by the large (~∆18°C) gradient in ambient temperature that occurs from the surface waters to depth. When compared to most other active, pelagic fishes, bigeye thresher sharks (Alopias vulpinus) and swordfish (Xiphias gladius) are distinct in their ability to rapidly transit from the surface waters (≥20°C) to depths well below the thermocline (<8°C), where they remain to forage for prolonged periods of time (≥10 hours). Despite similar vertical movements, these two species exhibit marked differences in their phylogeny, body shape, and both the position and vasculature of the red muscle (RM) that powers sustained aerobic swimming. Similar to most fishes, the RM of bigeye thresher sharks is in a sub-cutaneous position and lacks any vascular heat-exchanging retia, which results in an RM temperature that approximates ambient temperature (i.e., ectothermy). By contrast, the RM of swordfish is located closer to the vertebrae and has associated vascular retia, which may enable the elevation of RM temperature relative to ambient (i.e., RM endothermy). These two different RM morphologies may result in varying rates of heat loss or heat gain during vertical movements. Such differential heat transfer rates may also cause the RM of these two species to operate under distinct thermal environments,which may ultimately impact RM performance and the capacity for sustained swimming.To date, there have been no studies to assess the biomechanical and biochemical performance of the RM in bigeye thresher sharks or swordfish during sustained swimming through disparate thermal habitats. Therefore, the main objectives of this research were to assess how these two species differ in their ability to physiologically control RM temperature, and how this may alter the contractile function and metabolic biochemical capacity of the swimming muscles. First, we provided a more detailed anatomical description of the muscular and cardiovascular systems of swordfish, as well as expanded previous thermodynamic analyses of RM temperature and ambient water temperature telemetry data obtained in free-swimming swordfish. Second, we investigated the impact of temperature on the mechanical work and power output of RM isolated from bigeye thresher sharks and swordfish. Lastly, we investigated the impact of temperature on the aerobic and anaerobic biochemical pathways of energy production,which are necessary to maintain contraction-relaxation cycles, in the swimming muscles.Our findings suggest that while RM morphology of swordfish does not allow for a constant, elevated RM temperature, there is some degree of physiological thermoregulation that maintains a relatively warm RM during prolonged exposure to cold. Briefly, modifications in blood flow patterns to and from the RM may allow the swordfish to slow the rate of RM cooling when diving below the thermocline and to expedite the rate of RM re-heating when returning to the surface. As in other fishes with RM endothermy, the slow rate of heat loss allows the RM of swordfish to operate at temperatures that are warmer than ambient during much of the dive cycle.This results in increased contractile performance and biochemical capacity that together enhance the contraction-relaxation cycling and power output of the RM. This capacity for physiological hermoregulation may allow swordfish to maintain a higher capacity for sustained swimming during prolonged exposure to cold, as compared to sympatric bigeye thresher sharks. However,unlike other fishes with RM endothermy, the RM of swordfish maintains contractile performance even after cooling to ambient temperature during prolonged dives.This body of research offers new insight into the effects of temperature on the biomechanical and biochemical rate processes that govern sustained swimming. In particular,low temperatures or large temperature gradients may limit the movement-patterns of active,predatory, pelagic fishes, permitting only some species, like bigeye thresher sharks and swordfish, to hunt in the colder waters at greater depths. Only by elucidating the physiological mechanisms by which fishes adjust to their surroundings, and not simply their presence or absence in a habitat, can we better understand how abiotic factors, like temperature, constrain or facilitate the movement-patterns of commercially important species in the face of globally warming ocean temperatures.