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

Fish Physiology and Biochemistry, 2020

A l o p i a s superciliosus) and swordfish (Xiphias gladius) are large, pelagic fishes, which make long-duration, diurnal foraging dives from warm, surface waters (18-24°C) to cold waters beneath the thermocline (5-10°C). In bigeye thresher sharks, the subcutaneous position of the red, aerobic swimming muscles (RM) suggests that RM temperature mirrors ambient during dives (i.e., ectothermy). In swordfish, the RM is closer to the vertebrae and its associated with vascular counter-current heat exchangers that maintain RM temperature above ambient (i.e., RM endothermy). Here, we sought to determine how exposure to a wide range of ambient temperatures (8, 16, 24°C) impacted peak power output and optimum cycle (i.e., tailbeat) frequency (0.25, 0.5, 1 Hz) in RM isolated from both species. Bigeye thresher shark RM did not produce substantial power at high cycle frequencies, even at high temperatures; but it did produce relatively high power at slow cycle frequencies regardless of temperature. Swordfish RM produced more power when operating at a combination of fast cycle frequencies and higher temperatures. This suggests that swordfish RM benefits considerably more from warming than bigeye thresher shark RM, while the RM of both species was able to produce power at cold temperatures and slow cycle frequencies. Despite different thermal strategies (i.e., ectothermy vs. RM endothermy), the ability of the RM to power sustained swimming during foraging-related search behaviors may contribute to the unique ability of these fishes to successfully exploit food resources in deep, cold water.

Journal of Experimental Biology, 2020

It is generally assumed that the body temperature of large animals is less likely to change due to their large body size, resulting in a high thermal inertia and a smaller surface area to volume ratio. The goal of this study was to investigate the stability of body temperature in large fish using data from field experiments. We measured the muscle temperatures of free-ranging whale sharks (Rhincodon typus), the largest extant fish globally, and investigated their ectothermic physiology and the stability of their body temperatures. The measured muscle temperature of the whale sharks changed substantially more slowly than the water temperature fluctuations associated with vertical movements, and the whole-body heat-transfer coefficients (HTC) of whale sharks estimated using heat-budget models were lower than those of any other fish species measured to date. The heat-budget models also showed that internal heat production does not contribute to changes in muscle temperature. A comparat...

The Journal of experimental biology, 2001

The mako shark (Isurus oxyrinchus) has specialized vascular networks (retia mirabilia) forming counter-current heat exchangers that allow metabolic heat retention in certain regions of the body, including the aerobic, locomotor red muscle and the viscera. Red muscle, white muscle and stomach temperatures were measured in juvenile (5-13.6 kg) makos swimming steadily in a water tunnel and exposed to stepwise square-wave changes in ambient temperature (T(a)) to estimate the rates of heat transfer and to determine their capacity for the activity-independent control of heat balance. The rates of heat gain of red muscle during warming were significantly higher than the rates of heat loss during cooling, and neither the magnitude of the change in T(a) nor the direction of change in T(a) had a significant effect on red muscle latency time. Our findings for mako red muscle are similar to those recorded for tunas and suggest modulation of retial heat-exchange efficiency as the underlying mech...

Journal of Comparative Physiology B-biochemical Systemic and Environmental Physiology - J COMP PHYSIOL B, 1997

Stomach temperatures of three white sharks, Carcharodoncarcharias, (one reported previously and two new individuals) were intermittently recorded by acoustic telemetry at the South Farallon Islands, central California. Temperature profiles of the water column were obtained concurrently. Stomach temperatures were elevated over ambient water temperatures by as much as 14.3 °C. Stomach temperatures varied within a narrow range while ambient water temperature fluctuated over a much larger range, showing that this species regulates its body temperature. These data, in combination with previous work on the physiology and anatomy of white sharks, indicate that the white shark is endothermic. It appears that the heat retention system in lamnid sharks has allowed them to inhabit cold water and remain active predators of swift and agile prey.

Environmental Biology of Fishes, 2004

Salmon sharks, Lamna ditropis, belong to a small group of sharks that possess vascular counter-current heat exchangers (retia mirabilia) allowing retention of metabolically generated heat, resulting in elevated body temperatures. The capacity of free-swimming lamnid sharks to regulate rates of heat gain and loss has not been demonstrated. Using acoustic telemetry, we recorded swimming depth and stomach temperature from four free-swimming salmon sharks in Prince William Sound, Alaska. Temperature data were obtained over time periods ranging from 3.8 to 20.7 h. Temperature profiles of the water column were obtained concurrently for use as estimates of ambient temperature. Mean stomach temperature among four individuals tracked ranged from 25.0 to 25.7°C. These sharks defended specific elevated temperatures regardless of changes in ambient temperature, which ranged from about 5-16°C. The maximum observed elevation of stomach temperature over ambient was 21.2°C. Because stomach temperatures were so strictly maintained relative to changes in ambient temperature, a thermal rate coefficient, k, (°C min )1°C thermal gradient )1 ) for cooling of 0.053 min )1 was obtained via a 'control' experiment with a dead salmon shark. We show that free-swimming adult salmon sharks maintain a specific stomach temperature independent of changes in ambient temperature through a combination of physical and physiological means, and essentially function as homeotherms. This unique ability is probably the underlying factor in the evolutionary niche expansion of salmon sharks into boreal waters and in their ability to actively pursue and capture highly active prey such as salmon.

Copeia, 2005

This paper reports on the in vivo temperature measurements for slow-twitch, red aerobic muscle (RM) and fast twitch, white muscle (WM) of 24 Common Thresher Sharks, Alopias vulpinus, captured off the coast of Southern California. Mean (؎ SE) RM temperature elevation was 2.33 ؎ 0.30 C warmer than the ambient sea surface temperature (SST, 19.13 ؎ 0.22 C) and 2.25 ؎ 0.35 C warmer than the coldest WM temperature measured (19.23 ؎ 0.30 C). The maximum RM temperature elevation was 5.4 C above SST and up to 7.6 C above the WM. Nine Common Thresher Sharks exhibited RM temperatures that exceeded 3.0 C above SST. No significant relationship was found between fish total length and RM temperature elevation. Although there was individual variability in RM temperature elevation, this study documents that the Common Thresher Shark is capable of significantly elevating its RM temperature above that of the ambient conditions.

Science, 2015

Endothermy (the metabolic production and retention of heat to warm body temperature above ambient) enhances physiological function, and whole-body endothermy generally sets mammals and birds apart from other animals. Here, we describe a whole-body form of endothermy in a fish, the opah (Lampris guttatus), that produces heat through the constant "flapping" of wing-like pectoral fins and minimizes heat loss through a series of counter-current heat exchangers within its gills. Unlike other fish, opah distribute warmed blood throughout the body, including to the heart, enhancing physiological performance and buffering internal organ function while foraging in the cold, nutrient-rich waters below the ocean thermocline.

Marine Biology

Large pelagic fishes often dive and surface repeatedly as if they were airbreathers, raising a question about the functions of these movements. Some species (e.g., bigeye tuna, ocean sunfish) apparently alternate foraging in deep cold waters and rewarming in shallow warm waters. However, it is unclear how prevalent this pattern is among species. Blue sharks are the widest-ranging pelagic shark with expanded vertical niches, providing a model for studying foraging-thermoregulation associations. We used electronic tags, including video cameras, to record the diving behaviour, muscle temperature, and foraging events of two blue sharks. During repeated deep dives (max. 422 m), muscle temperature changed more slowly than ambient water temperature. Sharks shifted between descents and ascents before muscle temperature reached ambient temperature, leading to a narrower range (8 °C) of muscle temperature than ambient temperature (20 °C). 2.5-h video footage showed a shark catching a squid, during which a burst swimming event was recorded. Similar swimming events, detected from the entire tag data (20 − 22 h), occurred over a wide depth range (5 − 293 m). We conclude that, instead of alternating foraging and rewarming, blue sharks at our study site forage and thermoregulate continuously in the water column. Furthermore, our comparative analyses showed that the heat exchange rates of blue sharks during the warming and cooling process were not exceptional among fishes for their body size. Thus, behavioural thermoregulation linked to foraging, rather than enhanced abilities to control heat exchange rates, is likely key to the expanded thermal niches of this ectothermic species.

Canadian Journal of Zoology-revue Canadienne De Zoologie, 1988

in fish: conservative and labile properties of swimming muscle. Can. J. Zool. 66: 1105Zool. 66: -1115. Given the rapid thermal equilibration of most fish with their environment, thermal compensation of metabolic and contractile properties is essential for the maintenance of locomotory capacities over a wide range of temperatures. The response of fish swimming performance, contractile properties of isolated fibers, myosin ATPase activity, and metabolic systems for ATP generation to short-and long-term changes in temperature have received sufficient study to allow one to identify certain constrained and labile properties. Sustained swimming performance and its components generally have their optimal performance and lowest thermal sensitivity within the range of temperatures frequently encountered by the organism. These principles are particularly well established for isolated enzyme systems. Furthermore, swimming performance and most of its components demonstrate thermal compensation on the evolutionary time scale. Temperature acclimation also leads to compensatory responses which, while quite species-specific, consistently increase the capacity for sustained swimming at low temperatures. The position of the thermal optimum for locomotion in relation to the width of a species' tolerance limits aids in predicting the species' capacity for thermal compensation during acclimation. Goldfish (Carassius auratus) and common carp (Cyprinus capio), which tolerate temperatures 25 -30°C below their optimum for locomotion, show thermal compensation in terms of contractile properties, myosin ATPase activity, the proportion of red fibers in their axial musculature, and the levels of aerobic enzymes in their musculature. By contrast, striped bass (Morone saxatilis) and chain pickerel (Esox niger), which have lower optimal temperatures for locomotion, only increase the proportion of red fibers and (or) the levels of aerobic enzymes with cold acclimation. Finally, lake whitefish (Coregonus clupeaformis), which have their optimal temperature for locomotion at 12"C, show none of these responses. Given that when thermal compensation occurs, aerobic enzymes in red muscle generally increase, the capacity of red muscle to generate ATP seems more temperature sensitive than other metabolic or contractile properties. Whether this compensatory response serves to counteract the effect of temperature on diffusive exchange between mitochondria and the cytoplasm or its effect on the catalytic capacity of aerobic metabolism remains to be established. GUDERLEY, H., et BLIER, P. 1988. Thermal acclimation in fish: conservative and labile properties of swimming muscle.

Journal of The Royal Society Interface, 2012