Behavioural thermoregulation linked to foraging in blue sharks.

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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00227-021-03971-3.

Behavioural response of a whale shark during the passage of a typhoon.

During a behavioural survey of a tagged whale shark (Rhincodon typus) conducted in 2019 in the waters off Kagoshima, Japan, a typhoon passed close to the area under surveillance. As the typhoon approached, monitoring of the shark's movements indicated that it dived to depths of up to 90 m, and during this period, the authors recorded the effects of the typhoon-induced waves. They also detected changes in the vertical thermal structure of the waters, possibly due to the disturbance caused by the typhoon.

Similar circling movements observed across marine megafauna taxa.

Advances in biologging technology have enabled 3D dead-reckoning reconstruction of marine animal movements at spatiotemporal scales of meters and seconds. Examining high-resolution 3D movements of sharks (Galeocerdo cuvier, N = 4; Rhincodon typus, N = 1), sea turtles (Chelonia mydas, N = 3), penguins (Aptenodytes patagonicus, N = 6), and marine mammals (Arctocephalus gazella, N = 4; Ziphius cavirostris, N = 1), we report the discovery of circling events where animals consecutively circled more than twice at relatively constant angular speeds. Similar circling behaviors were observed across a wide variety of marine megafauna, suggesting these behaviors might serve several similar purposes across taxa including foraging, social interactions, and navigation.

Body temperature stability in the whale shark, the world's largest fish.

It is generally assumed that the body temperature of large animals is less likely to change because of 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 temperature. The muscle temperature changed substantially more slowly than the water temperature fluctuations associated with vertical movements, and the whole-body heat-transfer coefficients (HTCs) 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 comparative analysis showed that the HTC at cooling in various fish species including both ectothermic and endothermic species ranging from 10-4 to 103 kg was proportional to body mass-0.63 This allometry was present regardless of whether the fish were ectothermic or endothermic, and was an extension of the relationship observed in previous studies on small fish. Thus, large fish have the advantage of body temperature stability while moving in environments with large temperature variations. Our results suggest that the large body size of whale sharks aids in preventing a decrease in body temperature during deep excursions to more than 1000 m depths without high metabolic costs of producing heat.

Body temperature stability observed in the whale sharks, the world's largest fish.

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 comparative analysis showed that the HTC at cooling in various fish species including both ectothermic and endothermic species ranging from 10-4 to 103 kg was proportional to body mass-0.63. This allometry was present regardless of whether the fish were ectothermic or endothermic, and was an extension of the relationship observed in previous studies on small fish. Thus, large fish have the advantage of body temperature stability while moving in environments with large temperature variations. Our results suggest that the large body size of whale sharks aids in preventing a decrease in body temperature during deep excursions to more than 1000 m depths without high metabolic costs of producing heat.

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator.

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Unexpected Positive Buoyancy in Deep Sea Sharks, Hexanchus griseus, and a Echinorhinus cookei.

We do not expect non air-breathing aquatic animals to exhibit positive buoyancy. Sharks, for example, rely on oil-filled livers instead of gas-filled swim bladders to increase their buoyancy, but are nonetheless ubiquitously regarded as either negatively or neutrally buoyant. Deep-sea sharks have particularly large, oil-filled livers, and are believed to be neutrally buoyant in their natural habitat, but this has never been confirmed. To empirically determine the buoyancy status of two species of deep-sea sharks (bluntnose sixgill sharks, Hexanchus griseus, and a prickly shark, Echinorhinus cookei) in their natural habitat, we used accelerometer-magnetometer data loggers to measure their swimming performance. Both species of deep-sea sharks showed similar diel vertical migrations: they swam at depths of 200-300 m at night and deeper than 500 m during the day. Ambient water temperature was around 15°C at 200-300 m but below 7°C at depths greater than 500 m. During vertical movements, all deep-sea sharks showed higher swimming efforts during descent than ascent to maintain a given swimming speed, and were able to glide uphill for extended periods (several minutes), indicating that these deep-sea sharks are in fact positively buoyant in their natural habitats. This positive buoyancy may adaptive for stealthy hunting (i.e. upward gliding to surprise prey from underneath) or may facilitate evening upward migrations when muscle temperatures are coolest, and swimming most sluggish, after spending the day in deep, cold water. Positive buoyancy could potentially be widespread in fish conducting daily vertical migration in deep-sea habitats.

Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores.

Ocean sunfish (Mola mola) were believed to be inactive jellyfish feeders because they are often observed lying motionless at the sea surface. Recent tracking studies revealed that they are actually deep divers, but there has been no evidence of foraging in deep water. Furthermore, the surfacing behaviour of ocean sunfish was thought to be related to behavioural thermoregulation, but there was no record of sunfish body temperature. Evidence of ocean sunfish feeding in deep water was obtained using a combination of an animal-borne accelerometer and camera with a light source. Siphonophores were the most abundant prey items captured by ocean sunfish and were typically located at a depth of 50-200 m where the water temperature was <12 °C. Ocean sunfish were diurnally active, made frequently deep excursions and foraged mainly at 100-200 m depths during the day. Ocean sunfish body temperatures were measured under natural conditions. The body temperatures decreased during deep excursions and recovered during subsequent surfacing periods. Heat-budget models indicated that the whole-body heat-transfer coefficient between sunfish and the surrounding water during warming was 3-7 times greater than that during cooling. These results suggest that the main function of surfacing is the recovery of body temperature, and the fish might be able to increase heat gain from the warm surface water by physiological regulation. The thermal environment of ocean sunfish foraging depths was lower than their thermal preference (c. 16-17 °C). The behavioural and physiological thermoregulation enables the fish to increase foraging time in deep, cold water. Feeding rate during deep excursions was not related to duration or depth of the deep excursions. Cycles of deep foraging and surface warming were explained by a foraging strategy, to maximize foraging time with maintaining body temperature by vertical temperature environment.