Thermal sensitivity of metabolic rate mirrors biogeographic differences between teleosts and elasmobranchs.

Environmental temperature affects physiological functions, representing a barrier for the range expansions of ectothermic species. To understand the link between thermal physiology and biogeography, a key question is whether among-species thermal sensitivity of metabolic rates is mechanistically constrained or buffered through physiological remodeling over evolutionary time. The former conception, the Universal Temperature Dependence hypothesis, predicts similar among- and within-species thermal sensitivity. The latter conception, the Metabolic Cold Adaptation hypothesis, predicts lower among-species thermal sensitivity than within-species sensitivity. Previous studies that tested these hypotheses for fishes overwhelmingly investigated teleosts with elasmobranchs understudied. Here, we show that among-species thermal sensitivity of resting metabolic rates is lower than within-species sensitivity in teleosts but not in elasmobranchs. Further, species richness declines with latitude more rapidly in elasmobranchs than in teleosts. Metabolic Cold Adaptation exhibited by teleosts might underpin their high diversity at high latitudes, whereas the inflexible thermal sensitivity approximated by Universal Temperature Dependence of elasmobranchs might explain their low diversity at high latitudes.

Biologging and Biotelemetry: Tools for Understanding the Lives and Environments of Marine Animals.

Addressing important questions in animal ecology, physiology, and environmental science often requires in situ information from wild animals. This difficulty is being overcome by biologging and biotelemetry, or the use of miniaturized animal-borne sensors. Although early studies recorded only simple parameters of animal movement, advanced devices and analytical methods can now provide rich information on individual and group behavior, internal states, and the surrounding environment of free-ranging animals, especially those in marine systems. We summarize the history of technologies used to track marine animals. We then identify seven major research categories of marine biologging and biotelemetry and explain significant achievements, as well as future opportunities. Big data approaches via international collaborations will be key to tackling global environmental issues (e.g., climate change impacts), and curiosity about the secret lives of marine animals will also remain a major driver of biologging and biotelemetry studies.

Factors affecting gestation periods in elasmobranch fishes.

Gestation periods vary greatly across elasmobranch species. Differences in body size and body temperature (i.e. major determinants of metabolic rates) might explain such variation. Although temperature effects have been demonstrated for captive animals, body size effects remain undocumented. Moreover, whether metabolic rates of mothers or those of embryos affect gestation periods remains unclear. Because biological times generally scale with mass1-ß, where ß is metabolic scaling exponent (0.8-0.9 in fishes), we hypothesized that elasmobranch gestation periods would scale with mass0.1-0.2. We also hypothesized that regionally endothermic species with elevated metabolic rates should have shorter gestation periods than similar-sized ectothermic species if the metabolic rates of mothers are responsible. We compiled data on gestation periods for 36 elasmobranch species to show that gestation periods scale with M0.11 and m0.17, where M and m are adult female mass and birth mass, respectively. Litter size and body temperature also affected gestation periods. Our findings suggest that the body-mass dependence of metabolic rate explains some variations in elasmobranch gestation periods. Unexpectedly, regionally endothermic sharks did not have shorter gestation periods than their ectothermic counterparts, suggesting that the metabolic rates of embryos, which are likely ectothermic in all elasmobranch species, may be responsible. This article has an associated First Person interview with the first author of the paper.

Accelerometer-based analyses of animal sleep patterns.

Body-motion sensors can be used to study non-invasively how animals sleep in the wild, opening up exciting opportunities for comparative analyses across species.

Life in the slow lane: field metabolic rate and prey consumption rate of the Greenland shark (Somniosus microcephalus) modelled using archival biologgers.

Field metabolic rate (FMR) is a holistic measure of metabolism representing the routine energy utilization of a species living within a specific ecological context, thus providing insight into its ecology, fitness and resilience to environmental stressors. For animals that cannot be easily observed in the wild, FMR can also be used in concert with dietary data to quantitatively assess their role as consumers, improving understanding of the trophic linkages that structure food webs and allowing for informed management decisions. Here, we modelled the FMR of Greenland sharks (Somniosus microcephalus) equipped with biologger packages or pop-up archival satellite tags (PSATs) in two coastal inlets of Baffin Island (Nunavut) using metabolic scaling relationships for mass, temperature and activity. We estimated that Greenland sharks had an overall mean (±s.d.) FMR of 21.67±2.30 mg O2 h-1 kg-0.84 (n=30; 1-4 day accelerometer package deployments) while residing inside these cold-water fjord systems in the late summer, and 25.48±0.47 mg O2 h-1 kg-0.84 (n=6; PSATs) over an entire year. When considering prey consumption rate, an average shark in these systems (224 kg) requires a maintenance ration of 61-193 g of fish or marine mammal prey daily. As Greenland sharks are a lethargic polar species, these low FMR estimates, and corresponding prey consumption estimates, suggest they require very little energy to sustain themselves under natural conditions. These data provide the first characterization of the energetics and consumer role of this vulnerable and understudied species in the wild, which is essential given growing pressures from climate change and expanding commercial fisheries in the Arctic.

Water column structure influences long-distance latitudinal migration patterns and habitat use of bumphead sunfish Mola alexandrini in the Pacific Ocean.

Satellite-tracking of adult bumphead sunfish, Mola alexandrini, revealed long-distance latitudinal migration patterns covering thousands of kilometers. Horizontal and vertical movements of four bumphead sunfish off Taiwan were recorded with pop-up satellite archival tags in 2019-2020. Two individuals moved northward and traveled to Okinawa Island and Kyushu, Japan and two moved southwards; crossing the equator, to Papua New Guinea and New Caledonia. During daytime, bumphead sunfish descended below the thermocline and ascended to mixed layer depths (MLD) during nighttime. The N-S migrants, however, demonstrated different habitat utilization patterns. Instead of using prevailing currents, the northward movements of sunfish cohorts exhibited extensive use of mesoscale eddies. Fish in anticyclonic eddies usually occupied deeper habitats whereas those in cyclonic eddies used near-surface habitats. On northward excursions, fish spent most of their time in regions with high dissolved oxygen concentrations. Southward movement patterns were associated with major currents and thermal stratification of the water column. In highly stratified regions, fish stayed below the thermocline and frequently ascended to MLD during daytime either to warm muscles or repay oxygen debts. These results for bumphead sunfish present important insights into different habitat use patterns and the ability to undergo long-distance migrations over varying spatial-temporal scales and features.

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.

Too big to study? The biologging approach to understanding the behavioural energetics of ocean giants.

Wild animals are under selective pressure to optimise energy budgets; therefore, quantifying energy expenditure, intake and allocation to specific activities is important if we are to understand how animals survive in their environment. One approach toward estimating energy budgets has involved measuring oxygen consumption rates under controlled conditions and constructing allometric relationships across species. However, studying 'giant' marine vertebrates (e.g. pelagic sharks, whales) in this way is logistically difficult or impossible. An alternative approach involves the use of increasingly sophisticated electronic tags that have allowed recordings of behaviour, internal states and the surrounding environment of marine animals. This Review outlines how we could study the energy expenditure and intake of free-living ocean giants using this 'biologging' technology. There are kinematic, physiological and theoretical approaches for estimating energy expenditure, each of which has merits and limitations. Importantly, tag-derived energy proxies can hardly be validated against oxygen consumption rates for giant species. The proxies are thus qualitative, rather than quantitative, estimates of energy expenditure, and have more limited utilities. Despite this limitation, these proxies allow us to study the energetics of ocean giants in their behavioural context, providing insight into how these animals optimise their energy budgets under natural conditions. We also outline how information on energy intake and foraging behaviour can be gained from tag data. These methods are becoming increasingly important owing to the natural and anthropogenic environmental changes faced by ocean giants that can alter their energy budgets, fitness and, ultimately, population sizes.

Ultrahigh foraging rates of Baikal seals make tiny endemic amphipods profitable in Lake Baikal.

Understanding what, how, and how often apex predators hunt is important due to their disproportionately large effects on ecosystems. In Lake Baikal with rich endemic fauna, Baikal seals appear to eat, in addition to fishes, a tiny (<0.1 g) endemic amphipod Macrohectopus branickii (the world's only freshwater planktonic species). Yet, its importance as prey to seals is unclear. Globally, amphipods are rarely targeted by single-prey feeding (i.e., nonfilter-feeding) mammals, presumably due to their small size. If M. branickii is energetically important prey, Baikal seals would exhibit exceptionally high foraging rates, potentially with behavioral and morphological specializations. Here, we used animal-borne accelerometers and video cameras to record Baikal seal foraging behavior. Unlike the prevailing view that they predominantly eat fishes, they also hunted M. branickii at the highest rates (mean, 57 individuals per dive) ever recorded for single-prey feeding aquatic mammals, leading to thousands of catches per day. These rates were achieved by gradual changes in dive depth following the diel vertical migration of M. branickii swarms. Examining museum specimens revealed that Baikal seals have the most specialized comb-like postcanine teeth in the subfamily Phocinae, allowing them to expel water while retaining prey during high-speed foraging. Our findings show unique mammal-amphipod interactions in an ancient lake, demonstrating that organisms even smaller than krill can be important prey for single-prey feeding aquatic mammals if the environment and predators' adaptations allow high foraging rates. Further, our finding that Baikal seals directly eat macroplankton may explain why they are so abundant in this ultraoligotrophic lake.

A first look at the metabolic rate of Greenland sharks (Somniosus microcephalus) in the Canadian Arctic.

Metabolic rate is intricately linked to the ecology of organisms and can provide a framework to study the behaviour, life history, population dynamics, and trophic impact of a species. Acquiring measures of metabolic rate, however, has proven difficult for large water-breathing animals such as sharks, greatly limiting our understanding of the energetic lives of these highly threatened and ecologically important fish. Here, we provide the first estimates of resting and active routine metabolic rate for the longest lived vertebrate, the Greenland shark (Somniosus microcephalus). Estimates were acquired through field respirometry conducted on relatively large-bodied sharks (33-126 kg), including the largest individual shark studied via respirometry. We show that despite recording very low whole-animal resting metabolic rates for this species, estimates are within the confidence intervals predicted by derived interspecies allometric and temperature scaling relationships, suggesting this species may not be unique among sharks in this respect. Additionally, our results do not support the theory of metabolic cold adaptation which assumes that polar species maintain elevated metabolic rates to cope with the challenges of life at extreme cold temperatures.

Foraging behavior links sea ice to breeding success in Antarctic penguins.

Population trends and breeding success variability of Adélie penguins, a bioindicator of Antarctic environments, have been attributed to changing sea-ice extents; however, causative mechanisms remain unclear. By electronically tagging 175 penguins in four seasons with contrasting sea-ice conditions, we show that ice-free environments enhance, not deteriorate, foraging efficiencies and breeding success. In an ice-free season, penguins traveled by swimming rather than walking, leading to larger foraging areas, shorter trip durations, and lower energy expenditure than three ice-covered seasons. Freed from the need to find cracks for breathing, dive durations decreased, and more krill were captured per unit dive time, which may also be associated with phytoplankton blooms and increased krill density in the sunlit ice-free water. Consequently, adult body mass, chick growth rates, and breeding success increased. Our findings explain the regional population trends and demonstrate a key link among sea ice, foraging behavior, and reproductive success in this iconic species.

A framework to estimate the likelihood of species interactions and behavioural responses using animal-borne acoustic telemetry transceivers and accelerometers.

Interactions between animals structure food webs and regulate ecosystem function and productivity. Quantifying subsurface behavioural interactions among marine organisms is challenging, but technological advances are promoting novel opportunities. Here, we present a framework to estimate when there is a high likelihood that aquatic animal subsurface interactions occur and test for a movement-related behavioural response to those interactions over short temporal scales (days) using a novel multi-sensor biologging package on a large marine predator, the Greenland shark (Somniosus microcephalus). We deployed a recoverable biologging package combining a VEMCO Mobile Transceiver (VMT), accelerometer and a temperature-depth tag to quantitatively assess fine-scale behaviour during detection events, that is when sharks carrying the novel VMT package (animalR , n = 3) detected sharks independently tagged with transmitters in the system (animalT , n = 29). Concurrently, we developed simulations to estimate the distances between animalR and animalT by accounting for their swim speed, the estimated detection efficiency of the VMT and the number of consecutive transmissions recorded. Accelerometer-derived activity indices were then used as a means to test for response to potential interactions when animals are expected to be in close proximity. Based on this approach, the three VMT-equipped Greenland sharks exhibited higher body acceleration and greater depth changes during detections, suggesting a potential behavioural response to the presence of other sharks. A generalized additive model indicated a moderate increasing relationship in activity associated with a greater number of animalT detections. Through the proposed framework, detection events with varying probabilities of interaction likelihoods can be derived and those data isolated and explicitly tested using acceleration data to quantify behavioural interactions. Through inputting known parameters for a species of interest, the framework presented is applicable for all aquatic taxa and can guide future study design.

Distribution, body size and biology of the megamouth shark Megachasma pelagios.

We compiled historical reports of megamouth sharks Megachasma pelagios (mostly fishery by-catch and strandings) from 1976 to 2018 (n = 117) and found that they are distributed globally (highest latitude, 36°) with three hotspots: Japan, Taiwan and the Philippines. Despite possible biases due to variability in fishing effort, more individuals were reported at higher latitudes in the summer, suggesting seasonal, latitudinal migrations. Sex ratios were female-biased in Japan, but more even in Taiwan and the Philippines, suggesting some sexual segregation. Females (total length, LT = 3.41-7.10 m) were larger than males (LT = 1.77-5.39 m) and matured at a larger LT (5.17 m) than males (4.26 m). Also, we reviewed the systematics, feeding ecology and swimming behaviour of Megachasma pelagios based on the literature. Our review shows that, compared with their morphology, anatomy and genetics, behavioural ecology of this species remains largely unknown and electronic tagging studies are warranted.

Swimming strategies and energetics of endothermic white sharks during foraging.

Some fishes and sea turtles are distinct from ectotherms by having elevated core body temperatures and metabolic rates. Quantifying the energetics and activity of the regionally endothermic species will help us understand how a fundamental biophysical process (i.e. temperature-dependent metabolism) shapes animal ecology; however, such information is limited owing to difficulties in studying these large, highly active animals. White sharks, Carcharodon carcharias, are the largest fish with regional endothermy, and potentially among the most energy-demanding fishes. Here, we deployed multi-sensor loggers on eight white sharks aggregating near colonies of long-nosed fur seals, Arctocephalus forsteri, off the Neptune Islands, Australia. Simultaneous measurements of depth, swim speed (a proxy for swimming metabolic rate) and body acceleration (indicating when sharks exhibited energy-efficient gliding behaviour) revealed their fine-scale swimming behaviour and allowed us to estimate their energy expenditure. Sharks repeatedly dived (mean swimming depth, 29 m) and swam at the surface between deep dives (maximum depth, 108 m). Modal swim speeds (0.80-1.35 m s-1) were slower than the estimated speeds that minimize cost of transport (1.3-1.9 m s-1), a pattern analogous to a 'sit-and-wait' strategy for a perpetually swimming species. All but one shark employed unpowered gliding during descents, rendering deep (>50 m) dives 29% less costly than surface swimming, which may incur additional wave drag. We suggest that these behavioural strategies may help sharks to maximize net energy gains by reducing swimming cost while increasing encounter rates with fast-swimming seals.

Global Monitoring of Persistent Organic Pollutants (POPs) Using Seabird Preen Gland Oil.

Situated at high positions on marine food webs, seabirds accumulate high concentrations of persistent organic pollutants (POPs), such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane and its metabolites (DDTs), and hexachlorocyclohexanes (HCHs). Our previous studies proposed the usefulness of seabirds preen gland oil as a nondestructive biomonitoring tool. The present study applied this approach to 154 adult birds of 24 species collected from 11 locations during 2005-2016 to demonstrate the utility of preen gland oil as a tool for global monitoring POPs, i.e., PCBs, DDTs, and HCHs. Concentrations of the POPs were higher in the Northern Hemisphere than in the Southern Hemisphere. In particular, ∑20PCBs and∑DDTs were highly concentrated in European shags (Phalacrocorax aristotelis) and Japanese cormorants (Phalacrocorax capillatus), explainable by a diet of benthic fishes. Higher concentrations of γ-HCH were detected in species from the polar regions, possibly reflecting the recent exposure and global distillation of ∑HCHs. We examined the relationship between age and POP concentrations in preen gland oil from 20 male European shags, aged 3-16 years old. Concentrations and compositions of POPs were not related to age. We also examined sex differences in the POP concentrations from 24 streaked shearwaters (Calonectris leucomelas) and did not detect a sex bias. These results underline the importance of the geographic concentration patterns and the dietary behavior as determinants species-specific POPs concentrations in preen gland oil.

Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming.

BACKGROUND: Central place foragers (CPF) rest within a central place, and theory predicts that distance of patches from this central place sets the outer limits of the foraging arena. Many marine ectothermic predators behave like CPF animals, but never stop swimming, suggesting that predators will incur 'travelling' costs while resting. Currently, it is unknown how these CPF predators behave or how modulation of behavior contributes to daily energy budgets. We combine acoustic telemetry, multi-sensor loggers, and hidden Markov models (HMMs) to generate 'activity seascapes', which combine space use with patterns of activity, for reef sharks (blacktip reef and grey reef sharks) at an unfished Pacific atoll. RESULTS: Sharks of both species occupied a central place during the day within deeper, cooler water where they were less active, and became more active over a larger area at night in shallower water. However, video cameras on two grey reef sharks revealed foraging attempts/success occurring throughout the day, and that multiple sharks were refuging in common areas. A simple bioenergetics model for grey reef sharks predicted that diel changes in energy expenditure are primarily driven by changes in swim speed and not body temperature. CONCLUSIONS: We provide a new method for simultaneously visualizing diel space use and behavior in marine predators, which does not require the simultaneous measure of both from each animal. We show that blacktip and grey reef sharks behave as CPFs, with diel changes in activity, horizontal and vertical space use. However, aspects of their foraging behavior may differ from other predictions of traditional CPF models. In particular, for species that never stop swimming, patch foraging times may be unrelated to patch travel distance.

Interacting with wildlife tourism increases activity of white sharks.

Anthropogenic activities are dramatically changing marine ecosystems. Wildlife tourism is one of the fastest growing sectors of the tourism industry and has the potential to modify the natural environment and behaviour of the species it targets. Here, we used a novel method to assess the effects of wildlife tourism on the activity of white sharks (Carcharodon carcharias). High frequency three-axis acceleration loggers were deployed on ten white sharks for a total of ~9 days. A combination of multivariate and univariate analysis revealed that the increased number of strong accelerations and vertical movements when sharks are interacting with cage-diving operators result in an overall dynamic body acceleration (ODBA) ~61% higher compared with other times when sharks are present in the area where cage-diving occurs. Since ODBA is considered a proxy of metabolic rate, interacting with cage-divers is probably more costly than are normal behaviours of white sharks at the Neptune Islands. However, the overall impact of cage-diving might be small if interactions with individual sharks are infrequent. This study suggests wildlife tourism changes the instantaneous activity levels of white sharks, and calls for an understanding of the frequency of shark-tourism interactions to appreciate the net impact of ecotourism on this species' fitness.

A miniaturized threshold-triggered acceleration data-logger for recording burst movements of aquatic animals.

Although animal-borne accelerometers are effective tools for quantifying the kinematics of animal behaviors, quantifying the burst movements of small and agile aquatic animals remains challenging. To capture the details of burst movements, accelerometers need to sample at a very high frequency, which will inevitably shorten the recording duration or increase the device size. To overcome this problem, we developed a high-frequency acceleration data-logger that can be triggered by a manually defined acceleration threshold, thus allowing the selective measurement of burst movements. We conducted experiments under laboratory and field conditions to examine the performance of the logger. The laboratory experiment using red seabream (Pagrus major) showed that the new logger could measure the kinematics of their escape behaviors. The field experiment using free-swimming yellowtail kingfish (Seriola lalandi) showed that the loggers trigger correctly. We suggest that this new logger can be applied to measure the burst movements of various small and agile animals.

Optimal swimming strategies and behavioral plasticity of oceanic whitetip sharks.

Animal behavior should optimize the difference between the energy they gain from prey and the energy they spend searching for prey. This is all the more critical for predators occupying the pelagic environment, as prey is sparse and patchily distributed. We theoretically derive two canonical swimming strategies for pelagic predators, that maximize their energy surplus while foraging. They predict that while searching, a pelagic predator should maintain small dive angles, swim at speeds near those that minimize the cost of transport, and maintain constant speed throughout the dive. Using biologging sensors, we show that oceanic whitetip shark (Carcharhinus longimanus) behavior matches these predictions. We estimate that daily energy requirements of an adult shark can be met by consuming approximately 1-1.5 kg of prey (1.5% body mass) per day; shark-borne video footage shows a shark encountering potential prey numbers exceeding that amount. Oceanic whitetip sharks showed incredible plasticity in their behavioral strategies, ranging from short low-energy bursts on descents, to high-speed vertical surface breaches from considerable depth. Oceanic whitetips live a life of energy speculation with minimization, very different to those of tunas and billfish.