Diving into the vertical dimension of elasmobranch movement ecology.

Knowledge of the three-dimensional movement patterns of elasmobranchs is vital to understand their ecological roles and exposure to anthropogenic pressures. To date, comparative studies among species at global scales have mostly focused on horizontal movements. Our study addresses the knowledge gap of vertical movements by compiling the first global synthesis of vertical habitat use by elasmobranchs from data obtained by deployment of 989 biotelemetry tags on 38 elasmobranch species. Elasmobranchs displayed high intra- and interspecific variability in vertical movement patterns. Substantial vertical overlap was observed for many epipelagic elasmobranchs, indicating an increased likelihood to display spatial overlap, biologically interact, and share similar risk to anthropogenic threats that vary on a vertical gradient. We highlight the critical next steps toward incorporating vertical movement into global management and monitoring strategies for elasmobranchs, emphasizing the need to address geographic and taxonomic biases in deployments and to concurrently consider both horizontal and vertical movements.

Multivariate analysis of biologging data reveals the environmental determinants of diving behaviour in a marine reptile.

Diving behaviour of 'surfacers' such as sea snakes, cetaceans and turtles is complex and multi-dimensional, thus may be better captured by multi-sensor biologging data. However, analysing these large multi-faceted datasets remains challenging, though a high priority. We used high-resolution multi-sensor biologging data to provide the first detailed description of the environmental influences on flatback turtle (Natator depressus) diving behaviour, during its foraging life-history stage. We developed an analytical method to investigate seasonal, diel and tidal effects on diving behaviour for 24 adult flatback turtles tagged with biologgers. We extracted 16 dive variables associated with three-dimensional and kinematic characteristics for 4128 dives. K-means and hierarchical cluster analyses failed to identify distinct dive types. Instead, principal component analysis objectively condensed the dive variables, removing collinearity and highlighting the main features of diving behaviour. Generalized additive mixed models of the main principal components identified significant seasonal, diel and tidal effects on flatback turtle diving behaviour. Flatback turtles altered their diving behaviour in response to extreme tidal and water temperature ranges, displaying thermoregulation and predator avoidance strategies while likely optimizing foraging in this challenging environment. This study demonstrates an alternative statistical technique for objectively interpreting diving behaviour from multivariate collinear data derived from biologgers.

The power of national acoustic tracking networks to assess the impacts of human activity on marine organisms during the COVID-19 pandemic.

COVID-19 restrictions have led to an unprecedented global hiatus in anthropogenic activities, providing a unique opportunity to assess human impact on biological systems. Here, we describe how a national network of acoustic tracking receivers can be leveraged to assess the effects of human activity on animal movement and space use during such global disruptions. We outline variation in restrictions on human activity across Australian states and describe four mechanisms affecting human interactions with the marine environment: 1) reduction in economy and trade changing shipping traffic; 2) changes in export markets affecting commercial fisheries; 3) alterations in recreational activities; and 4) decline in tourism. We develop a roadmap for the analysis of acoustic tracking data across various scales using Australia's national Integrated Marine Observing System (IMOS) Animal Tracking Facility as a case study. We illustrate the benefit of sustained observing systems and monitoring programs by assessing how a 51-day break in white shark (Carcharodon carcharias) cage-diving tourism due to COVID-19 restrictions affected the behaviour and space use of two resident species. This cessation of tourism activities represents the longest break since cage-diving vessels started day trips in this area in 2007. Long-term monitoring of the local environment reveals that the activity space of yellowtail kingfish (Seriola lalandi) was reduced when cage-diving boats were absent compared to periods following standard tourism operations. However, white shark residency and movements were not affected. Our roadmap is globally applicable and will assist researchers in designing studies to assess how anthropogenic activities can impact animal movement and distributions during regional, short-term through to major, unexpected disruptions like the COVID-19 pandemic.

Temporal niche partitioning as a novel mechanism promoting co-existence of sympatric predators in marine systems.

Niche partitioning of time, space or resources is considered the key to allowing the coexistence of competitor species, and particularly guilds of predators. However, the extent to which these processes occur in marine systems is poorly understood due to the difficulty in studying fine-scale movements and activity patterns in mobile underwater species. Here, we used acceleration data-loggers to investigate temporal partitioning in a guild of marine predators. Six species of co-occurring large coastal sharks demonstrated distinct diel patterns of activity, providing evidence of strong temporal partitioning of foraging times. This is the first instance of diel temporal niche partitioning described in a marine predator guild, and is probably driven by a combination of physiological constraints in diel timing of activity (e.g. sensory adaptations) and interference competition (hierarchical predation within the guild), which may force less dominant predators to suboptimal foraging times to avoid agonistic interactions. Temporal partitioning is often thought to be rare compared to other partitioning mechanisms, but the occurrence of temporal partitioning here and similar characteristics in many other marine ecosystems (multiple predators simultaneously present in the same space with dietary overlap) introduces the question of whether this is a common mechanism of resource division in marine systems.

Using tri-axial accelerometer loggers to identify spawning behaviours of large pelagic fish.

BACKGROUND: Tri-axial accelerometers have been used to remotely describe and identify in situ behaviours of a range of animals without requiring direct observations. Datasets collected from these accelerometers (i.e. acceleration, body position) are often large, requiring development of semi-automated analyses to classify behaviours. Marine fishes exhibit many "burst" behaviours with high amplitude accelerations that are difficult to interpret and differentiate. This has constrained the development of accurate automated techniques to identify different "burst" behaviours occurring naturally, where direct observations are not possible. METHODS: We trained a random forest machine learning algorithm based on 624 h of accelerometer data from six captive yellowtail kingfish during spawning periods. We identified five distinct behaviours (swim, feed, chafe, escape, and courtship), which were used to train the model based on 58 predictive variables. RESULTS: Overall accuracy of the model was 94%. Classification of each behavioural class was variable; F1 scores ranged from 0.48 (chafe) - 0.99 (swim). The model was subsequently applied to accelerometer data from eight free-ranging kingfish, and all behaviour classes described from captive fish were predicted by the model to occur, including 19 events of courtship behaviours ranging from 3 s to 108 min in duration. CONCLUSION: Our findings provide a novel approach of applying a supervised machine learning model on free-ranging animals, which has previously been predominantly constrained to direct observations of behaviours and not predicted from an unseen dataset. Additionally, our findings identify typically ambiguous spawning and courtship behaviours of a large pelagic fish as they naturally occur.

Accounting for body mass effects in the estimation of field metabolic rates from body acceleration.

Dynamic body acceleration (DBA), measured through animal-attached tags, has emerged as a powerful method for estimating field metabolic rates of free-ranging individuals. Following respirometry to calibrate oxygen consumption rate (MO2) with DBA under controlled conditions, predictive models can be applied to DBA data collected from free-ranging individuals. However, laboratory calibrations are generally performed on a relatively narrow size range of animals, which may introduce biases if predictive models are applied to differently sized individuals in the field. Here, we tested the mass dependence of the MO2-DBA relationship to develop an experimental framework for the estimation of field metabolic rates when organisms differ in size. We performed respirometry experiments with individuals spanning one order of magnitude in body mass (1.74-17.15 kg) and used a two-stage modelling process to assess the intraspecific scale dependence of the MO2-DBA relationship and incorporate such dependencies into the coefficients of MO2 predictive models. The final predictive model showed scale dependence; the slope of the MO2-DBA relationship was strongly allometric (M1.55), whereas the intercept term scaled closer to isometry (M1.08). Using bootstrapping and simulations, we evaluated the performance of this coefficient-corrected model against commonly used methods of accounting for mass effects on the MO2-DBA relationship and found the lowest error and bias in the coefficient-corrected approach. The strong scale dependence of the MO2-DBA relationship indicates that caution must be exercised when models developed using one size class are applied to individuals of different sizes.

Wet season flood magnitude drives resilience to dry season drought of a euryhaline elasmobranch in a dry-land river.

The increase in severity and occurrence of drought from environmental change poses a significant threat to freshwater ecosystems. However, many of the mechanisms by which periodic drought affects aquatic animals are poorly understood. Here we integrated physical, physiological, and behavioural measurements made in the field over a twelve-year period to provide a comprehensive understanding of the factors affecting the loss of body condition of fish in arid rivers, using the Critically Endangered freshwater sawfish (Pristis pristis) in the dryland Fitzroy River, Western Australia, as a model species. Sawfish lost condition throughout the long dry season in all years and had significantly poorer body condition throughout years characterized by low volumes of wet season flooding and little occurrence of overbank flooding. A mechanistic examination of factors leading to this loss of condition using measurements of body temperature, field energetics, and habitat use from telemetry techniques showed that the loss of condition throughout the season was likely due to substantial habitat compression and low productivity in drier years, while high rates of competition were more likely to drive this pattern in wetter years. This information can be used to forecast how climate change and water abstraction will affect aquatic fauna experiencing intermittent drought and can inform management decisions to help mitigate these threats.

Depth-dependent dive kinematics suggest cost-efficient foraging strategies by tiger sharks.

Tiger sharks, Galeocerdo cuvier, are a keystone, top-order predator that are assumed to engage in cost-efficient movement and foraging patterns. To investigate the extent to which oscillatory diving by tiger sharks conform to these patterns, we used a biologging approach to model their cost of transport. High-resolution biologging tags with tri-axial sensors were deployed on 21 tiger sharks at Ningaloo Reef for durations of 5-48 h. Using overall dynamic body acceleration as a proxy for energy expenditure, we modelled the cost of transport of oscillatory movements of varying geometries in both horizontal and vertical planes for tiger sharks. The cost of horizontal transport was minimized by descending at the smallest possible angle and ascending at an angle of 5-14°, meaning that vertical oscillations conserved energy compared to swimming at a level depth. The reduction of vertical travel costs occurred at steeper angles. The absolute dive angles of tiger sharks increased between inshore and offshore zones, presumably to reduce the cost of transport while continuously hunting for prey in both benthic and surface habitats. Oscillatory movements of tiger sharks conform to strategies of cost-efficient foraging, and shallow inshore habitats appear to be an important habitat for both hunting prey and conserving energy while travelling.

Divergent field metabolic rates highlight the challenges of increasing temperatures and energy limitation in aquatic ectotherms.

Environments where extreme temperatures and low productivity occur introduce energetically challenging circumstances that may be exacerbated by climate change. Despite the strong link between metabolism and temperature in ectotherms, there is a paucity of data regarding how the metabolic ecology of species affects growth and fitness under such circumstances. Here, we integrated data describing field metabolic rates and body condition of two sympatric species of ectotherms with divergent lifestyles, the benthic freshwater (or largetooth) sawfish (Pristis pristis) and the epipelagic bull shark (Carcharhinus leucas) occurring in the Fitzroy River, Western Australia, to test the implications of their differing metabolic ecologies for vulnerability to rising temperatures. Over a temperature range of 18-34 °C, sawfish had lower field metabolic rates (63-187 mg O2 kg-0.86 h-1) and lower temperature sensitivity of metabolic rates [activation energy (EA) = 0.35 eV] than bull sharks (187-506 mg O2 kg-0.86 h-1; EA = 0.48 eV). Both species lost body mass throughout the dry season, although bull sharks significantly more (0.17% mass loss day-1) than sawfish (0.07% mass loss day-1). Subsequent bioenergetics modelling showed that under future climate change scenarios, both species would reach potentially lethal levels of mass loss during dry season periods before the end of the century. These results suggest that ectotherms with low metabolic rates may be better suited to extreme environmental conditions, and that even small increases in temperature due to climate change could have substantial impacts on the ability of ectotherms to grow and survive in harsh conditions, including high temperatures and energy-limiting circumstances.

Biomechanical Analysis of the Slow-Twitch (Red) Muscle Force Transmission Pathways in Tunas.

In tunas, the slow-twitch red muscle, which has an elevated temperature, powers thunniform locomotion, a stiff-bodied swimming style. The anatomical placement and operating temperatures of red muscle vary widely among teleosts: in tunas, the red muscle is located centrally in the body, adjacent to the spine, and maintains an elevated temperature. In the majority of ectothermic teleosts, red muscle is located laterally in the body, adjacent to the skin, and operates at ambient temperature. The specialized physiology and biomechanics of red muscle in tunas are often considered important adaptations to their high-performance pelagic lifestyle; however, the mechanics of how muscular work is transmitted to the tail remains largely unknown. The red muscle has a highly pennate architecture and is connected to the spine through a network of bones (epicentral bones) and long tendons (posterior oblique tendons). The network of long tendons has been hypothesized to enhance the power transmitted to the tail. Here, we investigate the morphology and biomechanics of the tuna's red muscle and tendons to determine whether elasticity is exploited to reduce the cost of transport, as is the case in many terrestrial vertebrates. To address this question, we evaluate two hypotheses: (1) tendons stretch during red-muscle-actuated swimming and (2) tendons comprise the primary load transmission pathway from the red muscle to the spine. To evaluate these hypotheses, we measured the mechanical properties of the posterior oblique tendons and performed novel dissections to estimate the peak force that the red muscle can generate. The force-generating capacity of the red muscle is calculated to be much greater than the load-bearing capacity of the posterior oblique tendons. Thus, the long tendons likely stretch under force from the red muscle, but they are not strong enough to be the primary force transmission pathway. These results suggest that other pathways, such as serial load transmission through the red muscle myomeres to the great lateral tendon and/or the anterior oblique tendons to the skin, transmit appreciable force to the tail.

Respirometer in a box: development and use of a portable field respirometer for estimating oxygen consumption of large-bodied fishes.

This study developed a portable, low-cost field respirometer for measuring oxygen consumption rates of large-bodied fishes. The respirometer performed well in laboratory tests and was used to measure the oxygen consumption rates ( M ˙ O2 ) of bull sharks Carcharhinus leucas (mean: 249.21 ± 58.10 mg O2 kg-1 h-1 at 27.05°C). Interspecific comparisons and assessments of oxygen degradation curves indicated that the respirometer provided reliable measurements of M ˙ O2 . This system presents a field-based alternative to laboratory respirometers, opening opportunities for studies on species in remote localities, increasing the ability to validate physiological field studies.

Recruitment of a critically endangered sawfish into a riverine nursery depends on natural flow regimes.

The freshwater sawfish (Pristis pristis) was recently listed as the most Evolutionarily Distinct and Globally Endangered (EDGE) animal. The Fitzroy River in the remote Kimberley region of north-western Australia represents a significant stronghold for the species, which uses the freshwater reaches of the river as a nursery. There is also mounting pressure to develop the water resources of the region for agriculture that may substantially affect life history dynamics of sawfish in this system. However, the relationship between hydrology and population dynamics of freshwater sawfish was unknown. We used standardized catch data collected over 17 years to determine how wet season volume influences recruitment of freshwater sawfish into their riverine nursery. Negligible recruitment occurred in years with few days of high flood levels (above 98th percentile of cease-to-flow stage height), and relatively high recruitment occurred in years with 14 or more days of high flood levels. This relationship is indicative of a distinct boom-or-bust cycle, whereby freshwater sawfish rely almost entirely on the few years with large wet season floods, and the brief periods of highest water levels within these years, to replenish juvenile populations in the Fitzroy River nursery. This has direct implications for sustainable water resource management for the Fitzroy River basin in order to preserve one of the last known intact nursery habitats for this globally threatened species.

Thermal performance responses in free-ranging elasmobranchs depend on habitat use and body size.

Temperature is one of the most influential drivers of physiological performance and behaviour in ectotherms, determining how these animals relate to their ecosystems and their ability to succeed in particular habitats. Here, we analysed the largest set of acceleration data compiled to date for elasmobranchs to examine the relationship between volitional activity and temperature in 252 individuals from 8 species. We calculated activation energies for the thermal performance response in each species and estimated optimum temperatures using an Arrhenius breakpoint analysis, subsequently fitting thermal performance curves to the activity data. Juveniles living in confined nursery habitats not only spent substantially more time above their optimum temperature and at the upper limits of their performance breadths compared to larger, less site-restricted animals, but also showed lower activation energies and broader performance curves. Species or life stages occupying confined habitats featured more generalist behavioural responses to temperature change, whereas wider ranging elasmobranchs were characterised by more specialist behavioural responses. The relationships between the estimated performance regimes and environmental temperature limits suggest that animals in confined habitats, including many juvenile elasmobranchs within nursery habitats, are likely to experience a reduction of performance under a warming climate, although their flatter thermal response will likely dampen this impact. The effect of warming on less site-restricted species is difficult to forecast since three of four species studied here did not reach their optimum temperature in the wild, although their specialist performance characteristics may indicate a more rapid decline should optimum temperatures be exceeded.

Direct measurement of swimming and diving kinematics of giant Atlantic bluefin tuna (Thunnus thynnus).

Tunas possess a range of physiological and mechanical adaptations geared towards high-performance swimming that are of considerable interest to physiologists, ecologists and engineers. Advances in biologging have provided significant improvements in understanding tuna migrations and vertical movement patterns, yet our understanding of the locomotion and swimming mechanics of these fish under natural conditions is limited. We equipped Atlantic bluefin tuna (Thunnus thynnus) with motion-sensitive tags and video cameras to quantify the gaits and kinematics used by wild fish. Our data reveal significant variety in the locomotory kinematics of Atlantic bluefin tuna, ranging from continuous locomotion to two types of intermittent locomotion. The tuna sustained swimming speeds in excess of 1.5 m s-1 (0.6 body lengths s-1), while beating their tail at a frequency of approximately 1 Hz. While diving, some descents were entirely composed of passive glides, with slower descent rates featuring more gliding, while ascents were primarily composed of active swimming. The observed swimming behaviour of Atlantic bluefin tuna is consistent with theoretical models predicting such intermittent locomotion to result in mechanical and physiological advantages. Our results confirm that Atlantic bluefin tuna possess behavioural specializations to increase their locomotory performance, which together with their unique physiology improve their capacity to use pelagic and mesopelagic habitats.

Cryptic habitat use of white sharks in kelp forest revealed by animal-borne video.

Traditional forms of marine wildlife research are often restricted to coarse telemetry or surface-based observations, limiting information on fine-scale behaviours such as predator-prey events and interactions with habitat features. We use contemporary animal-attached cameras with motion sensing dataloggers, to reveal novel behaviours by white sharks, Carcharodon carcharias, within areas of kelp forest in South Africa. All white sharks tagged in this study spent time adjacent to kelp forests, with several moving throughout densely kelp-covered areas, navigating through channels and pushing directly through stipes and fronds. We found that activity and turning rates significantly increased within kelp forest. Over 28 h of video data revealed that white shark encounters with Cape fur seals, Arctocephalus pusillus pusillus, occurred exclusively within kelp forests, with seals displaying predator evasion behaviour during those encounters. Uniquely, we reveal the use of kelp forest habitat by white sharks, previously assumed inaccessible to these large predators.

Temperature dependent pre- and postprandial activity in Pacific bluefin tuna (Thunnus orientalis).

Bluefin tunas are highly specialized fish with unique hydrodynamic designs and physiological traits. In this study, we present results in a captive population that demonstrate strong effects of ambient temperature on the tail beat frequency and swimming speed of a pelagic fish in both pre- and post-prandial states. We measured the responses of a ram ventilator, the Pacific bluefin tuna (Thunnus orientalis), after digestion of a meal to explore the impacts of the metabolic costs of digestion on behavior and respiration. A combination of respirometry, physiological biologging of visceral temperatures, and activity monitoring with accelerometry were used to explore the metabolic costs of digestion and the impacts on ventilation and swimming speed. Experiments were conducted at temperatures that are within the metabolic optimum for Pacific bluefin tuna (17 °C), and at a second temperature corresponding to the upper distributional limit of the species in the California Current (24 °C). Warmer temperatures resulted in higher tail-beat frequency and greater elevation of body temperature in pre-prandial Pacific bluefin tuna. Specific dynamic action (SDA) events resulted in a significant postprandial increase in tail-beat frequency of ~0.2 Hz, compared to pre-prandial levels of 1.5 Hz (17 °C) and 1.75 Hz (24 °C), possibly resulting from ventilatory requirements. Data of fish exercised in a swim-tunnel respirometer suggest that the observed increase in tail-beat frequency comprise 5.5 and 6.8% of the oxygen demand during peak SDA at 24 °C and 17 °C respectively. The facultative increase in swimming speed might increase oxygen uptake at the gills to meet the increasing demand by visceral organs involved in the digestive process, potentially decreasing the available energy of each meal for other metabolic processes, such as growth, maturation, and reproduction. We hypothesize that these post-prandial behaviors allow tuna to evacuate their guts more quickly, ultimately permitting fish to feed more frequently when prey is available.

Metabolic rates and the energetic cost of external tag attachment in juvenile blacktip sharks Carcharhinus limbatus.

This study reports on the metabolic rate of the blacktip shark Carcharhinus limbatus and the energetic costs of external tag attachment. Metabolic rates, swimming speed and tail-beat (BT ) frequency were measured in a static respirometer with untagged animals and animals equipped with a small data logger. Tagged sharks showed significantly higher routine oxygen consumption and lower swimming speeds than untagged animals, indicating that tagging significantly affected the swimming efficiency and energetic requirements in these small sharks, and that these effects must be accounted for when interpreting telemetry data from free-ranging individuals.

Temperature and the vertical movements of oceanic whitetip sharks, Carcharhinus longimanus.

Large-bodied pelagic ectotherms such as sharks need to maintain internal temperatures within a favourable range in order to maximise performance and be cost-efficient foragers. This implies that behavioural thermoregulation should be a key feature of the movements of these animals, although field evidence is limited. We used depth and temperature archives from pop-up satellite tags to investigate the role of temperature in driving vertical movements of 16 oceanic whitetip sharks, Carcharhinus longimanus, (OWTs). Spectral analysis, linear mixed modelling, segmented regression and multivariate techniques were used to examine the effect of mean sea surface temperature (SST) and mixed layer depth on vertical movements. OWTs continually oscillated throughout the upper 200 m of the water column. In summer when the water column was stratified with high SSTs, oscillations increased in amplitude and cycle length and sharks reduced the time spent in the upper 50 m. In winter when the water column was cooler and well-mixed, oscillations decreased in amplitude and cycle length and sharks frequently occupied the upper 50 m. SSTs of 28 oC marked a distinct change in vertical movements and the onset of thermoregulation strategies. Our results have implications for the ecology of these animals in a warming ocean.

Physical trade-offs shape the evolution of buoyancy control in sharks.

Buoyancy control is a fundamental aspect of aquatic life that has major implications for locomotor performance and ecological niche. Unlike terrestrial animals, the densities of aquatic animals are similar to the supporting fluid, thus even small changes in body density may have profound effects on locomotion. Here, we analysed the body composition (lipid versus lean tissue) of 32 shark species to study the evolution of buoyancy. Our comparative phylogenetic analyses indicate that although lean tissue displays minor positive allometry, liver volume exhibits pronounced positive allometry, suggesting that larger sharks evolved bulkier body compositions by adding lipid tissue to lean tissue rather than substituting lean for lipid tissue, particularly in the liver. We revealed a continuum of buoyancy control strategies that ranged from more buoyant sharks with larger livers in deeper ecosystems to relatively denser sharks with small livers in epipelagic habitats. Across this eco-morphological spectrum, our hydrodynamic modelling suggests that neutral buoyancy yields lower drag and more efficient steady swimming, whereas negative buoyancy may be more efficient during accelerated movements. The evolution of buoyancy control in sharks suggests that ecological and physiological factors mediate the selective pressures acting on these traits along two major gradients, body size and habitat depth.