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.

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.

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.

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.

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.

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.

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.

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.

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.

Correlations of metabolic rate and body acceleration in three species of coastal sharks under contrasting temperature regimes.

The ability to produce estimates of the metabolic rate of free-ranging animals is fundamental to the study of their ecology. However, measuring the energy expenditure of animals in the field has proved difficult, especially for aquatic taxa. Accelerometry presents a means of translating metabolic rates measured in the laboratory to individuals studied in the field, pending appropriate laboratory calibrations. Such calibrations have only been performed on a few fish species to date, and only one where the effects of temperature were accounted for. Here, we present calibrations between activity, measured as overall dynamic body acceleration (ODBA), and metabolic rate, measured through respirometry, for nurse sharks (Ginglymostoma cirratum), lemon sharks (Negaprion brevirostris) and blacktip sharks (Carcharhinus limbatus). Calibrations were made at a range of volitional swimming speeds and experimental temperatures. Linear mixed models were used to determine a predictive equation for metabolic rate based on measured ODBA values, with the optimal model using ODBA in combination with activity state and temperature to predict metabolic rate in lemon and nurse sharks, and ODBA and temperature to predict metabolic rate in blacktip sharks. This study lays the groundwork for calculating the metabolic rate of these species in the wild using acceleration data.

Swimming activity and energetic costs of adult lake sturgeon during fishway passage.

Fish migrations through riverine systems can be energetically demanding, and the presence of fishways to facilitate upstream passage can add an additional energetic cost that may directly affect fitness. Successful fishway passage is a function of the ability of fish to select appropriate paths and swimming strategies that do not exceed their swimming capacity. Triaxial accelerometers were used to estimate the energetic expenditure of adult lake sturgeon (Acipenser fulvescens) swimming through a vertical slot fishway, to determine whether individual behaviour or path selection, resulting in differences in cumulative energy use, explain fishway passage success. Most individuals attempted to pass the fishway (n=30/44; 68%), although successful passage only occurred for a subset of those attempting (n=7/30; 23%). High-speed swimming was rarely observed during upstream passage through fishway basins, and was of short duration. Two turning basins delayed passage, subsequently resulting in a higher energetic cost. The rate at which energy was expended did not differ among successful and unsuccessful individuals, although successful sturgeon exhibited higher costs of transport (42.75 versus 25.85 J kg(-1) m(-1)). Energy expenditure metrics were not predictive of successful fishway passage, leading us to conclude that other endogenous or exogenous factors influence passage success. In a practical application of field measurements of energy expenditure, we demonstrate that fishway passage through a structure designed to facilitate migration does result in an energetic loss for lake sturgeon (3249-16,331 J kg(-1)), equivalent to individuals travelling 5.8-28.2 km in a lentic system.

The effect of temperature on postprandial metabolism of yellowfin tuna (Thunnus albacares).

Specific dynamic action (SDA), the increase in metabolic expenditure associated with consumption of a meal, represents a substantial portion of fish energy budgets and is highly influenced by ambient temperature. The effect of temperature on SDA has not been studied in yellowfin tuna (Thunnus albacares, Bonnaterre 1788), an active pelagic predator that occupies temperate and subtropical waters. The energetic cost and duration of SDA were calculated by comparing routine and post-prandial oxygen consumption rates. Mean routine metabolic rates in yellowfin tuna increased with temperature, from 136 mg O2 kg(-1)h(-1) at 20 °C to 211 mg O2 kg(-1)h at 24 °C. The mean duration of SDA decreased from 40.2h at 20 °C to 33.1h at 24 °C, while mean SDA coefficient, the percentage of energy in a meal that is consumed during digestion, increased from 5.9% at 20 °C to 12.7% at 24 °C. Digestion in yellowfin tuna is faster at a higher temperature but requires additional oxidative energy. Enhanced characterization of the role of temperature in SDA of yellowfin tuna deepens our understanding of tuna physiology and can help improve management of aquaculture and fisheries.

Mechanical challenges to freshwater residency in sharks and rays.

Major transitions between marine and freshwater habitats are relatively infrequent, primarily as a result of major physiological and ecological challenges. Few species of cartilaginous fish have evolved to occupy freshwater habitats. Current thought suggests that the metabolic physiology of sharks has remained a barrier to the diversification of this taxon in freshwater ecosystems. Here, we demonstrate that the physical properties of water provide an additional constraint for this species-rich group to occupy freshwater systems. Using hydromechanical modeling, we show that occurrence in fresh water results in a two- to three-fold increase in negative buoyancy for sharks and rays. This carries the energetic cost of lift production and results in increased buoyancy-dependent mechanical power requirements for swimming and increased optimal swim speeds. The primary source of buoyancy, the lipid-rich liver, offers only limited compensation for increased negative buoyancy as a result of decreasing water density; maintaining the same submerged weight would involve increasing the liver volume by very large amounts: 3- to 4-fold in scenarios where liver density is also reduced to currently observed minimal levels and 8-fold without any changes in liver density. The first data on body density from two species of elasmobranch occurring in freshwater (the bull shark Carcharhinus leucas, Müller and Henle 1839, and the largetooth sawfish Pristis pristis, Linnaeus 1758) support this hypothesis, showing similar liver sizes as marine forms but lower liver densities, but the greatest negative buoyancies of any elasmobranch studied to date. Our data suggest that the mechanical challenges associated with buoyancy control may have hampered the invasion of freshwater habitats in elasmobranchs, highlighting an additional key factor that may govern the predisposition of marine organisms to successfully establish in freshwater habitats.

High activity and Levy searches: jellyfish can search the water column like fish.

Over-fishing may lead to a decrease in fish abundance and a proliferation of jellyfish. Active movements and prey search might be thought to provide a competitive advantage for fish, but here we use data-loggers to show that the frequently occurring coastal jellyfish (Rhizostoma octopus) does not simply passively drift to encounter prey. Jellyfish (327 days of data from 25 jellyfish with depth collected every 1 min) showed very dynamic vertical movements, with their integrated vertical movement averaging 619.2 m d(-1), more than 60 times the water depth where they were tagged. The majority of movement patterns were best approximated by exponential models describing normal random walks. However, jellyfish also showed switching behaviour from exponential patterns to patterns best fitted by a truncated Lévy distribution with exponents (mean µ=1.96, range 1.2-2.9) close to the theoretical optimum for searching for sparse prey (µopt≈2.0). Complex movements in these 'simple' animals may help jellyfish to compete effectively with fish for plankton prey, which may enhance their ability to increase in dominance in perturbed ocean systems.

Does prey size matter? Novel observations of feeding in the leatherback turtle (Dermochelys coriacea) allow a test of predator-prey size relationships.

Optimal foraging models predict that large predators should concentrate on large prey in order to maximize their net gain of energy intake. Here, we show that the largest species of sea turtle, Dermochelys coriacea, does not strictly adhere to this general pattern. Field observations combined with a theoretical model suggest that a 300 kg leatherback turtle would meet its energetic requirements by feeding for 3-4 h a day on 4 g jellyfish, but only if prey were aggregated in high-density patches. Therefore, prey abundance rather than prey size may, in some cases, be the overriding parameter for foraging leatherbacks. This is a classic example where the presence of small prey in the diet of a large marine predator may reflect profitable foraging decisions if the relatively low energy intake per small individual prey is offset by high encounter rates and minimal capture and handling costs. This study provides, to our knowledge, the first quantitative estimates of intake rate for this species.

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.

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.

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.