Scaling of Activity Space in Marine Organisms across Latitudinal Gradients.

AbstractUnifying models have shown that the amount of space used by animals (e.g., activity space, home range) scales allometrically with body mass for terrestrial taxa; however, such relationships are far less clear for marine species. We compiled movement data from 1,596 individuals across 79 taxa collected using a continental passive acoustic telemetry network of acoustic receivers to assess allometric scaling of activity space. We found that ectothermic marine taxa do exhibit allometric scaling for activity space, with an overall scaling exponent of 0.64. However, body mass alone explained only 35% of the variation, with the remaining variation best explained by trophic position for teleosts and latitude for sharks, rays, and marine reptiles. Taxon-specific allometric relationships highlighted weaker scaling exponents among teleost fish species (0.07) than sharks (0.96), rays (0.55), and marine reptiles (0.57). The allometric scaling relationship and scaling exponents for the marine taxonomic groups examined were lower than those reported from studies that had collated both marine and terrestrial species data derived using various tracking methods. We propose that these disparities arise because previous work integrated summarized data across many studies that used differing methods for collecting and quantifying activity space, introducing considerable uncertainty into slope estimates. Our findings highlight the benefit of using large-scale, coordinated animal biotelemetry networks to address cross-taxa evolutionary and ecological questions.

Centralized red muscle in Odontaspis ferox and the prevalence of regional endothermy in sharks.

The order Lamniformes contains charismatic species such as the white shark Carcharodon carcharias and extinct megatooth shark Otodus megalodon, and is of particular interest given their influence on marine ecosystems, and because some members exhibit regional endothermy. However, there remains significant debate surrounding the prevalence and evolutionary origin of regional endothermy in the order, and therefore the development of phenomena such as gigantism and filter-feeding in sharks generally. Here we show a basal lamniform shark, the smalltooth sand tiger shark Odontaspis ferox, has centralized skeletal red muscle and a thick compact-walled ventricle; anatomical features generally consistent with regionally endothermy. This result, together with the recent discovery of probable red muscle endothermy in filter feeding basking sharks Cetorhinus maximus, suggests that this thermophysiology is more prevalent in the Lamniformes than previously thought, which in turn has implications for understanding the evolution of regional endothermy, gigantism, and extinction risk of warm-bodied shark species both past and present.

Northerly range expansion and first confirmed records of the smalltooth sand tiger shark, Odontaspis ferox, in the United Kingdom and Ireland.

Three Odontaspis ferox (confirmed by mtDNA barcoding) were found in the English Channel and Celtic Sea in 2023 at Lepe, UK (50.7846, -1.3508), Kilmore Quay, Ireland (52.1714, -6.5937), and Lyme Bay, UK (50.6448, -2.9302). These are the first records of O. ferox in either country, and extend the species' range by over three degrees of latitude, to >52° N. They were ~275 (female), 433 (female), and 293 cm (male) total length, respectively. These continue a series of new records, possibly indicative of a climate change-induced shift in the species' range.

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.

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.

Latent power of basking sharks revealed by exceptional breaching events.

The fast swimming and associated breaching behaviour of endothermic mackerel sharks is well suited to the capture of agile prey. In contrast, the observed but rarely documented breaching capability of basking sharks is incongruous to their famously languid lifestyle as filter-feeding planktivores. Indeed, by analysing video footage and an animal-instrumented data logger, we found that basking sharks exhibit the same vertical velocity (approx. 5 m s-1) during breach events as the famously powerful predatory great white shark. We estimate that an 8-m, 2700-kg basking shark, recorded breaching at 5 m s-1 and accelerating at 0.4 m s-2, expended mechanical energy at a rate of 5.5 W kg-1; a mass-specific energetic cost comparable to that of the great white shark. The energy cost of such a breach is equivalent to around 1/17th of the daily standard metabolic cost for a basking shark, while the ratio is about half this for a great white shark. While breaches by basking sharks must serve a different function to white shark breaches, their similar breaching speeds questions our perception of the physiology of large filter-feeding fish.

An alternative explanation for global trends in thermal tolerance.

Ectotherms from higher latitudes can generally perform over broader temperature ranges than tropical ectotherms. This pattern is thought to reflect trends in temperature variability: tropical ectotherms evolve to be 'thermal specialists' because their environment is thermally stable. However, the tropics are also hotter, and most physiological rates increase exponentially with temperature. Using a dataset spanning diverse ectotherms, we show that the temperature ranges ectotherms tolerate (the difference between lower and upper critical temperatures, and between optimum and upper critical temperatures) generally represents the same range of equivalent biological rates (e.g. metabolism) for cool- and warm-adapted species, and independent of latitude or elevation. This suggests that geographical trends in temperature variability may not be the ultimate mechanism underlying latitudinal and elevational trends in thermal tolerance. Rather, we propose that tropical ectotherms can perform over a narrower range of temperatures than species from higher latitudes because the tropics are hotter.

From physiology to physics: are we recognizing the flexibility of biologging tools?

The remote measurement of data from free-ranging animals has been termed 'biologging' and in recent years this relatively small set of tools has been instrumental in addressing remarkably diverse questions--from 'how will tuna respond to climate change?' to 'why are whales big?'. While a single biologging dataset can have the potential to test hypotheses spanning physiology, ecology, evolution and theoretical physics, explicit illustrations of this flexibility are scarce and this has arguably hindered the full realization of the power of biologging tools. Here we present a small set of examples from studies that have collected data on two parameters widespread in biologging research (depth and acceleration), but that have interpreted their data in the context of extremely diverse phenomena: from tests of biomechanical and diving-optimality models to identifications of feeding events, Lévy flight foraging strategies and expanding oxygen minimum zones. We use these examples to highlight the remarkable flexibility of biologging tools, and identify several mechanisms that may enhance the scope and dissemination of future biologging research programs.

Thermal limitation of performance and biogeography in a free-ranging ectotherm: insights from accelerometry.

Theoretical and laboratory studies generally show that ectotherm performance increases with temperature to an optimum, and subsequently declines. Several physiological mechanisms probably shape thermal performance curves, but responses of free-ranging animals to temperature variation will represent a compromise between these mechanisms and ecological constraints. Thermal performance data from wild animals balancing physiology and ecology are rare, and this represents a hindrance for predicting population impacts of future temperature change. We used internally implanted accelerometers near the middle of a species' geographical distribution and gill-net catch data near the species' latitudinal extremes to quantify temperature-related activity levels of a wild predatory fish (Platycephalus fuscus). We examined our data in the context of established models of thermal performance, and the relationship between thermal performance thresholds and biogeography. Acceleration data approximated a thermal performance curve, with activity peaking at 23°C but declining rapidly at higher temperatures. Gill-net catch data displayed a similar trend, with a temperature-associated increase and decrease in catch rates in temperate and tropical regions, respectively. Extrapolated estimates of zero activity (CTmin and CTmax) from the accelerometers were similar to the minimum and maximum mean monthly water temperatures experienced at the southern and northern (respectively) limits of the species distribution, consistent with performance-limited biogeography in this species. These data highlight the fundamental influence of temperature on ectotherm performance, and how thermal performance limits may shape biogeography. Biologging approaches are rarely used to examine thermal performance curves in free-ranging animals, but these may be central to understanding the trade-offs between physiology and ecology that constrain species' biogeographies and determine the susceptibility of ectotherms to future increases in temperature.

Rain reverses diel activity rhythms in an estuarine teleost.

Activity rhythms are ubiquitous in nature, and generally synchronized with the day-night cycle. Several taxa have been shown to switch between nocturnal and diurnal activity in response to environmental variability, and these relatively uncommon switches provide a basis for greater understanding of the mechanisms and adaptive significance of circadian (approx. 24 h) rhythms. Plasticity of activity rhythms has been identified in association with a variety of factors, from changes in predation pressure to an altered nutritional or social status. Here, we report a switch in activity rhythm that is associated with rainfall. Outside periods of rain, the estuarine-associated teleost Acanthopagrus australis was most active and in shallower depths during the day, but this activity and depth pattern was reversed in the days following rain, with diurnality restored as estuarine conductivity and turbidity levels returned to pre-rain levels. Although representing the first example of a rain-induced reversal of activity rhythm in an aquatic animal of which we are aware, our results are consistent with established models on the trade-offs between predation risk and foraging efficiency.

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.

A review of elasmobranch catch-and-release science: synthesis of current knowledge, implications for best practice and future research directions.

Until relatively recently commercial fisheries have been considered the main driving factor for elasmobranch population declines. However, this belief has begun to shift with the realization that recreational elasmobranch catches may equal or exceed commercial catches in some regions. Many recreational angling fisheries for elasmobranchs involve high participation in catch-and-release angling practices. However, high release rates may not necessarily equate to high survival rates. Therefore, to assist accurate assessment of the potential impact of recreational angling on elasmobranchs, we attempted to summarize and integrate currently available information on specific risk factors associated with recreational angling, alongside associated mortality rates, as well as information on angler behaviour as it relates to identified risk factors. We categorized the major angling-related effects into two groups: injury-induced effects; and biochemical disruption-induced effects; providing a summary of each group and outlining the main lethal and sub-lethal outcomes stemming from these. These outcomes include immediate and delayed post-release mortality, behavioural recovery periods (which may in-turn confer increased predation risks), chronic health impacts and capture-induced parturition and abortion. Additionally, we detailed a range of angling practices and equipment, including hook-type, hook removal and emersion (i.e. air exposure), as well as inter- and intra-specific factors, including aerobic scope, respiratory mode, body size and species-specific behaviours, which are likely to influence injury and/or mortality rates and should therefore be considered when assessing angling-related impacts. We then utilized these data to provide a range of actionable recommendations for both anglers and policymakers which would serve to reduce the population-level impact of recreational angling on these enigmatic animals.

Tail shape and the swimming speed of sharks.

Trait-based ecology is a rapidly growing approach for developing insights and predictions for data-poor species. Caudal tail fin shape has the potential to reveal much about the energetics, activity and ecology of fishes and can be rapidly measured from field guides, which is particularly helpful for data-sparse species. One outstanding question is whether swimming speed in sharks is related to two morphological traits: caudal fin aspect ratio (CFAR, height2/tail area) and caudal lobe asymmetry ratio (CLAR). We derived both metrics from the species drawings in Sharks of the world (Ebert et al. 2013 Sharks of the world: a fully illustrated guide) and related fin shape to two published datasets of (1) instantaneous swimming speeds (Jacoby et al. 2015 Biol. Lett. 11, 20150781 (doi:10.1098/rsbl.2015.0781)) and (2) cruising speeds (Harding et al. 2021 Funct. Ecol. 35, 1951-1959 (doi:10.1111/1365-2435.13869)) for 28 total unique shark species. Both estimates of swimming speed were positively related to CFAR (and weakly negatively to CLAR). Hence, shark species with larger CFAR and more symmetric tails (low CLAR) tended to be faster-moving and have higher average speeds. This relationship demonstrates the opportunity to use tail shape as an easily measured trait to index shark swimming speed to broader trait-based analyses of ecological function and extinction risk.

Short-term behavioural responses of Atlantic bluefin tuna to catch-and-release fishing.

Catch-and-release (C&R) angling is often touted as a sustainable form of ecotourism, yet the fine-scale behaviour and physiological responses of released fish is often unknown, especially for hard-to-study large pelagic species like Atlantic bluefin tuna (ABFT; Thunnus thunnus). Multi-channel sensors were deployed and recovered from 10 ABFTs in a simulated recreational C&R event off the west coast of Ireland. Data were recorded from 6 to 25 hours, with one ABFT (tuna X) potentially suffering mortality minutes after release. Almost all ABFTs (n = 9, including tuna X) immediately and rapidly (vertical speeds of ~2.0 m s-1) made powered descents and used 50-60% of the available water column within 20 seconds, before commencing near-horizontal swimming ~60 seconds post-release. Dominant tailbeat frequency was ~50% higher in the initial hours post-release and appeared to stabilize at 0.8-1.0 Hz some 5-10 hours post-release. Results also suggest different short-term behavioural responses to noteworthy variations in capture and handling procedures (injury and reduced air exposure events). Our results highlight both the immediate and longer-term effects of C&R on ABFTs and that small variations in C&R protocols can influence physiological and behavioural responses of species like the commercially valuable and historically over-exploited ABFT.

Tiger sharks support the characterization of the world's largest seagrass ecosystem.

Seagrass conservation is critical for mitigating climate change due to the large stocks of carbon they sequester in the seafloor. However, effective conservation and its potential to provide nature-based solutions to climate change is hindered by major uncertainties regarding seagrass extent and distribution. Here, we describe the characterization of the world's largest seagrass ecosystem, located in The Bahamas. We integrate existing spatial estimates with an updated empirical remote sensing product and perform extensive ground-truthing of seafloor with 2,542 diver surveys across remote sensing tiles. We also leverage seafloor assessments and movement data obtained from instrument-equipped tiger sharks, which have strong fidelity to seagrass ecosystems, to augment and further validate predictions. We report a consensus area of at least 66,000 km2 and up to 92,000 km2 of seagrass habitat across The Bahamas Banks. Sediment core analysis of stored organic carbon further confirmed the global relevance of the blue carbon stock in this ecosystem. Data from tiger sharks proved important in supporting mapping and ground-truthing remote sensing estimates. This work provides evidence of major knowledge gaps in the ocean ecosystem, the benefits in partnering with marine animals to address these gaps, and underscores support for rapid protection of oceanic carbon sinks.

Accelerometry estimates field metabolic rate in giant Australian cuttlefish Sepia apama during breeding.

1. Estimating the metabolic rate of animals in nature is central to understanding the physiological, behavioural and evolutionary ecology of animals. Doubly labelled water and heart-rate methods are the most commonly used approaches, but both have limitations that preclude their application to some systems. 2. Accelerometry has emerged as a powerful tool for estimating energy expenditure in a range of animals, but is yet to be used to estimate field metabolic rate in aquatic taxa. We combined two-dimensional accelerometry and swim-tunnel respirometry to estimate patterns of energy expenditure in giant Australian cuttlefish Sepia apama during breeding. 3. Both oxygen consumption rate (Vo2) and swimming speed showed strong positive associations with body acceleration, with coefficients of determination comparable to those using similar accelerometers on terrestrial vertebrates. Despite increased activity during the day, field metabolic rate rarely approached Vo2, and night-time Vo2 was similar to that at rest. 4. These results are consistent with the life-history strategy of this species, which has a poor capacity to exercise anaerobically, and a mating strategy that is visually based. With the logistical difficulties associated with observation in aquatic environments, accelerometry is likely to prove a valuable tool for estimating energy expenditure in aquatic animals.

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.

Fish heating tolerance scales similarly across individual physiology and populations.

Extrapolating patterns from individuals to populations informs climate vulnerability models, yet biological responses to warming are uncertain at both levels. Here we contrast data on the heating tolerances of fishes from laboratory experiments with abundance patterns of wild populations. We find that heating tolerances in terms of individual physiologies in the lab and abundance in the wild decline with increasing temperature at the same rate. However, at a given acclimation temperature or optimum temperature, tropical individuals and populations have broader heating tolerances than temperate ones. These congruent relationships implicate a tight coupling between physiological and demographic processes underpinning macroecological patterns, and identify vulnerability in both temperate and tropical species.

Powering Ocean Giants: The Energetics of Shark and Ray Megafauna.

Shark and ray megafauna have crucial roles as top predators in many marine ecosystems, but are currently among the most threatened vertebrates and, based on historical extinctions, may be highly susceptible to future environmental perturbations. However, our understanding of their energetics lags behind that of other taxa. Such knowledge is required to answer important ecological questions and predict their responses to ocean warming, which may be limited by expanding ocean deoxygenation and declining prey availability. To develop bioenergetics models for shark and ray megafauna, incremental improvements in respirometry systems are useful but unlikely to accommodate the largest species. Advances in biologging tools and modelling could help answer the most pressing ecological questions about these iconic species.