The vulnerability of sharks, skates, and rays to ocean deoxygenation: Physiological mechanisms, behavioral responses, and ecological impacts.

Levels of dissolved oxygen in open ocean and coastal waters are decreasing (ocean deoxygenation), with poorly understood effects on marine megafauna. All of the more than 1000 species of elasmobranchs (sharks, skates, and rays) are obligate water breathers, with a variety of life-history strategies and oxygen requirements. This review demonstrates that although many elasmobranchs typically avoid hypoxic water, they also appear capable of withstanding mild to moderate hypoxia with changes in activity, ventilatory responses, alterations to circulatory and hematological parameters, and morphological alterations to gill structures. However, such strategies may be insufficient to withstand severe, progressive, or prolonged hypoxia or anoxia where anaerobic metabolic pathways may be used for limited periods. As water temperatures increase with climate warming, ectothermic elasmobranchs will exhibit elevated metabolic rates and are likely to be less able to tolerate the effects of even mild hypoxia associated with deoxygenation. As a result, sustained hypoxic conditions in warmer coastal or surface-pelagic waters are likely to lead to shifts in elasmobranch distributions. Mass mortalities of elasmobranchs linked directly to deoxygenation have only rarely been observed but are likely underreported. One key concern is how reductions in habitat volume as a result of expanding hypoxia resulting from deoxygenation will influence interactions between elasmobranchs and industrial fisheries. Catch per unit of effort of threatened pelagic sharks by longline fisheries, for instance, has been shown to be higher above oxygen minimum zones compared to adjacent, normoxic regions, and attributed to vertical habitat compression of sharks overlapping with increased fishing effort. How a compound stressor such as marine heatwaves alters vulnerability to deoxygenation remains an open question. With over a third of elasmobranch species listed as endangered, a priority for conservation and management now lies in understanding and mitigating ocean deoxygenation effects in addition to population declines already occurring from overfishing.

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.

Mammography Breast Cancer Screening Triage Using Deep Learning: A UK Retrospective Study.

Background Breast screening enables early detection of cancers; however, most women have normal mammograms, resulting in repetitive and resource-intensive reading tasks. Purpose To investigate if deep learning (DL) algorithms can be used to triage mammograms by identifying normal results to reduce workload or flag cancers that may be overlooked. Materials and Methods In this retrospective study, three commercial DL algorithms were investigated using consecutive mammograms from two UK Breast Screening Program sites from January 2015 to December 2017 and January 2017 to December 2018 on devices from two mammography vendors. Normal mammograms with a 3-year follow-up and histopathologically proven cancer detected at screening, the subsequent round, or in the 3-year interval were included. Two algorithm thresholds were set: in scenario A, 99.0% sensitivity for rule-out triage to a lone reader, and in scenario B, approximately 1.0% additional recall providing a rule-in triage for further assessment. Both thresholds were then applied to the screening workflow in scenario C. The sensitivity and specificity were used to assess the overall predictive performance of each DL algorithm. Results The data set comprised 78 849 patients (median age, 59 years [IQR, 53-63 years]) and 887 screening-detected, 439 interval, and 688 subsequent screening round-detected cancers. In scenario A (rule-out triage), models DL-1, DL-2, and DL-3 triaged 35.0% (27 565 of 78 849), 53.2% (41 937 of 78 849), and 55.6% (43 869 of 78 849) of mammograms, respectively, with 0.0% (0 of 887) to 0.1% (one of 887) of screening-detected cancers undetected. In scenario B, DL algorithms triaged in 4.6% (20 of 439) to 8.2% (36 of 439) of interval and 5.2% (36 of 688) to 6.1% (42 of 688) of subsequent-round cancers when applied after the routine double-reading workflow. Combining both approaches in scenario C resulted in an overall noninferior specificity (difference, -0.9%; P < .001) and superior sensitivity (difference, 2.7%; P < .001) for the adaptive workflow compared with routine double reading for all three algorithms. Conclusion Rule-out and rule-in DL-adapted triage workflows can improve the efficiency and efficacy of mammography breast cancer screening. © RSNA, 2023 Supplemental material is available for this article. See also the editorial by Nishikawa and Lu in this issue.

Energetic costs increase with faster heating in an aquatic ectotherm.

The thermal sensitivity of metabolism is widely studied due to its perceived importance for organismal fitness and resilience to future climate change. Almost all such studies estimate metabolism at a variety of constant temperatures, with very little work exploring how metabolism varies during temperature change. However, temperature in nature is rarely static, so our existing understanding from experiments may not reflect how temperature influences metabolism in natural systems. Using closed-chamber respirometry, we estimated the aerobic metabolic rate of an aquatic ectotherm, the Atlantic ditch shrimp Palaemonetes varians, under varying thermal conditions. We continuously measured oxygen consumption of shrimp during heating, cooling and constant temperatures, starting trials at a range of acclimation temperatures and exposing shrimp to a variety of rates of temperature change. In a broad sense, cumulative oxygen consumption estimated from static temperature exposures corresponded to estimates derived from ramping experiments. However, further analyses showed that oxygen consumption increases for both faster heating and faster cooling, with rapid heating driving higher metabolic rates than if shrimp were warmed slowly. These results suggest a systematic influence of heating rate on the thermal sensitivity of metabolism. With influential concepts such as the metabolic theory of ecology founded in data from constant temperature experiments, our results encourage further exploration of how variable temperature impacts organism energetics, and to test the generality of our findings across species. This is especially important given climate forecasts of heat waves that are characterised by both increased temperatures and faster rates of change.

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.

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.

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.

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.

Periodic aggregation patterns of oxide particles on corroding metals: chemical waves due to solution feedback processes.

Chemical waves that produce periodic patterns are common occurrences in nature. The underlying processes involved have been studied in many disciplines of science, but rarely reported in the chemistry of corrosion. In this study of carbon steel corrosion, iron oxide crystals are observed to deposit in concentric wave patterns or in discrete bands, known as Liesegang patterns. We demonstrate that oxide growth in these patterns is preceded by the formation of a hydrogel network, which consists of a semi-stationary phase of loosely connected metal-hydroxide colloids and a mobile phase of solution saturated with metal cations. Once the hydrogel network covers the metal surface, a metal cation produced by corrosion reactions at the metal surface must diffuse through the layer into the bulk solution. While diffusing through the porous network, the metal cation undergoes adsorption-precipitation as metal-hydroxide colloids which later can dissolve back into the solution. When the kinetics of precipitation and dissolution of the metal cation can be effectively coupled with the transport flux of the dissolved metal cation, the precipitation-dissolution-diffusion cycles can be sustained over time which can lead to periodic aggregation patterns of metal-hydroxide colloids at a specific time. We also establish that for transition metal cations the precipitation-dissolution-diffusion process can couple with reversible redox reactions between the soluble and less soluble metal cations, which can affect the overall transport of banded aggregates of metal-hydroxide colloids and the growth and transformation of metal-hydroxides into crystalline oxides. If systemic feedback between different elementary processes is sustained over long durations, iron-oxide crystals of different chemical compositions and shapes aggregate in Liesegang patterns. This work demonstrates unequivocally that non-uniform deposition of metal oxides during corrosion can occur via strongly coupled solution reactions and transport processes, and not simply as a result of metallurgical non-uniformity and/or localized solution environments.

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.

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.

Capture heats up sharks.

Catch-and-release fishing is an important component of ecotourism industries and scientific research worldwide, but its total impact on animal physiology, health and survival is understudied for many species of fishes, particularly sharks. We combined biologging and blood chemistry to explore how this fisheries interaction influenced the physiology of two widely distributed, highly migratory shark species: the blue shark (Prionace glauca) and the tiger shark (Galeocerdo cuvier). Nineteen sharks were caught by drum line or rod-and-reel angling; subcutaneous body temperature measurements were taken immediately upon capture, with six individuals also providing subsequent subcutaneous body temperature measurements via biologging as they swam freely for several hours post-release. We found that short-term capture caused shark body temperature to increase significantly and rapidly, with increases of 0.6°C-2.7°C for blue sharks (mean, 1.2 ± 0.6°C) and 0.5°C-0.9°C for tiger sharks (mean, 0.7 ± 0.2°C) and with capture-induced heating rates of blue sharks averaging 0.3°C min-1 but as high as 0.8°C min-1. Blue shark body temperature was even higher deeper into the white muscle. These heating rates were three to eight times faster than maximum rates encountered by our biologging sharks swimming through thermally stratified waters and faster than most acute heating experiments conducted with ectotherms in laboratory experiments. Biologging data showed that body temperatures underwent gradual decline after release, returning to match water temperatures 10-40 mins post-release. Blood biochemistry showed variable lactate/glucose levels following capture; however, these concentrations were not correlated with the magnitude of body temperature increase, nor with body size or hooking time. These perturbations of the natural state could have immediate and longer-term effects on the welfare and ecology of sharks caught in catch-and-release fisheries and we encourage further study of the broader implications of this reported phenomenon.

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.

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.

Charge Storage in Graphene Oxide: Impact of the Cation on Ion Permeability and Interfacial Capacitance.

The charge storage and membrane applications of graphene oxide (GO) materials are dictated by its intrinsic material properties. Structure-function relationships correlating periodic parameters, such as the hydrated ion radius and ion-GO interactions, are currently lacking yet are needed to provide insight on the charge storage and ion transport mechanism. We report the use of scanning ion conductance microscopy to measure the ion permeability of GO films and evaluate its relationship with the measured capacitance. We demonstrate that species (namely K+) with strong electrostatic interactions with the oxygen functionalities of GO provide the benefit of higher capacitance but suffer from inhibited ion mobility due to constriction of the GO interlayer spacing.

Fish body sizes change with temperature but not all species shrink with warming.

Ectotherms generally shrink under experimental warming, but whether this pattern extends to wild populations is uncertain. We analysed ten million visual survey records, spanning the Australian continent and multiple decades and comprising the most common coastal reef fishes (335 species). We found that temperature indeed drives spatial and temporal changes in fish body size, but not consistently in the negative fashion expected. Around 55% of species were smaller in warmer waters (especially among small-bodied species), while 45% were bigger. The direction of a species' response to temperature through space was generally consistent with its response to temperature increase through time at any given location, suggesting that spatial trends could help forecast fish responses to long-term warming. However, temporal changes were about ten times faster than spatial trends (~4% versus ~40% body size change per 1 °C change through space and time, respectively). The rapid and variable responses of fish size to warming may herald unexpected impacts on ecosystem restructuring, with potentially greater consequences than if all species were shrinking.

Super-resolution Scanning Electrochemical Microscopy.

To achieve super-resolution scanning electrochemical microscopy (SECM), we must overcome the theoretical limitation associated with noncontact electrochemical imaging of surface-generated species. This is the requirement for mass transfer to the electrode, which gives rise to the diffusional broadening of surface features. In this work, a procedure is developed for overcoming this limitation and thus generating "super-resolved" images using point spread function (PSF)-based deconvolution, where the point conductor plays the same role as the point emitter in optical imaging. In contrast to previous efforts in SECM towards this goal, our method uses a finite element model to generate a pair of corresponding blurred and sharp images for PSF estimation, avoiding the need to perform parameter optimization for effective deconvolution. It can therefore be used for retroactive data treatment and an enhanced understanding of the structure-property relationships that SECM provides.

Effect of Substrate Permeability on Scanning Ion Conductance Microscopy: Uncertainty in Tip-Substrate Separation and Determination of Ionic Conductivity.

Composite electrodes can significantly improve the performance of an electrochemical device by maximizing surface area and active material loading. Typically, additives such as carbon are used to improve conductivity and a polymer is used as a binder, leading to a heterogeneous surface film with thickness on the order of 10s of micrometers. For such composite electrodes, good ionic conduction within the film is critical to capitalize on the increased loading of active material and surface area. Ionic conductivity within a film can be tricky to measure directly, and homogenization models based on porosity are often used as a proxy. SICM has traditionally been a topography-mapping microscopy method for which we here outline a new function and demonstrate its capacity for measuring ion conductivity within a lithium-ion battery film.