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.

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.

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.

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.

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.

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.

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.

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.

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.

Evaluating the Use of Edge Detection in Extracting Feature Size from Scanning Electrochemical Microscopy Images.

The edge of a reactive or topographical feature is hard to estimate from feedback-based scanning electrochemical microscopy due to diffusional blurring, but is crucial to determining the accurate size and shape of these features. In this work, numerical simulations are used to demonstrate that the inflection point in a 1D line scan corresponds well to the true feature edge. This approach is then applied in 2D using the Canny algorithm to experimental images of two model substrates and a biological sample. This approach circumvents the need for aligning the imaged region between separate microscopy techniques, reveals hidden details embedded in SECM images, and allows individual features to be separated from their background more effectively.

Redox-Triggered Disassembly of Nanosized Liposomes Containing Ferrocene-Appended Amphiphiles.

We report a redox-responsive liposomal system capable of oxidatively triggered disassembly. We describe the synthesis, electrochemical characterization, and incorporation into vesicles of an alternative redox lipid with significantly improved synthetic efficiency and scalability compared to a ferrocene-appended phospholipid previously employed by our group in giant vesicles. The redox-triggered disassembly of both redox lipids is examined in nanosized liposomes as well as the influence of cholesterol mole fraction on liposome disassembly and suitability of various chemical oxidants for  in vitro disassembly experiments. Electronic structure density functional theory calculations of membrane-embedded ferrocenes are provided to characterize the role of charge redistribution in the initial stages of the disassembly process.

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.

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

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

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.

How strongly does diet variation explain variation in isotope values of animal consumers?

Analysis of stable isotopes in consumers is used commonly to study their ecological and/or environmental niche. There is, however, considerable debate regarding how isotopic values relate to diet and how other sources of variation confound this link, which can undermine the utility. From the analysis of a simple, but general, model of isotopic incorporation in consumer organisms, we examine the relationship between isotopic variance among individuals, and diet variability within a consumer population. We show that variance in consumer isotope values is directly proportional to variation in diet (through Simpson indices), to the number of isotopically distinct food sources in the diet, and to the baseline variation within and among the isotope values of the food sources. Additionally, when considering temporal diet variation within a consumer we identify the interplay between diet turnover rates and tissue turnover rates that controls the sensitivity of stable isotopes to detect diet variation. Our work demonstrates that variation in the stable isotope values of consumers reflect variation in their diet. This relationship, however, can be confounded with other factors to the extent that they may mask the signal coming from diet. We show how simple quantitative corrections can recover a direct 1:1 correlation in some situations, and in others we can adjust our interpretation in light of the new understanding arising from our models. Our framework provides guidance for the design and analysis of empirical studies where the goal is to infer niche width from stable isotope data.

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.