Linking vertical movements of large pelagic predators with distribution patterns of biomass in the open ocean.

Many predator species make regular excursions from near-surface waters to the twilight (200 to 1,000 m) and midnight (1,000 to 3,000 m) zones of the deep pelagic ocean. While the occurrence of significant vertical movements into the deep ocean has evolved independently across taxonomic groups, the functional role(s) and ecological significance of these movements remain poorly understood. Here, we integrate results from satellite tagging efforts with model predictions of deep prey layers in the North Atlantic Ocean to determine whether prey distributions are correlated with vertical habitat use across 12 species of predators. Using 3D movement data for 344 individuals who traversed nearly 1.5 million km of pelagic ocean in [Formula: see text]42,000 d, we found that nearly every tagged predator frequented the twilight zone and many made regular trips to the midnight zone. Using a predictive model, we found clear alignment of predator depth use with the expected location of deep pelagic prey for at least half of the predator species. We compared high-resolution predator data with shipboard acoustics and selected representative matches that highlight the opportunities and challenges in the analysis and synthesis of these data. While not all observed behavior was consistent with estimated prey availability at depth, our results suggest that deep pelagic biomass likely has high ecological value for a suite of commercially important predators in the open ocean. Careful consideration of the disruption to ecosystem services provided by pelagic food webs is needed before the potential costs and benefits of proceeding with extractive activities in the deep ocean can be evaluated.

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.

Building use-inspired species distribution models: Using multiple data types to examine and improve model performance.

Species distribution models (SDMs) are becoming an important tool for marine conservation and management. Yet while there is an increasing diversity and volume of marine biodiversity data for training SDMs, little practical guidance is available on how to leverage distinct data types to build robust models. We explored the effect of different data types on the fit, performance and predictive ability of SDMs by comparing models trained with four data types for a heavily exploited pelagic fish, the blue shark (Prionace glauca), in the Northwest Atlantic: two fishery dependent (conventional mark-recapture tags, fisheries observer records) and two fishery independent (satellite-linked electronic tags, pop-up archival tags). We found that all four data types can result in robust models, but differences among spatial predictions highlighted the need to consider ecological realism in model selection and interpretation regardless of data type. Differences among models were primarily attributed to biases in how each data type, and the associated representation of absences, sampled the environment and summarized the resulting species distributions. Outputs from model ensembles and a model trained on all pooled data both proved effective for combining inferences across data types and provided more ecologically realistic predictions than individual models. Our results provide valuable guidance for practitioners developing SDMs. With increasing access to diverse data sources, future work should further develop truly integrative modeling approaches that can explicitly leverage the strengths of individual data types while statistically accounting for limitations, such as sampling biases.

Direct measurement of cruising and burst swimming speeds of the shortfin mako shark (Isurus oxyrinchus) with estimates of field metabolic rate.

The shortfin mako shark is a large-bodied pursuit predator thought to be capable of the highest swimming speeds of any elasmobranch and potentially one of the highest energetic demands of any marine fish. Nonetheless, few direct speed measurements have been reported for this species. Here, animal-borne bio-loggers attached to two mako sharks were used to provide direct measurements of swimming speeds, kinematics and thermal physiology. Mean sustained (cruising) speed was 0.90 m s-1 (±0.07 s.d.) with a mean tail-beat frequency (TBF) of 0.51 Hz (±0.16 s.d.). The maximum burst speed recorded was 5.02 m s-1 (TBFmax = 3.65 Hz) from a 2 m long female. Burst swimming was sustained for 14 s (mean speed = 2.38 m s-1 ), leading to a 0.24°C increase in white muscle temperature in the 12.5 min after the burst. Routine field metabolic rate was estimated at 185.2 mg O2 kg-1 h-1 (at 18°C ambient temperature). Gliding behaviour (zero TBF) was more frequently observed after periods of high activity, especially after capture when internal (white muscle) temperature approached 21°C (ambient temperature: 18.3°C), indicating gliding probably functions as an energy recovery mechanism and limits further metabolic heat production. The results show shortfin mako sharks generally cruise at speeds similar to other endothermic fish - but faster than ectothermic sharks - with the maximum recorded burst speed being among the highest so far directly measured among sharks, tunas and billfishes. This newly recorded high-oxygen-demand performance of mako sharks suggests it may be particularly vulnerable to habitat loss due to climate-driven ocean deoxygenation.

Circles in the sea: annual courtship "torus" behaviour of basking sharks Cetorhinus maximus identified in the eastern North Atlantic Ocean.

Groups of basking sharks engaged in circling behaviour are rarely observed, and their function remains enigmatic in the absence of detailed observations. Here, underwater and aerial video recordings of multiple circling groups of basking sharks during late summer (August and September 2016-2021) in the eastern North Atlantic Ocean showed groups numbering between 6 and 23 non-feeding individuals of both sexes. Sharks swam slowly in a rotating "torus" (diameter range: 17-39 m), with individuals layered vertically from the surface to a maximum depth of 16 m. Within a torus, sharks engaged in close-following, echelon, close-flank approach or parallel-swimming behaviours. Measured shark total body lengths were 5.4-9.5 m (mean LT : 7.3 m ± 0.9 s.d.; median: 7.2 m, n = 27), overlapping known lengths of sexually mature males and females. Males possessed large claspers with abrasions that were also observed on female pectoral fins. Female body colouration was paler than that of males, similar to colour changes observed during courtship and mating in other shark species. Individuals associated with most other members rapidly (within minutes), indicating toroidal behaviours facilitate multiple interactions. Sharks interacted through fin-fin and fin-body contacts, rolling to expose the ventral surfaces to following sharks, and breaching behaviour. Toruses formed in late summer when feeding aggregations in zooplankton-rich thermal fronts switched to non-feeding following and circling behaviours. Collectively, the observations explain a courtship function for toruses. This study highlights northeast Atlantic coastal waters as a critical habitat supporting courtship reproductive behaviour of endangered basking sharks, the first such habitat identified for this species globally.

Meta-Fish-Lib: A generalised, dynamic DNA reference library pipeline for metabarcoding of fishes.

The accuracy and reliability of DNA metabarcoding analyses depend on the breadth and quality of the reference libraries that underpin them. However, there are limited options available to obtain and curate the huge volumes of sequence data that are available on public repositories such as NCBI and BOLD. Here, we provide a pipeline to download, clean and annotate mitochondrial DNA sequence data for a given list of fish species. Features of this pipeline include (a) support for multiple metabarcode markers; (b) searches on species synonyms and taxonomic name validation; (c) phylogeny assisted quality control for identification and removal of misannotated sequences; (d) automatically generated coverage reports for each new GenBank release update; and (e) citable, versioned DOIs. As an example we provide a ready-to-use curated reference library for the marine and freshwater fishes of the U.K. To augment this reference library for environmental DNA metabarcoding specifically, we generated 241 new MiFish-12S sequences for 88 U.K. marine species, and make available new primer sets useful for sequencing these. This brings the coverage of common U.K. species for the MiFish-12S fragment to 93%, opening new avenues for scaling up fish metabarcoding across wide spatial gradients. The Meta-Fish-Lib reference library and pipeline is hosted at https://github.com/genner-lab/meta-fish-lib.

Rationalizing spatial exploration patterns of wild animals and humans through a temporal discounting framework.

Understanding the exploration patterns of foragers in the wild provides fundamental insight into animal behavior. Recent experimental evidence has demonstrated that path lengths (distances between consecutive turns) taken by foragers are well fitted by a power law distribution. Numerous theoretical contributions have posited that "Lévy random walks"-which can produce power law path length distributions-are optimal for memoryless agents searching a sparse reward landscape. It is unclear, however, whether such a strategy is efficient for cognitively complex agents, from wild animals to humans. Here, we developed a model to explain the emergence of apparent power law path length distributions in animals that can learn about their environments. In our model, the agent's goal during search is to build an internal model of the distribution of rewards in space that takes into account the cost of time to reach distant locations (i.e., temporally discounting rewards). For an agent with such a goal, we find that an optimal model of exploration in fact produces hyperbolic path lengths, which are well approximated by power laws. We then provide support for our model by showing that humans in a laboratory spatial exploration task search space systematically and modify their search patterns under a cost of time. In addition, we find that path length distributions in a large dataset obtained from free-ranging marine vertebrates are well described by our hyperbolic model. Thus, we provide a general theoretical framework for understanding spatial exploration patterns of cognitively complex foragers.

Ocean-wide tracking of pelagic sharks reveals extent of overlap with longline fishing hotspots.

Overfishing is arguably the greatest ecological threat facing the oceans, yet catches of many highly migratory fishes including oceanic sharks remain largely unregulated with poor monitoring and data reporting. Oceanic shark conservation is hampered by basic knowledge gaps about where sharks aggregate across population ranges and precisely where they overlap with fishers. Using satellite tracking data from six shark species across the North Atlantic, we show that pelagic sharks occupy predictable habitat hotspots of high space use. Movement modeling showed sharks preferred habitats characterized by strong sea surface-temperature gradients (fronts) over other available habitats. However, simultaneous Global Positioning System (GPS) tracking of the entire Spanish and Portuguese longline-vessel fishing fleets show an 80% overlap of fished areas with hotspots, potentially increasing shark susceptibility to fishing exploitation. Regions of high overlap between oceanic tagged sharks and longliners included the North Atlantic Current/Labrador Current convergence zone and the Mid-Atlantic Ridge southwest of the Azores. In these main regions, and subareas within them, shark/vessel co-occurrence was spatially and temporally persistent between years, highlighting how broadly the fishing exploitation efficiently "tracks" oceanic sharks within their space-use hotspots year-round. Given this intense focus of longliners on shark hotspots, our study argues the need for international catch limits for pelagic sharks and identifies a future role of combining fine-scale fish and vessel telemetry to inform the ocean-scale management of fisheries.

Hierarchical random walks in trace fossils and the origin of optimal search behavior.

Efficient searching is crucial for timely location of food and other resources. Recent studies show that diverse living animals use a theoretically optimal scale-free random search for sparse resources known as a Lévy walk, but little is known of the origins and evolution of foraging behavior and the search strategies of extinct organisms. Here, using simulations of self-avoiding trace fossil trails, we show that randomly introduced strophotaxis (U-turns)--initiated by obstructions such as self-trail avoidance or innate cueing--leads to random looping patterns with clustering across increasing scales that is consistent with the presence of Lévy walks. This predicts that optimal Lévy searches may emerge from simple behaviors observed in fossil trails. We then analyzed fossilized trails of benthic marine organisms by using a novel path analysis technique and find the first evidence, to our knowledge, of Lévy-like search strategies in extinct animals. Our results show that simple search behaviors of extinct animals in heterogeneous environments give rise to hierarchically nested Brownian walk clusters that converge to optimal Lévy patterns. Primary productivity collapse and large-scale food scarcity characterizing mass extinctions evident in the fossil record may have triggered adaptation of optimal Lévy-like searches. The findings suggest that Lévy-like behavior has been used by foragers since at least the Eocene but may have a more ancient origin, which might explain recent widespread observations of such patterns among modern taxa.

Acoustic telemetry and network analysis reveal the space use of multiple reef predators and enhance marine protected area design.

Marine protected areas (MPAs) are commonly employed to protect ecosystems from threats like overfishing. Ideally, MPA design should incorporate movement data from multiple target species to ensure sufficient habitat is protected. We used long-term acoustic telemetry and network analysis to determine the fine-scale space use of five shark and one turtle species at a remote atoll in the Seychelles, Indian Ocean, and evaluate the efficacy of a proposed MPA. Results revealed strong, species-specific habitat use in both sharks and turtles, with corresponding variation in MPA use. Defining the MPA's boundary from the edge of the reef flat at low tide instead of the beach at high tide (the current best in Seychelles) significantly increased the MPA's coverage of predator movements by an average of 34%. Informed by these results, the larger MPA was adopted by the Seychelles government, demonstrating how telemetry data can improve shark spatial conservation by affecting policy directly.

Environmental context explains Lévy and Brownian movement patterns of marine predators.

An optimal search theory, the so-called Lévy-flight foraging hypothesis, predicts that predators should adopt search strategies known as Lévy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey. Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Lévy behaviour has recently been questioned. Consequently, whether foragers exhibit Lévy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory's central predictions. Here we use maximum-likelihood methods to test for Lévy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Lévy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Lévy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Lévy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Lévy-flight foraging hypothesis, supporting the contention that organism search strategies naturally evolved in such a way that they exploit optimal Lévy patterns.

Foraging success of biological Lévy flights recorded in situ.

It is an open question how animals find food in dynamic natural environments where they possess little or no knowledge of where resources are located. Foraging theory predicts that in environments with sparsely distributed target resources, where forager knowledge about resources' locations is incomplete, Lévy flight movements optimize the success of random searches. However, the putative success of Lévy foraging has been demonstrated only in model simulations. Here, we use high-temporal-resolution Global Positioning System (GPS) tracking of wandering (Diomedea exulans) and black-browed albatrosses (Thalassarche melanophrys) with simultaneous recording of prey captures, to show that both species exhibit Lévy and Brownian movement patterns. We find that total prey masses captured by wandering albatrosses during Lévy movements exceed daily energy requirements by nearly fourfold, and approached yields by Brownian movements in other habitats. These results, together with our reanalysis of previously published albatross data, overturn the notion that albatrosses do not exhibit Lévy patterns during foraging, and demonstrate that Lévy flights of predators in dynamic natural environments present a beneficial alternative strategy to simple, spatially intensive behaviors. Our findings add support to the possibility that biological Lévy flight may have naturally evolved as a search strategy in response to sparse resources and scant information.

Scaling laws of ambush predator 'waiting' behaviour are tuned to a common ecology.

The decisions animals make about how long to wait between activities can determine the success of diverse behaviours such as foraging, group formation or risk avoidance. Remarkably, for diverse animal species, including humans, spontaneous patterns of waiting times show random 'burstiness' that appears scale-invariant across a broad set of scales. However, a general theory linking this phenomenon across the animal kingdom currently lacks an ecological basis. Here, we demonstrate from tracking the activities of 15 sympatric predator species (cephalopods, sharks, skates and teleosts) under natural and controlled conditions that bursty waiting times are an intrinsic spontaneous behaviour well approximated by heavy-tailed (power-law) models over data ranges up to four orders of magnitude. Scaling exponents quantifying ratios of frequent short to rare very long waits are species-specific, being determined by traits such as foraging mode (active versus ambush predation), body size and prey preference. A stochastic-deterministic decision model reproduced the empirical waiting time scaling and species-specific exponents, indicating that apparently complex scaling can emerge from simple decisions. Results indicate temporal power-law scaling is a behavioural 'rule of thumb' that is tuned to species' ecological traits, implying a common pattern may have naturally evolved that optimizes move-wait decisions in less predictable natural environments.

Optimal foraging strategies: Lévy walks balance searching and patch exploitation under a very broad range of conditions.

While evidence for optimal random search patterns, known as Lévy walks, in empirical movement data is mounting for a growing list of taxa spanning motile cells to humans, there is still much debate concerning the theoretical generality of Lévy walk optimisation. Here, using a new and robust simulation environment, we investigate in the most detailed study to date (24×10(6) simulations) the foraging and search efficiencies of 2-D Lévy walks with a range of exponents, target resource distributions and several competing models. We find strong and comprehensive support for the predictions of the Lévy flight foraging hypothesis and in particular for the optimality of inverse square distributions of move step-lengths across a much broader range of resource densities and distributions than previously realised. Further support for the evolutionary advantage of Lévy walk movement patterns is provided by an investigation into the 'feast and famine' effect, with Lévy foragers in heterogeneous environments experiencing fewer long 'famines' than other types of searchers. Therefore overall, optimal Lévy foraging results in more predictable resources in unpredictable environments.

Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark.

Top predators inhabiting a dynamic environment, such as coastal waters, should theoretically possess sufficient cognitive ability to allow successful foraging despite unpredictable sensory stimuli. The cognition-related hunting abilities of marine mammals have been widely demonstrated. Having been historically underestimated, teleost cognitive abilities have also now been significantly demonstrated. Conversely, the abilities of elasmobranchs have received little attention, despite many species possessing relatively large brains comparable to some mammals. The need to determine what, if any, cognitive ability these globally distributed, apex predators are endowed with has been highlighted recently by questions arising from environmental assessments, specifically whether they are able to learn to distinguish between anthropogenic electric fields and prey bioelectric fields. We therefore used electroreceptive foraging behaviour in a model species, Scyliorhinus canicula (small-spotted catshark), to determine cognitive ability by analysing whether elasmobranchs are able to learn to improve foraging efficiency and remember learned behavioural adaptations. Positive reinforcement, operant conditioning was used to study catshark foraging behaviour towards artificial, prey-type electric fields (Efields). Catsharks rewarded with food for responding to Efields throughout experimental weeks were compared with catsharks that were not rewarded for responding in order to assess behavioural adaptation via learning ability. Experiments were repeated after a 3-week interval with previously rewarded catsharks this time receiving no reward and vice versa to assess memory ability. Positive reinforcement markedly and rapidly altered catshark foraging behaviour. Rewarded catsharks exhibited significantly more interest in the electrical stimulus than unrewarded catsharks. Furthermore, they improved their foraging efficiency over time by learning to locate and bite the electrodes to gain food more quickly. In contrast, unrewarded catsharks showed some habituation, whereby their responses to the electrodes abated and eventually entirely ceased, though they generally showed no changes in most foraging parameters. Behavioural adaptations were not retained after the interval suggesting learned behaviour was not memorised beyond the interval. Sequences of individual catshark search paths clearly illustrated learning and habituation behavioural adaptation. This study demonstrated learning and habituation occurring after few foraging events and a memory window of between 12 h and 3 weeks. These cognitive abilities are discussed in relation to diet, habitat, ecology and anthropogenic Efield sources.

Scaling laws of marine predator search behaviour.

Many free-ranging predators have to make foraging decisions with little, if any, knowledge of present resource distribution and availability. The optimal search strategy they should use to maximize encounter rates with prey in heterogeneous natural environments remains a largely unresolved issue in ecology. Lévy walks are specialized random walks giving rise to fractal movement trajectories that may represent an optimal solution for searching complex landscapes. However, the adaptive significance of this putative strategy in response to natural prey distributions remains untested. Here we analyse over a million movement displacements recorded from animal-attached electronic tags to show that diverse marine predators-sharks, bony fishes, sea turtles and penguins-exhibit Lévy-walk-like behaviour close to a theoretical optimum. Prey density distributions also display Lévy-like fractal patterns, suggesting response movements by predators to prey distributions. Simulations show that predators have higher encounter rates when adopting Lévy-type foraging in natural-like prey fields compared with purely random landscapes. This is consistent with the hypothesis that observed search patterns are adapted to observed statistical patterns of the landscape. This may explain why Lévy-like behaviour seems to be widespread among diverse organisms, from microbes to humans, as a 'rule' that evolved in response to patchy resource distributions.

Shark conservation requires mortality-limiting regulations amid global change.

Despite anti-finning laws aimed at conserving sharks, Worm et al. have revealed that global shark mortality rates have surprisingly risen over the past decade, driven in large part by increased demand for meat. Here, we discuss the importance of this study, underscoring the need for broader regulations addressing overall shark mortality amid threats from global change.