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.

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.

Global collision-risk hotspots of marine traffic and the world's largest fish, the whale shark.

Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks' horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (>300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial "cryptic" lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.

Predator-prey landscapes of large sharks and game fishes in the Florida Keys.

Interspecific interactions can play an essential role in shaping wildlife populations and communities. To date, assessments of interspecific interactions, and more specifically predator-prey dynamics, in aquatic systems over broad spatial and temporal scales (i.e., hundreds of kilometers and multiple years) are rare due to constraints on our abilities to measure effectively at those scales. We applied new methods to identify space-use overlap and potential predation risk to Atlantic tarpon (Megalops atlanticus) and permit (Trachinotus falcatus) from two known predators, great hammerhead (Sphyrna mokarran) and bull (Carcharhinus leucas) sharks, over a 3-year period using acoustic telemetry in the coastal region of the Florida Keys (USA). By examining spatiotemporal overlap, as well as the timing and order of arrival at specific locations compared to random chance, we show that potential predation risk from great hammerhead and bull sharks to Atlantic tarpon and permit are heterogeneous across the Florida Keys. Additionally, we find that predator encounter rates with these game fishes are elevated at specific locations and times, including a prespawning aggregation site in the case of Atlantic tarpon. Further, using machine learning algorithms, we identify environmental variability in overlap between predators and their potential prey, including location, habitat, time of year, lunar cycle, depth, and water temperature. These predator-prey landscapes provide insights into fundamental ecosystem function and biological conservation, especially in the context of emerging fishery-related depredation issues in coastal marine ecosystems.

Pieces in a global puzzle: Population genetics at two whale shark aggregations in the western Indian Ocean.

The whale shark Rhincodon typus is found throughout the world's tropical and warm-temperate ocean basins. Despite their broad physical distribution, research on the species has been concentrated at a few aggregation sites. Comparing DNA sequences from sharks at different sites can provide a demographically neutral understanding of the whale shark's global ecology. Here, we created genetic profiles for 84 whale sharks from the Saudi Arabian Red Sea and 72 individuals from the coast of Tanzania using a combination of microsatellite and mitochondrial sequences. These two sites, separated by approximately 4500 km (shortest over-water distance), exhibit markedly different population demographics and behavioral ecologies. Eleven microsatellite DNA markers revealed that the two aggregation sites have similar levels of allelic richness and appear to be derived from the same source population. We sequenced the mitochondrial control region to produce multiple global haplotype networks (based on different alignment methodologies) that were broadly similar to each other in terms of population structure but suggested different demographic histories. Data from both microsatellite and mitochondrial markers demonstrated the stability of genetic diversity within the Saudi Arabian aggregation site throughout the sampling period. These results contrast previously measured declines in diversity at Ningaloo Reef, Western Australia. Mapping the geographic distribution of whale shark lineages provides insight into the species' connectivity and can be used to direct management efforts at both local and global scales. Similarly, understanding historical fluctuations in whale shark abundance provides a baseline by which to assess current trends. Continued development of new sequencing methods and the incorporation of genomic data could lead to considerable advances in the scientific understanding of whale shark population ecology and corresponding improvements to conservation policy.

Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea.

Whale sharks (Rhincodon typus) are typically dispersed throughout their circumtropical range, but the species is also known to aggregate in specific coastal areas. Accurate site descriptions associated with these aggregations are essential for the conservation of R. typus, an Endangered species. Although aggregations have become valuable hubs for research, most site descriptions rely heavily on sightings data. In the present study, visual census, passive acoustic monitoring, and long range satellite telemetry were combined to track the movements of R. typus from Shib Habil, a reef-associated aggregation site in the Red Sea. An array of 63 receiver stations was used to record the presence of 84 acoustically tagged sharks (35 females, 37 males, 12 undetermined) from April 2010 to May 2016. Over the same period, identification photos were taken for 76 of these tagged individuals and 38 were fitted with satellite transmitters. In total of 37,461 acoustic detections, 210 visual encounters, and 33 satellite tracks were analyzed to describe the sharks' movement ecology. The results demonstrate that the aggregation is seasonal, mostly concentrated on the exposed side of Shib Habil, and seems to attract sharks of both sexes in roughly equal numbers. The combined methodologies also tracked 15 interannual homing-migrations, demonstrating that many sharks leave the area before returning in later years. When compared to acoustic studies from other aggregations, these results demonstrate that R. typus exhibits diverse, site-specific ecologies across its range. Sightings-independent data from acoustic telemetry and other sources are an effective means of validating more common visual surveys.

Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone.

Mesoscale eddies are critical components of the ocean's "internal weather" system. Mixing and stirring by eddies exerts significant control on biogeochemical fluxes in the open ocean, and eddies may trap distinctive plankton communities that remain coherent for months and can be transported hundreds to thousands of kilometers. Debate regarding how and why predators use fronts and eddies, for example as a migratory cue, enhanced forage opportunities, or preferred thermal habitat, has been ongoing since the 1950s. The influence of eddies on the behavior of large pelagic fishes, however, remains largely unexplored. Here, we reconstruct movements of a pelagic predator, the blue shark (Prionace glauca), in the Gulf Stream region using electronic tags, earth-observing satellites, and data-assimilating ocean forecasting models. Based on >2,000 tracking days and nearly 500,000 high-resolution time series measurements collected by 15 instrumented individuals, we show that blue sharks seek out the interiors of anticyclonic eddies where they dive deep while foraging. Our observations counter the existing paradigm that anticyclonic eddies are unproductive ocean "deserts" and suggest anomalously warm temperatures in these features connect surface-oriented predators to the most abundant fish community on the planet in the mesopelagic. These results also shed light on the ecosystem services provided by mesopelagic prey. Careful consideration will be needed before biomass extraction from the ocean twilight zone to avoid interrupting a key link between planktonic production and top predators. Moreover, robust associations between targeted fish species and oceanographic features increase the prospects for effective dynamic ocean management.

Mesoscale eddies influence the movements of mature female white sharks in the Gulf Stream and Sargasso Sea.

Satellite-tracking of mature white sharks (Carcharodon carcharias) has revealed open-ocean movements spanning months and covering tens of thousands of kilometers. But how are the energetic demands of these active apex predators met as they leave coastal areas with relatively high prey abundance to swim across the open ocean through waters often characterized as biological deserts? Here we investigate mesoscale oceanographic variability encountered by two white sharks as they moved through the Gulf Stream region and Sargasso Sea in the North Atlantic Ocean. In the vicinity of the Gulf Stream, the two mature female white sharks exhibited extensive use of the interiors of clockwise-rotating anticyclonic eddies, characterized by positive (warm) temperature anomalies. One tagged white shark was also equipped with an archival tag that indicated this individual made frequent dives to nearly 1,000 m in anticyclones, where it was presumably foraging on mesopelagic prey. We propose that warm temperature anomalies in anticyclones make prey more accessible and energetically profitable to adult white sharks in the Gulf Stream region by reducing the physiological costs of thermoregulation in cold water. The results presented here provide valuable new insight into open ocean habitat use by mature, female white sharks that may be applicable to other large pelagic predators.

Social Network Analysis Reveals Potential Fission-Fusion Behavior in a Shark.

Complex social networks and behaviors are difficult to observe for free-living marine species, especially those that move great distances. Using implanted acoustic transceivers to study the inter- and intraspecific interactions of sand tiger sharks Carcharias taurus, we observed group behavior that has historically been associated with higher order mammals. We found evidence strongly suggestive of fission-fusion behavior, or changes in group size and composition of sand tigers, related to five behavioral modes (summering, south migration, community bottleneck, dispersal, north migration). Our study shows sexually dimorphic behavior during migration, in addition to presenting evidence of a potential solitary phase for these typically gregarious sharks. Sand tigers spent up to 95 consecutive and 335 cumulative hours together, with the strongest relationships occurring between males. Species that exhibit fission-fusion group dynamics pose a particularly challenging issue for conservation and management because changes in group size and composition affect population estimates and amplify anthropogenic impacts.

Movement patterns of juvenile whale sharks tagged at an aggregation site in the Red Sea.

Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009-2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5-7 m total length with a sex ratio of approximately 1∶1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.

Extreme diving behaviour in devil rays links surface waters and the deep ocean.

Ecological connections between surface waters and the deep ocean remain poorly studied despite the high biomass of fishes and squids residing at depths beyond the euphotic zone. These animals likely support pelagic food webs containing a suite of predators that include commercially important fishes and marine mammals. Here we deploy pop-up satellite archival transmitting tags on 15 Chilean devil rays (Mobula tarapacana) in the central North Atlantic Ocean, which provide movement patterns of individuals for up to 9 months. Devil rays were considered surface dwellers but our data reveal individuals descending at speeds up to 6.0 m s(-1) to depths of almost 2,000 m and water temperatures <4 °C. The shape of the dive profiles suggests that the rays are foraging at these depths in deep scattering layers. Our results provide evidence of an important link between predators in the surface ocean and forage species occupying pelagic habitats below the euphotic zone in ocean ecosystems.

Seasonal distribution and historic trends in abundance of white sharks, Carcharodon carcharias, in the western North Atlantic Ocean.

Despite recent advances in field research on white sharks (Carcharodon carcharias) in several regions around the world, opportunistic capture and sighting records remain the primary source of information on this species in the northwest Atlantic Ocean (NWA). Previous studies using limited datasets have suggested a precipitous decline in the abundance of white sharks from this region, but considerable uncertainty in these studies warrants additional investigation. This study builds upon previously published data combined with recent unpublished records and presents a synthesis of 649 confirmed white shark records from the NWA compiled over a 210-year period (1800-2010), resulting in the largest white shark dataset yet compiled from this region. These comprehensive records were used to update our understanding of their seasonal distribution, relative abundance trends, habitat use, and fisheries interactions. All life stages were present in continental shelf waters year-round, but median latitude of white shark occurrence varied seasonally. White sharks primarily occurred between Massachusetts and New Jersey during summer and off Florida during winter, with broad distribution along the coast during spring and fall. The majority of fishing gear interactions occurred with rod and reel, longline, and gillnet gears. Historic abundance trends from multiple sources support a significant decline in white shark abundance in the 1970s and 1980s, but there have been apparent increases in abundance since the 1990s when a variety of conservation measures were implemented. Though the white shark's inherent vulnerability to exploitation warrants continued protections, our results suggest a more optimistic outlook for the recovery of this iconic predator in the Atlantic.

Diving behavior of the reef manta ray links coral reefs with adjacent deep pelagic habitats.

Recent successful efforts to increase protection for manta rays has highlighted the lack of basic ecological information, including vertical and horizontal movement patterns, available for these species. We deployed pop-up satellite archival transmitting tags on nine reef manta rays, Manta alfredi, to determine diving behaviors and vertical habitat use. Transmitted and archived data were obtained from seven tagged mantas over deployment periods of 102-188 days, including three recovered tags containing 2.6 million depth, temperature, and light level data points collected every 10 or 15 seconds. Mantas frequented the upper 10 m during daylight hours and tended to occupy deeper water throughout the night. Six of the seven individuals performed a cumulative 76 deep dives (>150 m) with one individual reaching 432 m, extending the known depth range of this coastal, reef-oriented species and confirming its role as an ecological link between epipelagic and mesopelagic habitats. Mean vertical velocities calculated from high-resolution dive data (62 dives >150 m) from three individuals suggested that mantas may use gliding behavior during travel and that this behavior may prove more efficient than continuous horizontal swimming. The behaviors in this study indicate manta rays provide a previously unknown link between the epi- and mesopelagic layers of an extremely oligotrophic marine environment and provide evidence of a third marine species that utilizes gliding to maximize movement efficiency.

Vertebral bomb radiocarbon suggests extreme longevity in white sharks.

Conservation and management efforts for white sharks (Carcharodon carcharias) remain hampered by a lack of basic demographic information including age and growth rates. Sharks are typically aged by counting growth bands sequentially deposited in their vertebrae, but the assumption of annual deposition of these band pairs requires testing. We compared radiocarbon (Δ(14)C) values in vertebrae from four female and four male white sharks from the northwestern Atlantic Ocean (NWA) with reference chronologies documenting the marine uptake of (14)C produced by atmospheric testing of thermonuclear devices to generate the first radiocarbon age estimates for adult white sharks. Age estimates were up to 40 years old for the largest female (fork length [FL]: 526 cm) and 73 years old for the largest male (FL: 493 cm). Our results dramatically extend the maximum age and longevity of white sharks compared to earlier studies, hint at possible sexual dimorphism in growth rates, and raise concerns that white shark populations are considerably more sensitive to human-induced mortality than previously thought.

The physiological response of the Caribbean reef shark (Carcharhinus perezi) to longline capture.

Longline fishing is the most common elasmobranch capture method around the world, yet the physiological consequences of this technique are poorly understood. To quantify the sub-lethal effects of longline capture in the commonly exploited Caribbean reef shark (Carcharhinus perezi), 37 individuals were captured using standard, mid-water longlines. Hook timers provided hooking duration to the nearest minute. Once sharks were landed, blood samples were taken and used to measure a suite of physiological parameters. Control data were obtained by sampling an additional three unrestrained Caribbean reef sharks underwater at an established shark feeding site. The greatest level of physiological disruption occurred after 120-180min of hooking, whereas sharks exposed to minimal and maximal hook durations exhibited the least disturbed blood chemistry. Significant relationships were established between hooking duration and blood pH, pCO(2), lactate, glucose, plasma calcium and plasma potassium. Longline capture appears more benign than other methods assessed to date, causing a shift in the stress response from acute at the onset of capture to a sub-acute regime as the capture event progresses, apparently facilitating a degree of physiological recovery. Continued investigation into the physiological response of elasmobranchs to longline capture is vital for the effective management of such fisheries.

The physiological response to anthropogenic stressors in marine elasmobranch fishes: a review with a focus on the secondary response.

Elasmobranchs (sharks, rays, and skates) are currently facing substantial anthropogenic threats, which expose them to acute and chronic stressors that may exceed in severity and/or duration those typically imposed by natural events. To date, the number of directed studies on the response of elasmobranch fishes to acute and chronic stress are greatly exceeded by those related to teleosts. Of the limited number of studies conducted to date, most have centered on sharks; batoids are poorly represented. Like teleosts, sharks exhibit primary and secondary responses to stress that are manifested in their blood biochemistry. The former is characterized by immediate and profound increases in circulating catecholamines and corticosteroids, which are thought to mobilize energy reserves and maintain oxygen supply and osmotic balance. Mediated by these primary responses, the secondary effects of stress in elasmobranchs include hyperglycemia, acidemia resulting from metabolic and respiratory acidoses, and profound disturbances to ionic, osmotic, and fluid volume homeostasis. The nature and magnitude of these secondary effects are species-specific and may be tightly linked to metabolic scope and thermal physiology as well as the type and duration of the stressor. In fishes, acute and chronic stressors can incite a tertiary response, which involves physiological changes at the organismal level, thereby impacting growth rates, reproductive outputs or investments, and disease resistance. Virtually no studies to date have been conducted on the tertiary stress response in elasmobranchs. Given the diversity of elasmobranchs, additional studies that characterize the nature, magnitude, and consequences of physiological stress over a broad spectrum of stressors are essential for the development of conservation measures. Additional studies on the primary, secondary, and tertiary stress response in elasmobranchs are warranted, with particular emphasis on expanding the range of species and stressors examined. Future studies should move beyond simply studying the effects of known stressors and focus on the underlying physiological mechanisms. Such studies should include the coupling of stress indicators with quantifiable aspects of the stressor, which will allow researchers to test hypotheses on survivorship and, ultimately, derive models that effectively link physiology to mortality. Studies of this nature are essential for decision-making that will result in the effective management and conservation of these species.

Transequatorial migrations by basking sharks in the western Atlantic Ocean.

The world's second largest fish, the basking shark (Cetorhinus maximus), is broadly distributed in boreal to warm temperate latitudes of the Atlantic and Pacific oceans from shallow coastal waters to the open ocean. Previous satellite archival tagging in the North Atlantic has shown that basking sharks move seasonally, are often associated with productive frontal zones, and may make occasional dives to mesopelagic depths. However, basking sharks are thought to be restricted to temperate latitudes, and the extent to which they exploit deeper-water habitat remains enigmatic. Via satellite archival tags and a novel geolocation technique, we demonstrate here that basking sharks are seasonal migrants to mesopelagic tropical waters. Tagged sharks moved from temperate feeding areas off the coast of southern New England to the Bahamas, the Caribbean Sea, and onward to the coast of South America and into the Southern Hemisphere. When in these areas, basking sharks descended to mesopelagic depths and in some cases remained there for weeks to months at a time. Our results demonstrate that tropical waters are not a barrier to migratory connectivity for basking shark populations and highlight the need for global conservation efforts throughout the species range.

Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks.

Stress from fishing capture can incite potentially lethal physiological changes in fishes. Blood acid-base status has routinely been utilized to gauge the magnitude of the stress response, which is dependent on the nature of the capture event and metabolic capacity of the species in question. The mortality induced by demersal longline capture has been shown to vary among taxonomically similar carcharhinid elasmobranchs. In this study, we aimed to: (1) quantify and compare blood acid-base disturbances associated with longline capture in five carcharhinid species; (2) examine the extent to which these disturbances correspond with reported at-vessel mortality rates; and (3) investigate how interspecific differences in the physiological stress response could relate to life history, ecology, and phylogeny. Results showed that blood acid-base disturbances from longline-capture varied between species, with relative degrees of disturbance by species proportional to previously reported at-vessel mortality rates. In addition, the degree in which metabolic and respiratory acidoses influenced relative depressions in blood pH also differed by species. The differences in blood acid-base status point to discrepancies in the aerobic and anaerobic capacities among these taxonomically similar species, and are important when considering the effects of, and possible means to mitigate deleterious consequences from, longline fishing capture.

Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks.

We conducted stable 13C and 15N analysis on white shark vertebrae and demonstrated that incremental analysis of isotopes along the radius of a vertebral centrum produces a chronological record of dietary information, allowing for reconstruction of an individual's trophic history. Isotopic data showed significant enrichments in 15N with increasing sampling distance from the centrum center, indicating a correlation between body size and trophic level. Additionally, isotopic values verified two distinct ontogenetic trophic shifts in the white shark: one following parturition, marking a dietary switch from yolk to fish; and one at a total length of >341 cm, representing a known diet shift from fish to marine mammals. Retrospective trophic-level reconstruction using vertebral tissue will have broad applications in future studies on the ecology of threatened, endangered, or extinct species to determine life-long feeding patterns, which would be impossible through other methods.