Novel CTD tag establishes shark fins as ocean observing platforms.

Animal-borne tags are effective instruments for collecting ocean data and can be used to fill spatial gaps in the observing network. We deployed the first conductivity, temperature, and depth (CTD) satellite tags on the dorsal fin of salmon sharks (Lamna ditropis) to demonstrate the potential of sharks to monitor essential ocean variables and oceanographic features in the Gulf of Alaska. Over 1360 km and 36 days in the summer of 2015, the salmon shark collected 56 geolocated, temperature-salinity profiles. The shark swam through a plume of anomalously salty water that originated from the "Blob" and encountered several mesoscale eddies, whose subsurface properties were altered by the marine heatwave. We demonstrate that salmon sharks have the potential to serve as submesoscale-resolving oceanographic platforms and substantially increase the spatial coverage of observations in the Gulf of Alaska.

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.

Impacts of marine heatwaves on top predator distributions are variable but predictable.

Marine heatwaves cause widespread environmental, biological, and socio-economic impacts, placing them at the forefront of 21st-century management challenges. However, heatwaves vary in intensity and evolution, and a paucity of information on how this variability impacts marine species limits our ability to proactively manage for these extreme events. Here, we model the effects of four recent heatwaves (2014, 2015, 2019, 2020) in the Northeastern Pacific on the distributions of 14 top predator species of ecological, cultural, and commercial importance. Predicted responses were highly variable across species and heatwaves, ranging from near total loss of habitat to a two-fold increase. Heatwaves rapidly altered political bio-geographies, with up to 10% of predicted habitat across all species shifting jurisdictions during individual heatwaves. The variability in predicted responses across species and heatwaves portends the need for novel management solutions that can rapidly respond to extreme climate events. As proof-of-concept, we developed an operational dynamic ocean management tool that predicts predator distributions and responses to extreme conditions in near real-time.

Multiple behaviors for turning performance of Pacific bluefin tuna (Thunnus orientalis).

Tuna are known for exceptional swimming speeds, which are possible because of their thunniform lift-based propulsion, large muscle mass and rigid fusiform body. A rigid body should restrict maneuverability with regard to turn radius and turn rate. To test if turning maneuvers by the Pacific bluefin tuna (Thunnus orientalis) are constrained by rigidity, captive animals were videorecorded overhead as the animals routinely swam around a large circular tank or during feeding bouts. Turning performance was classified into three different types: (1) glide turns, where the tuna uses the caudal fin as a rudder; (2) powered turns, where the animal uses continuous near symmetrical strokes of the caudal fin through the turn; and (3) ratchet turns, where the overall global turn is completed by a series of small local turns by asymmetrical stokes of the caudal fin. Individual points of the rostrum, peduncle and tip of the caudal fin were tracked and analyzed. Frame-by-frame analysis showed that the ratchet turn had the fastest turn rate for all points with a maximum of 302 deg s-1. During the ratchet turn, the rostrum exhibited a minimum global 0.38 body length turn radius. The local turn radii were only 18.6% of the global ratchet turn. The minimum turn radii ranged from 0.4 to 1.7 body lengths. Compared with the performance of other swimmers, the increased flexion of the peduncle and tail and the mechanics of turning behaviors used by tuna overcomes any constraints to turning performance from the rigidity of the anterior body morphology.

Using pseudo-absence models to test for environmental selection in marine movement ecology: the importance of sample size and selection strength.

BACKGROUND: Understanding the selection of environmental conditions by animals requires knowledge of where they are, but also of where they could have been. Presence data can be accurately estimated by direct sampling, sightings, or through electronic tag deployments. However, absence data are harder to determine because absences are challenging to measure in an uncontrolled setting. To address this problem, ecologists have developed different methods for generating pseudo-absence data relying on theoretical movement models. These null models represent the movement of environmentally naive individuals, creating a set of locations that animals could have been if they were not exhibiting environmental selection. METHODS: Here, we use four different kinds of null animal movement models-Brownian motion, Lévy walks, Correlated random walks, and Joint correlated random walks to test the ability and power of each of these null movement models to serve as appropriate animal absence models. We use Kolmogorov-Smirnov tests to detect environmental selection using two data sets, one of simulated animal tracks biased towards warmer sea surface temperatures, and one of 57 observed blue shark tracks of unknown sea surface temperature selection. RESULTS: The four different types of movement models showed minimal difference in the ability to serve as appropriate null models for environmental selection studies. Selection strength and sample size were more important in detecting true environmental selection. We show that this method can suffer from high false positive rates, especially in the case where animals are not selecting for specific environments. We provide estimates of test accuracy at different sample sizes and selection strengths to avoid false positives when using this method. CONCLUSION: We show how movement models can be used to generate pseudo-absences and test for habitat selection in marine organisms. While this approach efficiently detects environmental selection in marine organisms, it cannot detect the underlying mechanisms driving this selection.

Flexible use of a dynamic energy landscape buffers a marine predator against extreme climate variability.

Animal migrations track predictable seasonal patterns of resource availability and suitable thermal habitat. As climate change alters this 'energy landscape', some migratory species may struggle to adapt. We examined how climate variability influences movements, thermal habitat selection and energy intake by juvenile Pacific bluefin tuna (Thunnus orientalis) during seasonal foraging migrations in the California Current. We tracked 242 tuna across 15 years (2002-2016) with high-resolution archival tags, estimating their daily energy intake via abdominal warming associated with digestion (the 'heat increment of feeding'). The poleward extent of foraging migrations was flexible in response to climate variability, allowing tuna to track poleward displacements of thermal habitat where their standard metabolic rates were minimized. During a marine heatwave that saw temperature anomalies of up to +2.5°C in the California Current, spatially explicit energy intake by tuna was approximately 15% lower than average. However, by shifting their mean seasonal migration approximately 900 km poleward, tuna remained in waters within their optimal temperature range and increased their energy intake. Our findings illustrate how tradeoffs between physiology and prey availability structure migration in a highly mobile vertebrate, and suggest that flexible migration strategies can buffer animals against energetic costs associated with climate variability and change.

Natal origin and age-specific egress of Pacific bluefin tuna from coastal nurseries revealed with geochemical markers.

Geochemical chronologies were constructed from otoliths of adult Pacific bluefin tuna (PBT) to investigate the timing of age-specific egress of juveniles from coastal nurseries in the East China Sea or Sea of Japan to offshore waters of the Pacific Ocean. Element:Ca chronologies were developed for otolith Li, Mg, Mn, Zn, Sr, and Ba, and our assessment focused on the section of the otolith corresponding to the age-0 to age-1 + interval. Next, we applied a common time-series approach to geochemical profiles to identify divergences presumably linked to inshore-offshore migrations. Conspicuous geochemical shifts were detected during the juvenile interval for Mg:Ca, Mn:Ca, and Sr:Ca that were indicative of coastal-offshore transitions or egress generally occurring for individuals approximately 4-6 mo. old, with later departures (6 mo. or older) linked to overwintering being more limited. Changepoints in otolith Ba:Ca profiles were most common in the early age-1 period (ca. 12-16 mo.) and appear associated with entry into upwelling areas such as the California Current Large Marine Ecosystem following trans-Pacific migrations. Natal origin of PBT was also predicted using the early life portion of geochemical profile in relation to a baseline sample comprised of age-0 PBT from the two primary spawning areas in the East China Sea and Sea of Japan. Mixed-stock analysis indicated that the majority (66%) of adult PBT in our sample originated from the East China Sea, but individuals of Sea of Japan origin were also detected in the Ryukyu Archipelago.

Analysing detection gaps in acoustic telemetry data to infer differential movement patterns in fish.

A wide array of technologies are available for gaining insight into the movement of wild aquatic animals. Although acoustic telemetry can lack the fine-scale spatial resolution of some satellite tracking technologies, the substantially longer battery life can yield important long-term data on individual behavior and movement for low per-unit cost. Typically, however, receiver arrays are designed to maximize spatial coverage at the cost of positional accuracy leading to potentially longer detection gaps as individuals move out of range between monitored locations. This is particularly true when these technologies are deployed to monitor species in hard-to-access locations.Here, we develop a novel approach to analyzing acoustic telemetry data, using the timing and duration of gaps between animal detections to infer different behaviors. Using the durations between detections at the same and different receiver locations (i.e., detection gaps), we classify behaviors into "restricted" or potential wider "out-of-range" movements synonymous with longer distance dispersal. We apply this method to investigate spatial and temporal segregation of inferred movement patterns in two sympatric species of reef shark within a large, remote, marine protected area (MPA). Response variables were generated using network analysis, and drivers of these movements were identified using generalized linear mixed models and multimodel inference.Species, diel period, and season were significant predictors of "out-of-range" movements. Silvertip sharks were overall more likely to undertake "out-of-range" movements, compared with gray reef sharks, indicating spatial segregation, and corroborating previous stable isotope work between these two species. High individual variability in "out-of-range" movements in both species was also identified.We present a novel gap analysis of telemetry data to help infer differential movement and space use patterns where acoustic coverage is imperfect and other tracking methods are impractical at scale. In remote locations, inference may be the best available tool and this approach shows that acoustic telemetry gap analysis can be used for comparative studies in fish ecology, or combined with other research techniques to better understand functional mechanisms driving behavior.

The Twilight Zone as a Major Foraging Habitat and Mercury Source for the Great White Shark.

The twilight zone contains the largest biomass of the world's ocean. Identifying its role in the trophic supply and contaminant exposure of marine megafauna constitutes a critical challenge in the context of global change. The white shark (Carcharodon carcharias) is a threatened species with some of the highest concentrations of neurotoxin methylmercury (MeHg) among marine top predators. Large white sharks migrate seasonally from coastal habitats, where they primarily forage on pinnipeds, to oceanic offshore habitats. Tagging studies suggest that while offshore, white sharks may forage at depth on mesopelagic species, yet no biochemical evidence exists. Here, we used mercury isotopic composition to assess the dietary origin of MeHg contamination in white sharks from the Northeast Pacific Ocean. We estimated that a minimum of 72% of the MeHg accumulated by white sharks originates from the consumption of mesopelagic prey, while a maximum of 25% derives from pinnipeds. In addition to highlighting the potential of mercury isotopes to decipher the complex ecological cycle of marine predators, our study provides evidence that the twilight zone constitutes a crucial foraging habitat for these large predators, which had been suspected for over a decade. Climate change is predicted to expand the production of mesopelagic MeHg and modify the mesopelagic biomass globally. Considering the pivotal role of the twilight zone is therefore essential to better predict both MeHg exposure and trophic supply to white sharks, and effectively protect these key vulnerable predators.

Tracking the response of industrial fishing fleets to large marine protected areas in the Pacific Ocean.

Large marine protected areas (MPAs) of unprecedented size have recently been established across the global oceans, yet their ability to meet conservation objectives is debated. Key areas of debate include uncertainty over nations' abilities to enforce fishing bans across vast, remote regions and the intensity of human impacts before and after MPA implementation. We used a recently developed vessel tracking data set (produced using Automatic Identification System detections) to quantify the response of industrial fishing fleets to 5 of the largest MPAs established in the Pacific Ocean since 2013. After their implementation, all 5 MPAs successfully kept industrial fishing effort exceptionally low. Detected fishing effort was already low in 4 of the 5 large MPAs prior to MPA implementation, particularly relative to nearby regions that did not receive formal protection. Our results suggest that these large MPAs may present major conservation opportunities in relatively intact ecosystems with low immediate impact to industrial fisheries, but the large MPAs we considered often did not significantly reduce fishing effort because baseline fishing was typically low. It is yet to be determined how large MPAs may shape global ocean conservation in the future if the footprint of human influence continues to expand. Continued improvement in understanding of how large MPAs interact with industrial fisheries is a crucial step toward defining their role in global ocean management.

Seguimiento a la Respuesta de las Flotillas de Pesca Industrial a las Grandes Áreas Marinas Protegidas Extensas Resumen Recientemente se han establecido grandes áreas marinas protegidas (AMPs) de tamaños nunca vistos en todos los océanos del mundo; sin embargo, se sigue debatiendo su habilidad para lograr los objetivos de conservación. El debate se centra en los siguientes temas importantes: la incertidumbre por la capacidad de las naciones para hacer cumplir las vedas de pesca en regiones vastas y remotas y la intensidad del impacto humano antes y después de la implementación de una AMP. Usamos un conjunto de datos de rastreo de navíos recientemente desarrollado (producido usando detecciones mediante el Sistema Automático de Identificación) para cuantificar la respuesta de las flotillas de pesca industrial ante cinco de las AMPs más grandes establecidas en el océano Pacífico desde 2013. Después de su implementación, las cinco AMPs mantuvieron exitosamente los esfuerzos de pesca industrial a niveles excepcionalmente bajos. El esfuerzo de pesca detectado ya se encontraba bajo en cuatro de las cinco grandes AMPs previo a la implementación, particularmente en relación con las regiones próximas que no reciben protección formal. Nuestros resultados sugieren que estas grandes AMPs pueden presentar oportunidades importantes de conservación en ecosistemas relativamente intactos con un impacto inmediato bajo para las pesquerías industriales, pero las grandes AMPs que consideramos con frecuencia no redujeron significativamente el esfuerzo de pesca porque la línea base de la pesca con frecuencia ya era baja. Todavía se debe determinar cómo las grandes AMPs pueden moldear la conservación mundial de los océanos en el futuro si la huella de la influencia humana continúa expandiéndose. La mejoría continua del entendimiento de cómo las grandes AMPs interactúan con las pesquerías industriales es un paso importante hacia la definición de su papel en el manejo mundial de los océanos.

Skeletal muscle and cardiac transcriptomics of a regionally endothermic fish, the Pacific bluefin tuna, Thunnus orientalis.

BACKGROUND: The Pacific bluefin tuna (Thunnus orientalis) is a regionally endothermic fish that maintains temperatures in their swimming musculature, eyes, brain and viscera above that of the ambient water. Within their skeletal muscle, a thermal gradient exists, with deep muscles, close to the backbone, operating at elevated temperatures compared to superficial muscles near the skin. Their heart, by contrast, operates at ambient temperature, which in bluefin tunas can range widely. Cardiac function in tunas reduces in cold waters, yet the heart must continue to supply blood for metabolically demanding endothermic tissues. Physiological studies indicate Pacific bluefin tuna have an elevated cardiac capacity and increased cold-tolerance compared to warm-water tuna species, primarily enabled by increased capacity for sarcoplasmic reticulum calcium cycling within the cardiac muscles. RESULTS: Here, we compare tissue-specific gene-expression profiles of different cardiac and skeletal muscle tissues in Pacific bluefin tuna. There was little difference in the overall expression of calcium-cycling and cardiac contraction pathways between atrium and ventricle. However, expression of a key sarcoplasmic reticulum calcium-cycling gene, SERCA2b, which plays a key role maintaining intracellular calcium stores, was higher in atrium than ventricle. Expression of genes involved in aerobic metabolism and cardiac contraction were higher in the ventricle than atrium. The two morphologically distinct tissues that derive the ventricle, spongy and compact myocardium, had near-identical levels of gene expression. More genes had higher expression in the cool, superficial muscle than in the warm, deep muscle in both the aerobic red muscle (slow-twitch) and anaerobic white muscle (fast-twitch), suggesting thermal compensation. CONCLUSIONS: We find evidence of widespread transcriptomic differences between the Pacific tuna ventricle and atrium, with potentially higher rates of calcium cycling in the atrium associated with the higher expression of SERCA2b compared to the ventricle. We find no evidence that genes associated with thermogenesis are upregulated in the deep, warm muscle compared to superficial, cool muscle. Heat generation may be enabled by by the high aerobic capacity of bluefin tuna red muscle.

Biomechanical Analysis of the Slow-Twitch (Red) Muscle Force Transmission Pathways in Tunas.

In tunas, the slow-twitch red muscle, which has an elevated temperature, powers thunniform locomotion, a stiff-bodied swimming style. The anatomical placement and operating temperatures of red muscle vary widely among teleosts: in tunas, the red muscle is located centrally in the body, adjacent to the spine, and maintains an elevated temperature. In the majority of ectothermic teleosts, red muscle is located laterally in the body, adjacent to the skin, and operates at ambient temperature. The specialized physiology and biomechanics of red muscle in tunas are often considered important adaptations to their high-performance pelagic lifestyle; however, the mechanics of how muscular work is transmitted to the tail remains largely unknown. The red muscle has a highly pennate architecture and is connected to the spine through a network of bones (epicentral bones) and long tendons (posterior oblique tendons). The network of long tendons has been hypothesized to enhance the power transmitted to the tail. Here, we investigate the morphology and biomechanics of the tuna's red muscle and tendons to determine whether elasticity is exploited to reduce the cost of transport, as is the case in many terrestrial vertebrates. To address this question, we evaluate two hypotheses: (1) tendons stretch during red-muscle-actuated swimming and (2) tendons comprise the primary load transmission pathway from the red muscle to the spine. To evaluate these hypotheses, we measured the mechanical properties of the posterior oblique tendons and performed novel dissections to estimate the peak force that the red muscle can generate. The force-generating capacity of the red muscle is calculated to be much greater than the load-bearing capacity of the posterior oblique tendons. Thus, the long tendons likely stretch under force from the red muscle, but they are not strong enough to be the primary force transmission pathway. These results suggest that other pathways, such as serial load transmission through the red muscle myomeres to the great lateral tendon and/or the anterior oblique tendons to the skin, transmit appreciable force to the tail.

Complete mitochondrial genome of the gray reef shark, Carcharhinus amblyrhynchos (Carcharhiniformes: Carcharhinidae).

We report the first mitochondrial genome sequences for the gray reef shark, Carcharhinus amblyrhynchos. Two specimens from the British Indian Ocean Territory were sequenced independently using two different next generation sequencing methods, namely short read sequencing on the Illumina HiSeq and long read sequencing on the Oxford Nanopore Technologies' MinION sequencer. The two sequences are 99.9% identical and are 16,705 base pairs (bp) and 16,706 bp in length. The mitogenome contains 22 tRNA genes, two rRNA genes, 13 protein-coding genes and two non-coding regions; the control region and the origin of light-strand replication (OL).

Mitochondrial genome of the Silvertip shark, Carcharhinus albimarginatus, from the British Indian Ocean Territory.

The Chagos archipelago in the British Indian Ocean Territory (BIOT) has been lacking in detailed genetic studies of its chondrichthyan populations. Chondrichthyes in Chagos continue to be endangered through illegal fishing operations, necessitating species distribution and abundance studies to facilitate urgent monitoring and conservation of the species. Here, we present a complete mitochondrial genome of the Silvertip Shark, Carcharhinus albimarginatus sampled in the Chagos archipelago. The mitochondrial genome of C. albimarginatus was 16,706 bp in length and consisted of 13 protein-coding genes, 22 tRNA genes, two rRNA genes, a replication origin and a D-loop region. GC content was at 38.7% and the control region was 1,065 bp in length. We expect that mitogenomes presented here will aid development of molecular assays for species distribution studies. Overall these studies will promote effective conservation of marine ecosystemes in the BIOT.

Complete mitochondrial genome of the whitetip reef shark Triaenodon obesus from the British Indian Ocean Territory Marine Protected Area.

We present the first mitochondrial genome of Trianenodon obesus from the Chagos Archipelago in the British Indian Ocean Territory (BIOT) Marine Protected Area. The mitogenome was 16,702 bp in length and consisted of 13 protein-coding genes (PCGs), 22 tRNA genes, 2 rRNA genes, and a non-coding control region (D-loop). GC content was at 38.9%. The control region was 1064 bp in length. This mitogenome for the BIOT MPA T. obesus differed from the previously published T. obesus genome by 15 bp and the differences include a 2 bp insertion and 13 single nucleotide polymorphisms distributed across the mitogenome in the BIOT MPA sequence. Whole mitogenome sequence of T. obesus from the Chagos archipelago presented here fills existing gaps in genetic information on marine species from the BIOT MPA and provides additional tools for species specific assessments as to the effectiveness of MPA management. In addition, methods presented here lay the framework for genetic studies in remote locations with limited infrastructure.

Mitochondrial genome of the silky shark Carcharhinus falciformis from the British Indian Ocean Territory Marine Protected Area.

We present the first mitochondrial genome of Carcharhinus falciformis from the Chagos Archipelago in the British Indian Ocean Territory (BIOT) Marine Protected Area (MPA). The mitochondrial genome of C. falciformis is 16,701 bp in length and consists of 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes, and a non-coding control region (D-loop). GC content was at 40.1%. The control region was 1063 bp in length. The complete mitogenome sequence of C. falciformis from the BIOT MPA will enable improved conservation measures of the CITES listed species through studies of species distribution, population abundance, fishing pressure and wildlife trade.

Cardiac remodeling in response to embryonic crude oil exposure involves unconventional NKX family members and innate immunity genes.

Cardiac remodeling results from both physiological and pathological stimuli. Compared with mammalian hearts, fish hearts show a broader array of remodeling changes in response to environmental influences, providing exceptional models for dissecting the molecular and cellular bases of cardiac remodeling. We recently characterized a form of pathological remodeling in juvenile pink salmon (Oncorhynchus gorbuscha) in response to crude oil exposure during embryonic cardiogenesis. In the absence of overt pathology (cardiomyocyte death or inflammatory infiltrate), cardiac ventricles in exposed fish showed altered shape, reduced thickness of compact myocardium and hypertrophic changes in spongy, trabeculated myocardium. Here, we used RNA sequencing to characterize molecular pathways underlying these defects. In juvenile ventricular cardiomyocytes, antecedent embryonic oil exposure led to dose-dependent upregulation of genes involved in innate immunity and two NKX homeobox transcription factors not previously associated with cardiomyocytes, nkx2.3 and nkx3.3 Absent from mammalian genomes, the latter is largely uncharacterized. In zebrafish embryos, nkx3.3 demonstrated a potent effect on cardiac morphogenesis, equivalent to that of nkx2.5, the primary transcription factor associated with ventricular cardiomyocyte identity. The role of nkx3.3 in heart growth is potentially linked to the unique regenerative capacity of fish and amphibians. Moreover, these findings support a cardiomyocyte-intrinsic role for innate immune response genes in pathological hypertrophy. This study demonstrates how an expanding mechanistic understanding of environmental pollution impacts - i.e. the chemical perturbation of biological systems - can ultimately yield new insights into fundamental biological processes.

The importance of migratory connectivity for global ocean policy.

The distributions of migratory species in the ocean span local, national and international jurisdictions. Across these ecologically interconnected regions, migratory marine species interact with anthropogenic stressors throughout their lives. Migratory connectivity, the geographical linking of individuals and populations throughout their migratory cycles, influences how spatial and temporal dynamics of stressors affect migratory animals and scale up to influence population abundance, distribution and species persistence. Population declines of many migratory marine species have led to calls for connectivity knowledge, especially insights from animal tracking studies, to be more systematically and synthetically incorporated into decision-making. Inclusion of migratory connectivity in the design of conservation and management measures is critical to ensure they are appropriate for the level of risk associated with various degrees of connectivity. Three mechanisms exist to incorporate migratory connectivity into international marine policy which guides conservation implementation: site-selection criteria, network design criteria and policy recommendations. Here, we review the concept of migratory connectivity and its use in international policy, and describe the Migratory Connectivity in the Ocean system, a migratory connectivity evidence-base for the ocean. We propose that without such collaboration focused on migratory connectivity, efforts to effectively conserve these critical species across jurisdictions will have limited effect.