White shark genome reveals ancient elasmobranch adaptations associated with wound healing and the maintenance of genome stability.

The white shark (Carcharodon carcharias; Chondrichthyes, Elasmobranchii) is one of the most publicly recognized marine animals. Here we report the genome sequence of the white shark and comparative evolutionary genomic analyses to the chondrichthyans, whale shark (Elasmobranchii) and elephant shark (Holocephali), as well as various vertebrates. The 4.63-Gbp white shark genome contains 24,520 predicted genes, and has a repeat content of 58.5%. We provide evidence for a history of positive selection and gene-content enrichments regarding important genome stability-related genes and functional categories, particularly so for the two elasmobranchs. We hypothesize that the molecular adaptive emphasis on genome stability in white and whale sharks may reflect the combined selective pressure of large genome sizes, high repeat content, high long-interspersed element retrotransposon representation, large body size, and long lifespans, represented across these two species. Molecular adaptation for wound healing was also evident, with positive selection in key genes involved in the wound-healing process, as well as Gene Ontology enrichments in fundamental wound-healing pathways. Sharks, particularly apex predators such as the white shark, are believed to have an acute sense of smell. However, we found very few olfactory receptor genes, very few trace amine-associated receptors, and extremely low numbers of G protein-coupled receptors. We did however, identify 13 copies of vomeronasal type 2 (V2R) genes in white shark and 10 in whale shark; this, combined with the over 30 V2Rs reported previously for elephant shark, suggests this gene family may underlie the keen odorant reception of chondrichthyans.

Coastal sharks supply the global shark fin trade.

Progress in global shark conservation has been limited by constraints to understanding the species composition and geographic origins of the shark fin trade. Previous assessments that relied on earlier genetic techniques and official trade records focused on abundant pelagic species traded between Europe and Asia. Here, we combine recent advances in DNA barcoding and species distribution modelling to identify the species and source the geographic origin of fins sold at market. Derived models of species environmental niches indicated that shark fishing effort is concentrated within Exclusive Economic Zones, mostly in coastal Australia, Indonesia, the United States, Brazil, Mexico and Japan. By coupling two distinct tools, barcoding and niche modelling, our results provide new insights for monitoring and enforcement. They suggest stronger local controls of coastal fishing may help regulate the unsustainable global trade in shark fins.

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.

Cryptic habitat use of white sharks in kelp forest revealed by animal-borne video.

Traditional forms of marine wildlife research are often restricted to coarse telemetry or surface-based observations, limiting information on fine-scale behaviours such as predator-prey events and interactions with habitat features. We use contemporary animal-attached cameras with motion sensing dataloggers, to reveal novel behaviours by white sharks, Carcharodon carcharias, within areas of kelp forest in South Africa. All white sharks tagged in this study spent time adjacent to kelp forests, with several moving throughout densely kelp-covered areas, navigating through channels and pushing directly through stipes and fronds. We found that activity and turning rates significantly increased within kelp forest. Over 28 h of video data revealed that white shark encounters with Cape fur seals, Arctocephalus pusillus pusillus, occurred exclusively within kelp forests, with seals displaying predator evasion behaviour during those encounters. Uniquely, we reveal the use of kelp forest habitat by white sharks, previously assumed inaccessible to these large predators.

An evaluation of body condition and morphometric relationships within southern California juvenile white sharks Carcharodon carcharias.

Length, mass and girth relationships are presented for 112 juvenile white sharks (JWS) Carcharodon carcharias caught in the Southern California Bight (SCB) nursery area between June 2008 and August 2017. No difference was found between male and female JWS length-mass relationships, but data suggest that JWS in the SCB gain more mass per unit length for the juvenile size classes compared with other C. carcharias populations. Condition-factor-to-liver-mass and condition-factor-to-liver-lipid-content relationships revealed that length and mass (i.e., condition factor) can be used as a non-invasive proxy for body condition for juveniles of this species. The parameters estimated in this study are key information for population assessments of juvenile C. carcharias in the north-east Pacific Ocean and will contribute to the conservation and management of this IUCN Red List Vulnerable species.

Travelling light: white sharks (Carcharodon carcharias) rely on body lipid stores to power ocean-basin scale migration.

Many species undertake long-distance annual migrations between foraging and reproductive areas. Such migrants depend on the efficient packaging, storage and utilization of energy to succeed. A diverse assemblage of organisms accomplishes this through the use of lipid reserves; yet, it remains unclear whether the migrations of elasmobranchs, which include the largest gill breathers on Earth, depend on such a mechanism. We examine depth records from pop-up satellite archival tags to discern changes in buoyancy as a proxy for energy storage in Eastern Pacific white sharks, and assess whether lipid depletion fuels long-distance (approx. 4000 km) migrations. We develop new algorithms to assess body condition, buoyancy and drift rate during drift dives and validate the techniques using a captive white shark. In the wild, we document a consistent increase in drift rate over the course of all migrations, indicating a decrease in buoyancy caused by the depletion of lipid reserves. These results comprise, to our knowledge, the first assessment of energy storage and budgeting in migrating sharks. The methods provide a basis for further insights into using electronic tags to reveal the energetic strategies of a wide range of elasmobranchs.

A biologging database of juvenile white sharks from the northeast Pacific.

Species occurrence records are vital data streams in marine conservation with a wide range of important applications. From 2001-2020, the Monterey Bay Aquarium led an international research collaboration to understand the life cycle, ecology, and behavior of white sharks (Carcharodon carcharias) in the southern California Current. The collaboration was devoted to tagging juveniles with animal-borne sensors, also known as biologging. Here we report the full data records from 59 pop-up archival (PAT) and 20 smart position and temperature transmitting (SPOT) tags that variously recorded pressure, temperature, and light-level data, and computed depth and geolocations for 63 individuals. Whether transmitted or from recovered devices, raw data files from successful deployments (n = 70) were auto-ingested from the manufacturer into the United States (US) Animal Telemetry Network's (ATN) Data Assembly Center (DAC). There they have attributed a full suite of metadata, visualized within their public-facing data portal, compiled for permanent archive under the DataONE Research Workspace member node, and are accessible for download from the ATN data portal.

A first estimate of white shark, Carcharodon carcharias, abundance off Central California.

The decline of sharks in the global oceans underscores the need for careful assessment and monitoring of remaining populations. The northeastern Pacific is the home range for a genetically distinct clade of white sharks (Carcharodon carcharias). Little is known about the conservation status of this demographically isolated population, concentrated seasonally at two discrete aggregation sites: Central California (CCA) and Guadalupe Island, Mexico. We used photo-identification of dorsal fins in a sequential Bayesian mark-recapture algorithm to estimate white shark abundance off CCA. We collected 321 photographs identifying 130 unique individuals, and estimated the abundance off CCA to be 219 mature and sub-adult individuals ((130, 275) 95% credible intervals), substantially smaller than populations of other large marine predators. Our methods can be readily expanded to estimate shark population abundance at other locations, and over time, to monitor the status, population trends and protection needs of these globally distributed predators.

North Pacific warming shifts the juvenile range of a marine apex predator.

During the 2014-2016 North Pacific marine heatwave, unprecedented sightings of juvenile white sharks (Carcharodon carcharias) emerged in central California. These records contradicted the species established life history, where juveniles remain in warmer waters in the southern California Current. This spatial shift is significant as it creates potential conflicts with commercial fisheries, protected species conservation, and public safety concerns. Here, we integrate community science, photogrammetry, biologging, and mesoscale climate data to describe and explain this phenomenon. We find a dramatic increase in white sharks from 2014 to 2019 in Monterey Bay that was overwhelmingly comprised of juvenile sharks < 2.5 m in total body length. Next, we derived thermal preferences from 22 million tag measurements of 14 juvenile sharks and use this to map the cold limit of their range. Consistent with historical records, the position of this cold edge averaged 34° N from 1982 to 2013 but jumped to 38.5° during the 2014-2016 marine heat wave. In addition to a poleward shift, thermally suitable habitat for juvenile sharks declined 223.2 km2 year-1 from 1982 to 2019 and was lowest in 2015 at the peak of the heatwave. In addition to advancing the adaptive management of this apex marine predator, we discuss this opportunity to engage public on climate change through marine megafauna.

Philopatry and migration of Pacific white sharks.

Advances in electronic tagging and genetic research are making it possible to discern population structure for pelagic marine predators once thought to be panmictic. However, reconciling migration patterns and gene flow to define the resolution of discrete population management units remains a major challenge, and a vital conservation priority for threatened species such as oceanic sharks. Many such species have been flagged for international protection, yet effective population assessments and management actions are hindered by lack of knowledge about the geographical extent and size of distinct populations. Combining satellite tagging, passive acoustic monitoring and genetics, we reveal how eastern Pacific white sharks (Carcharodon carcharias) adhere to a highly predictable migratory cycle. Individuals persistently return to the same network of coastal hotspots following distant oceanic migrations and comprise a population genetically distinct from previously identified phylogenetic clades. We hypothesize that this strong homing behaviour has maintained the separation of a northeastern Pacific population following a historical introduction from Australia/New Zealand migrants during the Late Pleistocene. Concordance between contemporary movement and genetic divergence based on mitochondrial DNA demonstrates a demographically independent management unit not previously recognized. This population's fidelity to discrete and predictable locations offers clear population assessment, monitoring and management options.

Model-based assessment of persistence in proposed marine protected area designs.

Assessment of marine protected areas (MPAs) requires the ability to quantify the effects of proposed MPA size and placement, habitat distribution, larval dispersal, and fishing on the persistence of protected populations. Here we describe a model-based approach to assessment of the contribution of a network of marine protected areas to the persistence of populations with a sedentary adult phase and a dispersing larval phase. The model integrates the effects of a patchy spatial distribution of habitat, the spatial scale of larval dispersal, and the level of fishing outside of reserves into a calculation of the spatial distribution of equilibrium settlement. We use the amount of coastline predicted to have equilibrium settlement rates that saturate post-settlement habitat as a response variable for the assessment and comparison of MPA network designs. We apply this model to a set of recently proposed MPA networks for the central coast of California, USA. Results show that the area of habitat set aside is a good predictor of the area over which population levels will be high for short-distance dispersers. However, persistence of longer distance dispersers depends critically on the spatial distribution of habitat and reserves, ranging from not persistent anywhere to persistent over a greater area than that set aside in reserves. These results depend on the mechanisms of persistence, with self-replacement supporting short-distance dispersers and network effects supporting long-distance dispersers. Persistence also depends critically on fishery status outside the MPAs, as well as how fishing effort is redistributed after MPA implementation. This assessment method provides important benchmarks, as well as a transparent modeling approach, for improving initial MPA configurations that may result from less-comprehensive rule- or habitat-based methods of designing MPAs.

Non-trophic impacts from white sharks complicate population recovery for sea otters.

Complex interactions between protected populations may challenge the recovery of whole ecosystems. In California, white sharks (Carcharodon carcharias) mistargeting southern sea otters (Enhydra lutris nereis) are an emergent impact to sea otter recovery, inhibiting the broader ecosystem restoration sea otters might provide. Here, we integrate and analyze tracking and stranding data to compare the phenology of interactions between white sharks and their targeted prey (elephant seals, Mirounga angustirostris) with those of mistargeted prey (sea otters, humans). Pronounced seasonal peaks in shark bites to otters and humans overlap in the late boreal summer, immediately before the annual adult white shark migration to elephant seal rookeries. From 1997 to 2017, the seasonal period when sharks bite otters expanded from 2 to 8 months of the year and occurred primarily in regions where kelp cover declined. Immature and male otters, demographics most associated with range expansion, were disproportionately impacted. While sea otters are understood to play a keystone role in kelp forests, recent ecosystem shifts are revealing unprecedented bottom-up and top-down interactions. Such shifts challenge ecosystem management programs that rely on static models of species interactions.

Quantifying habitat selection and variability in habitat suitability for juvenile white sharks.

While adult white sharks (Carcharodon carcharias) are apex predators with a circumglobal distribution, juvenile white sharks (JWS) feed primarily on bottom dwelling fishes and tend to be coastally associated. Despite the assumedly easier access to juveniles compared to large, migratory adults, limited information is available on the movements, environments, and distributions of individuals during this life stage. To quantify movement and understand their distribution in the southern California Bight, JWS were captured and fitted with dorsal fin-mounted satellite transmitters (SPOT tags; n = 18). Nine individuals crossed the U.S. border into Baja California, Mexico. Individuals used shallow habitats (134.96 ± 191.1 m) close to shore (7.16 ± 5.65 km). A generalized linear model with a binomial distribution was used to predict the presence of individuals based on several environmental predictors from these areas. Juveniles were found to select shallow habitats (< 1000 m deep) close to land (< 30 km of the shoreline) in waters ranging from 14 to 24°C. Southern California was found to be suitable eight months of the year, while coastal habitats in Baja California were suitable year-round. The model predicted seasonal movement with sharks moving from southern California to Baja California during winter. Additionally, habitat distribution changed inter-annually with sharks having a more northerly distribution during years with a higher Pacific Decadal Oscillation index, suggesting sharks may forego their annual fall migrations to Baja California, Mexico, during El Niño years. Model predictions aligned with fishery-dependent catch data, with a greater number of sharks being captured during periods and/or areas of increased habitat suitability. Thus, habitat models could be useful for predicting the presence of JWS in other areas, and can be used as a tool for potentially reducing fishery interactions during seasons and locations where there is increased susceptibility of incidental catch.

Killer whales redistribute white shark foraging pressure on seals.

Predatory behavior and top-down effects in marine ecosystems are well-described, however, intraguild interactions among co-occurring marine top predators remain less understood, but can have far reaching ecological implications. Killer whales and white sharks are prominent upper trophic level predators with highly-overlapping niches, yet their ecological interactions and subsequent effects have remained obscure. Using long-term electronic tagging and survey data we reveal rare and cryptic interactions between these predators at a shared foraging site, Southeast Farallon Island (SEFI). In multiple instances, brief visits from killer whales displaced white sharks from SEFI, disrupting shark feeding behavior for extended periods at this aggregation site. As a result, annual predations of pinnipeds by white sharks at SEFI were negatively correlated with close encounters with killer whales. Tagged white sharks relocated to other aggregation sites, creating detectable increases in white shark density at Ano Nuevo Island. This work highlights the importance of risk effects and intraguild relationships among top ocean predators and the value of long-term data sets revealing these consequential, albeit infrequent, ecological interactions.

The political biogeography of migratory marine predators.

During their migrations, marine predators experience varying levels of protection and face many threats as they travel through multiple countries' jurisdictions and across ocean basins. Some populations are declining rapidly. Contributing to such declines is a failure of some international agreements to ensure effective cooperation by the stakeholders responsible for managing species throughout their ranges, including in the high seas, a global commons. Here we use biologging data from marine predators to provide quantitative measures with great potential to inform local, national and international management efforts in the Pacific Ocean. We synthesized a large tracking data set to show how the movements and migratory phenology of 1,648 individuals representing 14 species-from leatherback turtles to white sharks-relate to the geopolitical boundaries of the Pacific Ocean throughout species' annual cycles. Cumulatively, these species visited 86% of Pacific Ocean countries and some spent three-quarters of their annual cycles in the high seas. With our results, we offer answers to questions posed when designing international strategies for managing migratory species.

Dispersal per recruit: an efficient method for assessing sustainability in marine reserve networks.

Marine reserves are an increasingly important tool for the management of marine ecosystems around the world. However, the effects of proposed marine reserve configurations on sustainability and yield of populations are typically not estimated because of the computational intensity of direct simulation and uncertainty in larval dispersal and density-dependent recruitment. Here we develop a method for efficiently assessing a marine reserve configuration for persistence and yield of a population with sedentary adults and dispersing larvae. The method extends the familiar sustainability criteria of individual replacement for single populations based on eggs-per-recruit (EPR) to spatially distributed populations with sedentary adults, a dispersing larval phase, and limited carrying capacity in the settlement-recruit relationship. We refer to this approach as dispersal-per-recruit (DPR). In some cases, a single DPR calculation, based on the assumption that post-settlement habitat is saturated (i.e., at maximum recruitment), is sufficient to determine population persistence, while in other cases further iterative calculations are required. These additional calculations reach an equilibrium more rapidly than a full simulation of age- or size-structured populations. From the DPR result, fishery yield can be computed from yield-per-recruit (YPR) at each point. We assess the utility of DPR calculations by applying them to single reserves, uniformly distributed systems of reserves, and randomly sized and spaced systems of reserves on a linear coastline. We find that for low levels of EPR in fished areas (e.g., 10% or less of the natural, unfished EPR when post-settlement habitats are saturated by 35% of natural settlement), a single DPR calculation is sufficient to determine persistence of the population. We also show that, in uniform systems of reserves with finite reserve size, maximal fisheries yield occurs when the density of reserves is such that all post-settlement habitat is nearly saturated with settlers. Finally, we demonstrate the application of this approach to a realistic proposed marine reserve configuration.

Seasonal changes in fish assemblage structure at a shallow seamount in the Gulf of California.

Seamounts have generally been identified as locations that can promote elevated productivity, biomass and predator biodiversity. These properties attract seamount-associated fisheries where elevated harvests can be obtained relative to surrounding areas. There exists large variation in the geological and oceanographic environment among the thousands of locations that fall within the broad definition of seamount. Global seamount surveys have revealed that not all seamounts are hotspots of biodiversity, and there remains a strong need to understand the mechanisms that underlie variation in species richness observed. We examined the process of fish species assembly at El Bajo Espiritu Santo (EBES) seamount in the Gulf of California over a five-year study period. To effectively quantify the relative abundance of fast-moving and schooling fishes in a 'blue water' habitat, we developed a simplified underwater visual census (UVC) methodology and analysis framework suitable for this setting and applicable to future studies in similar environments. We found correlations between seasonally changing community structure and variability in oceanographic conditions. Individual species responses to thermal habitat at EBES revealed three distinct assemblages, a 'fall assemblage' tracking warmer overall temperature, a 'spring assemblage' correlated with cooler temperature, and a 'year-round assemblage' with no significant response to temperature. Species richness was greatest in spring, when cool and warm water masses stratified the water column and a greater number of species from all three assemblages co-occurred. We discuss our findings in the context of potential mechanisms that could account for predator biodiversity at shallow seamounts.

Eating or meeting? Cluster analysis reveals intricacies of white shark (Carcharodon carcharias) migration and offshore behavior.

Elucidating how mobile ocean predators utilize the pelagic environment is vital to understanding the dynamics of oceanic species and ecosystems. Pop-up archival transmitting (PAT) tags have emerged as an important tool to describe animal migrations in oceanic environments where direct observation is not feasible. Available PAT tag data, however, are for the most part limited to geographic position, swimming depth and environmental temperature, making effective behavioral observation challenging. However, novel analysis approaches have the potential to extend the interpretive power of these limited observations. Here we developed an approach based on clustering analysis of PAT daily time-at-depth histogram records to distinguish behavioral modes in white sharks (Carcharodon carcharias). We found four dominant and distinctive behavioral clusters matching previously described behavioral patterns, including two distinctive offshore diving modes. Once validated, we mapped behavior mode occurrence in space and time. Our results demonstrate spatial, temporal and sex-based structure in the diving behavior of white sharks in the northeastern Pacific previously unrecognized including behavioral and migratory patterns resembling those of species with lek mating systems. We discuss our findings, in combination with available life history and environmental data, and propose specific testable hypotheses to distinguish between mating and foraging in northeastern Pacific white sharks that can provide a framework for future work. Our methodology can be applied to similar datasets from other species to further define behaviors during unobservable phases.

Using stable isotope analysis to understand the migration and trophic ecology of northeastern Pacific white sharks (Carcharodon carcharias).

The white shark (Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (δ(13)C) and nitrogen (δ(15)N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle δ(13)C and δ(15)N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.