Energetic connectivity of diverse elasmobranch populations - implications for ecological resilience.

Understanding the factors shaping patterns of ecological resilience is critical for mitigating the loss of global biodiversity. Throughout aquatic environments, highly mobile predators are thought to serve as important vectors of energy between ecosystems thereby promoting stability and resilience. However, the role these predators play in connecting food webs and promoting energy flow remains poorly understood in most contexts. Using carbon and nitrogen isotopes, we quantified the use of several prey resource pools (small oceanic forage, large oceanics, coral reef, and seagrass) by 17 species of elasmobranch fishes (n = 351 individuals) in The Bahamas to determine their functional diversity and roles as ecosystem links. We observed remarkable functional diversity across species and identified four major groups responsible for connecting discrete regions of the seascape. Elasmobranchs were responsible for promoting energetic connectivity between neritic, oceanic and deep-sea ecosystems. Our findings illustrate how mobile predators promote ecosystem connectivity, underscoring their functional significance and role in supporting ecological resilience. More broadly, strong predator conservation efforts in developing island nations, such as The Bahamas, are likely to yield ecological benefits that enhance the resilience of marine ecosystems to combat imminent threats such as habitat degradation and climate change.

From rivers to ocean basins: The role of ocean barriers and philopatry in the genetic structuring of a cosmopolitan coastal predator.

The Bull Shark (Carcharhinus leucas) faces varying levels of exploitation around the world due to its coastal distribution. Information regarding population connectivity is crucial to evaluate its conservation status and local fishing impacts. In this study, we sampled 922 putative Bull Sharks from 19 locations in the first global assessment of population structure of this cosmopolitan species. Using a recently developed DNA-capture approach (DArTcap), samples were genotyped for 3400 nuclear markers. Additionally, full mitochondrial genomes of 384 Indo-Pacific samples were sequenced. Reproductive isolation was found between and across ocean basins (eastern Pacific, western Atlantic, eastern Atlantic, Indo-West Pacific) with distinct island populations in Japan and Fiji. Bull Sharks appear to maintain gene flow using shallow coastal waters as dispersal corridors, whereas large oceanic distances and historical land-bridges act as barriers. Females tend to return to the same area for reproduction, making them more susceptible to local threats and an important focus for management actions. Given these behaviors, the exploitation of Bull Sharks from insular populations, such as Japan and Fiji, may instigate local decline that cannot readily be replenished by immigration, which can in turn affect ecosystem dynamics and functions. These data also supported the development of a genetic panel to ascertain the population of origin, which will be useful in monitoring the trade of fisheries products and assessing population-level impacts of this harvest.

Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers.

Resolving the identity, phylogeny and distribution of cryptic species within species complexes is an essential precursor to management. The bonnethead shark, Sphyrna tiburo, is a small coastal shark distributed in the Western Atlantic from North Carolina (U.S.A.) to southern Brazil. Genetic analyses based on mitochondrial markers revealed that bonnethead sharks comprise a species complex with at least two lineages in the Northwestern Atlantic and the Caribbean (S. tiburo and Sphyrna aff. tiburo, respectively). The phylogeographic and phylogenetic analysis of two mitochondrial markers [control region (mtCR) and cytochrome oxidase I (COI)] showed that bonnethead sharks from southeastern Brazil correspond to S. aff. tiburo, extending the distribution of this cryptic species >5000 km. Bonnethead shark populations are only managed in the U.S.A. and in the 2000s were considered to be regionally extinct or collapsed in southeast Brazil. The results indicate that there is significant genetic differentiation between S. aff. tiburo from Brazil and other populations from the Caribbean (ΦST  = 0.9053, P < 0.000), which means that collapsed populations in the former are unlikely to be replenished from Caribbean immigration. The species identity of bonnethead sharks in the Southwest Atlantic and their relationship to North Atlantic and Caribbean populations still remains unresolved. Taxonomic revision and further sampling are required to reevaluate the status of the bonnethead shark complex through its distribution range.

Moray eels are more common on coral reefs subject to higher human pressure in the greater Caribbean.

Proximity and size of the nearest market ('market gravity') have been shown to have strong negative effects on coral reef fish communities that can be mitigated by the establishment of closed areas. However, moray eels are functionally unique predators that are generally not subject to targeted fishing and should therefore not directly be affected by these factors. We used baited remote underwater video systems to investigate associations between morays and anthropogenic, habitat, and ecological factors in the Caribbean region. Market gravity had a positive effect on morays, while the opposite pattern was observed in a predator group subject to exploitation (sharks). Environmental DNA analyses corroborated the positive effect of market gravity on morays. We hypothesize that the observed pattern could be the indirect result of the depletion of moray competitors and predators near humans.

Using fisher-contributed secondary fins to fill critical shark-fisheries data gaps.

Developing-world shark fisheries are typically not assessed or actively managed for sustainability; one fundamental obstacle is the lack of species and size-composition catch data. We tested and implemented a new and potentially widely applicable approach for collecting these data: mandatory submission of low-value secondary fins (anal fins) from landed sharks by fishers and use of the fins to reconstruct catch species and size. Visual and low-cost genetic identification were used to determine species composition, and linear regression was applied to total length and anal fin base length for catch-size reconstruction. We tested the feasibility of this approach in Belize, first in a local proof-of-concept study and then scaling it up to the national level for the 2017-2018 shark-fishing season (1,786 fins analyzed). Sixteen species occurred in this fishery. The most common were the Caribbean reef (Carcharhinus perezi), blacktip (C. limbatus), sharpnose (Atlantic [Rhizoprionodon terraenovae] and Caribbean [R. porosus] considered as a group), and bonnethead (Sphyrna cf. tiburo). Sharpnose and bonnethead sharks were landed primarily above size at maturity, whereas Caribbean reef and blacktip sharks were primarily landed below size at maturity. Our approach proved effective in obtaining critical data for managing the shark fishery, and we suggest the tools developed as part of this program could be exported to other nations in this region and applied almost immediately if there were means to communicate with fishers and incentivize them to provide anal fins. Outside the tropical Western Atlantic, we recommend further investigation of the feasibility of sampling of secondary fins, including considerations of time, effort, and cost of species identification from these fins, what secondary fin type to use, and the means with which to communicate with fishers and incentivize participation. This program could be a model for collecting urgently needed data for developing-world shark fisheries globally. Article impact statement: Shark fins collected from fishers yield data critical to shark fisheries management in developing nations.

Uso de Aletas Secundarias Proporcionadas por Pescadores para Llenar Vacíos Importantes de Información sobre las Pesquerías de Tiburones Resumen Con frecuencia no se evalúan las pesquerías de tiburones del mundo en desarrollo ni cuentan con un manejo activo de sustentabilidad. Uno de los principales obstáculos para esto es la falta de información sobre las especies y la composición de los tamaños en las capturas. Probamos e implementamos una estrategia nueva y potencialmente aplicable en todas partes para la recolección de estos datos: la entrega obligatoria de las aletas secundarias de bajo valor económico (aletas anales) obtenidas de los tiburones desembarcados por parte de los pescadores y el uso de estas aletas para reconstruir las especies y tamaños en la captura. Usamos identificaciones genéticas de bajo costo e identificaciones visuales para determinar la composición de las especies y aplicamos una regresión lineal a la longitud total y a la de la base de la aleta anal para la reconstrucción del tamaño en captura. Probamos la viabilidad de esta estrategia en Belice, primero en un estudio de prueba de concepto y después subiendo al nivel nacional para la temporada de pesca de tiburón 2017-2018 (1,786 aletas analizadas). Se registraron 16 especies en esta pesquería. Las más comunes fueron Carcharhinus perezi, C. limbatus, Rhizoprionodon terraenovae y R. porosus (consideradas como un grupo) y Sphyrna cf. tiburo. Las últimas tres especies fueron desembarcadas principalmente por encima del tamaño maduro, mientras que con las dos primeras especies lo hacían por debajo del tamaño maduro. Nuestra estrategia demostró ser efectiva en la obtención de información crítica para el manejo de la pesquería de tiburones y sugerimos que las herramientas desarrolladas como parte de este programa puedan ser exportadas a otras naciones en esta región y aplicadas casi de manera inmediata si existen los medios para comunicarse con los pescadores e incentivarlos a proporcionar las aletas anales. Fuera del Atlántico Occidental tropical, recomendamos una mayor investigación de la viabilidad del muestreo de aletas secundarias, incluyendo la consideración del tiempo, esfuerzo y costo de la identificación de especies a partir de estas aletas; cuál tipo de aleta secundaria utilizar; y los medios mediante los cuales comunicarse con los pescadores e incentivarlos a participar. Este programa podría ser un modelo para la recolección de información de necesidad urgente para las pesquerías del mundo en desarrollo.

Elucidating shark diets with DNA metabarcoding from cloacal swabs.

Animal dietary information provides the foundation for understanding trophic relationships, which is essential for ecosystem management. Yet, in marine systems, high-resolution diet reconstruction tools are currently under-developed. This is particularly pertinent for large marine vertebrates, for which direct foraging behaviour is difficult or impossible to observe and, due to their conservation status, the collection of stomach contents at adequate sample sizes is frequently impossible. Consequently, the diets of many groups, such as sharks, have largely remained unresolved. To address this knowledge gap, we applied metabarcoding to prey DNA in faecal residues (fDNA) collected on cotton swabs from the inside of a shark's cloaca. We used a previously published primer set targeting a small section of the 12S rRNA mitochondrial gene to amplify teleost prey species DNA. We tested the utility of this method in a controlled feeding experiment with captive juvenile lemon sharks (Negaprion brevirostris) and on free-ranging juvenile bull sharks (Carcharhinus leucas). In the captive trial, we successfully isolated and correctly identified teleost prey DNA without incurring environmental DNA contamination from the surrounding seawater. In the field, we were able to reconstruct high-resolution teleost dietary information from juvenile C. leucas fDNA that was generally consistent with expectations based on published diet studies of this species. While further investigation is needed to validate the method for larger sharks and other species, it is expected to be broadly applicable to aquatic vertebrates and provides an opportunity to advance our understanding of trophic interactions in marine and freshwater systems.

Annual breeding in a captive smalltooth sawfish, Pristis pectinata.

The critically endangered smalltooth sawfish Pristis pectinata reproduces biennially in central west Florida, U.S.A. Here we demonstrate that smalltooth sawfish are physiologically capable of reproducing annually in a captive environment. The smalltooth sawfish are held in an open system, with abiotic conditions that vary naturally with the surrounding environment in The Bahamas. This suggests wild smalltooth sawfish may also be capable of annual reproduction provided there are adequate prey resources, limited competition and mate availability.

Author Correction: Global status and conservation potential of reef sharks.

An Amendment to this paper has been published and can be accessed via a link at the top of the paper.

Species composition of the largest shark fin retail-market in mainland China.

Species-specific monitoring through large shark fin market surveys has been a valuable data source to estimate global catches and international shark fin trade dynamics. Hong Kong and Guangzhou, mainland China, are the largest shark fin markets and consumption centers in the world. We used molecular identification protocols on randomly collected processed fin trimmings (n = 2000) and non-parametric species estimators to investigate the species composition of the Guangzhou retail market and compare the species diversity between the Guangzhou and Hong Kong shark fin retail markets. Species diversity was similar between both trade hubs with a small subset of species dominating the composition. The blue shark (Prionace glauca) was the most common species overall followed by the CITES-listed silky shark (Carcharhinus falciformis), scalloped hammerhead shark (Sphyrna lewini), smooth hammerhead shark (S. zygaena) and shortfin mako shark (Isurus oxyrinchus). Our results support previous indications of high connectivity between the shark fin markets of Hong Kong and mainland China and suggest that systematic studies of other fin trade hubs within Mainland China and stronger law-enforcement protocols and capacity building are needed.

Global status and conservation potential of reef sharks.

Decades of overexploitation have devastated shark populations, leaving considerable doubt as to their ecological status1,2. Yet much of what is known about sharks has been inferred from catch records in industrial fisheries, whereas far less information is available about sharks that live in coastal habitats3. Here we address this knowledge gap using data from more than 15,000 standardized baited remote underwater video stations that were deployed on 371 reefs in 58 nations to estimate the conservation status of reef sharks globally. Our results reveal the profound impact that fishing has had on reef shark populations: we observed no sharks on almost 20% of the surveyed reefs. Reef sharks were almost completely absent from reefs in several nations, and shark depletion was strongly related to socio-economic conditions such as the size and proximity of the nearest market, poor governance and the density of the human population. However, opportunities for the conservation of reef sharks remain: shark sanctuaries, closed areas, catch limits and an absence of gillnets and longlines were associated with a substantially higher relative abundance of reef sharks. These results reveal several policy pathways for the restoration and management of reef shark populations, from direct top-down management of fishing to indirect improvement of governance conditions. Reef shark populations will only have a high chance of recovery by engaging key socio-economic aspects of tropical fisheries.

Environmental DNA detection tracks established seasonal occurrence of blacktip sharks (Carcharhinus limbatus) in a semi-enclosed subtropical bay.

The integration of eDNA analysis into the population assessment and monitoring of sharks could greatly improve temporal and spatial data used for management purposes. This study aimed to compare eDNA detection against well-established seasonal changes in blacktip shark (Carcharhinus limbatus) abundance in Terra Ceia Bay (FL, USA). We used a species-specific real-time PCR approach to detect C. limbatus eDNA in the bay on a near monthly basis from spring through mid-fall in 2018 and 2019. Previous studies have shown that C. limbatus give birth in the bay in early summer and immature sharks occur there until late fall, when decreasing water temperatures cause them to move offshore and southwards. Water samples (2 L) were collected (4-6 per month) and filtered in the field, with each then being subjected to real-time PCR. Carcharhinus limbatus 'positive' filters were significantly more commonly collected during the April-July sampling period than during the August-October sampling period. While following the predicted pattern, eDNA concentration was generally too low for accurate quantification. Our results show that C. limbatus eDNA detection follows known seasonal residency patterns consistently over 2 years of monitoring. Species-specific eDNA analysis using real-time PCR could therefore represent a cost-effective, scalable sampling tool to facilitate improved shark population monitoring in semi-enclosed marine habitats.

An encounter between a pelagic shark and giant cephalopod.

An oceanic whitetip shark (Carcharhinus longimanus) was observed off the coast of Kona, Hawaii, with scars caused by the tentacles of a large cephalopod. While the exact species could not be confirmed, candidate species include the giant squid (Architeuthis dux) or species from the genera Thysanoteuthis (flying squids) and Megalocranchia (glass squids). Telemetry shows C. longimanus will dive within the mesopelagic zone and may interact with or even forage for large cephalopods.

Mercury and arsenic in processed fins from nine of the most traded shark species in the Hong Kong and China dried seafood markets: The potential health risks of shark fin soup.

Shark fin is one of Asia's most valued dried seafood products, with over 80 shark species traded in Hong Kong [HK]. We analyzed processed shark fins from mainland China and HK markets (n = 267) for mercury, methyl­mercury, and arsenic, to inform consumers, policy makers and public health officials on the health risks of ingesting fins from nine of the most common shark species in the fin trade. Fins from all species frequently exceed Hg limits established by HK authorities. Most of the mercury found is in the form of methyl­mercury (69.0 ± 33.5%). Five species surpass methyl­mercury PTWIs and blue shark fins can exceed inorganic arsenic BMDL0.5. Species-of-origin was a significant predictor of heavy metal concentrations, with higher mercury concentrations associated with coastal sharks and lower arsenic levels found with increasing shark trophic level. Species-specific labeling would help consumers avoid shark fin products that pose the highest health risk.

Microsatellite primer development in elasmobranchs using next generation sequencing of enriched libraries.

Microsatellites are useful in studies of population genetics, sibship, and parentage. Here, we screened for microsatellites from multiple elasmobranch genomic libraries using an enrichment protocol followed by sequencing on an Illumina platform. We concurrently screened five and then nine genomes and describe the number of potential loci from each respective round of sequencing. To validate the efficacy of the protocol, we developed and tested primers for the pelagic thresher shark, Alopias pelagicus. The method described here is a cost-effective protocol to increase the pool of potential useful loci and allows the concurrent screening of multiple libraries.

Individual and Population Benefits of Marine Reserves for Reef Sharks.

No-take marine protected areas (MPAs) are a commonly applied tool to reduce human fishing impacts on marine and coastal ecosystems. However, conservation outcomes of MPAs for mobile and long-lived predators such as sharks are highly variable. Here, we use empirical animal tracking data from 459 individual sharks and baited remote underwater video surveys undertaken in 36 countries to construct an empirically supported individual-based model that estimates the conservation effectiveness of MPAs for five species of coral reef-associated sharks (Triaenodon obesus, Carcharhinus melanopterus, Carcharhinus amblyrhynchos, Carcharhinus perezi, and Ginglymostoma cirratum). We demonstrate how species-specific individual movement traits can contribute to fishing mortality of sharks found within MPAs as they move outside to adjacent fishing grounds. We discovered that the world's officially recorded coral reef-based managed areas (with a median width of 9.4 km) would need to be enforced as strict no-take MPAs and up to 5 times larger to expect protection of the majority of individuals of the five investigated reef shark species. The magnitude of this effect depended on local abundances and fishing pressure, with MPAs required to be 1.6-2.6 times larger to protect the same number of Atlantic and Caribbean species, which occur at lower abundances than similar species in the western Pacific. Furthermore, our model was used to quantify partially substantial reductions (>50%) in fishing mortality resulting from small increases in MPA size, allowing us to bridge a critical gap between traditional conservation planning and fisheries management. Overall, our results highlight the challenge of relying on abundance data alone to ensure that estimates of shark conservation impacts of MPAs follow the precautionary approach.

Global spatial risk assessment of sharks under the footprint of fisheries.

Effective ocean management and the conservation of highly migratory species depend on resolving the overlap between animal movements and distributions, and fishing effort. However, this information is lacking at a global scale. Here we show, using a big-data approach that combines satellite-tracked movements of pelagic sharks and global fishing fleets, that 24% of the mean monthly space used by sharks falls under the footprint of pelagic longline fisheries. Space-use hotspots of commercially valuable sharks and of internationally protected species had the highest overlap with longlines (up to 76% and 64%, respectively), and were also associated with significant increases in fishing effort. We conclude that pelagic sharks have limited spatial refuge from current levels of fishing effort in marine areas beyond national jurisdictions (the high seas). Our results demonstrate an urgent need for conservation and management measures at high-seas hotspots of shark space use, and highlight the potential of simultaneous satellite surveillance of megafauna and fishers as a tool for near-real-time, dynamic management.

Biodiversity assessment of tropical shelf eukaryotic communities via pelagic eDNA metabarcoding.

Our understanding of marine communities and their functions in an ecosystem relies on the ability to detect and monitor species distributions and abundances. Currently, the use of environmental DNA (eDNA) metabarcoding is increasingly being applied for the rapid assessment and monitoring of aquatic species. Most eDNA metabarcoding studies have either focussed on the simultaneous identification of a few specific taxa/groups or have been limited in geographical scope. Here, we employed eDNA metabarcoding to compare beta diversity patterns of complex pelagic marine communities in tropical coastal shelf habitats spanning the whole Caribbean Sea. We screened 68 water samples using a universal eukaryotic COI barcode region and detected highly diverse communities, which varied significantly among locations, and proved good descriptors of habitat type and environmental conditions. Less than 15% of eukaryotic taxa were assigned to metazoans, most DNA sequences belonged to a variety of planktonic "protists," with over 50% of taxa unassigned at the phylum level, suggesting that the sampled communities host an astonishing amount of micro-eukaryotic diversity yet undescribed or absent from COI reference databases. Although such a predominance of micro-eukaryotes severely reduces the efficiency of universal COI markers to investigate vertebrate and other metazoans from aqueous eDNA, the study contributes to the advancement of rapid biomonitoring methods and brings us closer to a full inventory of extant marine biodiversity.