Directed conservation of the world's reef sharks and rays.

Many shark populations are in decline around the world, with severe ecological and economic consequences. Fisheries management and marine protected areas (MPAs) have both been heralded as solutions. However, the effectiveness of MPAs alone is questionable, particularly for globally threatened sharks and rays ('elasmobranchs'), with little known about how fisheries management and MPAs interact to conserve these species. Here we use a dedicated global survey of coral reef elasmobranchs to assess 66 fully protected areas embedded within a range of fisheries management regimes across 36 countries. We show that conservation benefits were primarily for reef-associated sharks, which were twice as abundant in fully protected areas compared with areas open to fishing. Conservation benefits were greatest in large protected areas that incorporate distinct reefs. However, the same benefits were not evident for rays or wide-ranging sharks that are both economically and ecologically important while also threatened with extinction. We show that conservation benefits from fully protected areas are close to doubled when embedded within areas of effective fisheries management, highlighting the importance of a mixed management approach of both effective fisheries management and well-designed fully protected areas to conserve tropical elasmobranch assemblages globally.

From little things big things grow: enhancement of an acoustic telemetry network to monitor broad-scale movements of marine species along Australia's east coast.

BACKGROUND: Acoustic telemetry has become a fundamental tool to monitor the movement of aquatic species. Advances in technology, in particular the development of batteries with lives of > 10 years, have increased our ability to track the long-term movement patterns of many species. However, logistics and financial constraints often dictate the locations and deployment duration of acoustic receivers. Consequently, there is often a compromise between optimal array design and affordability. Such constraints can hinder the ability to track marine animals over large spatial and temporal scales. Continental-scale receiver networks have increased the ability to study large-scale movements, but significant gaps in coverage often remain. METHODS: Since 2007, the Integrated Marine Observing System's Animal Tracking Facility (IMOS ATF) has maintained permanent receiver installations on the eastern Australian seaboard. In this study, we present the recent enhancement of the IMOS ATF acoustic tracking infrastructure in Queensland to collect data on large-scale movements of marine species in the northeast extent of the national array. Securing a relatively small initial investment for expanding receiver deployment and tagging activities in Queensland served as a catalyst, bringing together a diverse group of stakeholders (research institutes, universities, government departments, port corporations, industries, Indigenous ranger groups and tourism operators) to create an extensive collaborative network that could sustain the extended receiver coverage into the future. To fill gaps between existing installations and maximise the monitoring footprint, the new initiative has an atypical design, deploying many single receivers spread across 2,100 km of Queensland waters. RESULTS: The approach revealed previously unknown broad-scale movements for some species and highlights that clusters of receivers are not always required to enhance data collection. However, array designs using predominantly single receiver deployments are more vulnerable to data gaps when receivers are lost or fail, and therefore "redundancy" is a critical consideration when designing this type of array. CONCLUSION: Initial results suggest that our array enhancement, if sustained over many years, will uncover a range of previously unknown movements that will assist in addressing ecological, fisheries, and conservation questions for multiple species.

Fishing for oil and meat drives irreversible defaunation of deepwater sharks and rays.

The deep ocean is the last natural biodiversity refuge from the reach of human activities. Deepwater sharks and rays are among the most sensitive marine vertebrates to overexploitation. One-third of threatened deepwater sharks are targeted, and half the species targeted for the international liver-oil trade are threatened with extinction. Steep population declines cannot be easily reversed owing to long generation lengths, low recovery potentials, and the near absence of management. Depth and spatial limits to fishing activity could improve conservation when implemented alongside catch regulations, bycatch mitigation, and international trade regulation. Deepwater sharks and rays require immediate trade and fishing regulations to prevent irreversible defaunation and promote recovery of this threatened megafauna group.

Elemental analysis of vertebrae discerns diadromous movements of threatened non-marine elasmobranchs.

River sharks (Glyphis spp.) and some sawfishes (Pristidae) inhabit riverine environments, although their long-term habitat use patterns are poorly known. We investigated the diadromous movements of the northern river shark (Glyphis garricki), speartooth shark (Glyphis glyphis), narrow sawfish (Anoxypristis cuspidata), and largetooth sawfish (Pristis pristis) using in situ laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) on vertebrae to recover elemental ratios over each individual's lifetime. We also measured elemental ratios for the bull shark (Carcharhinus leucas) and a range of inshore and offshore stenohaline marine species to assist in interpretation of results. Barium (Ba) was found to be an effective indicator of freshwater use, whereas lithium (Li) and strontium (Sr) were effective indicators of marine water use. The relationships between Ba and Li and Ba and Sr were negatively correlated, whereas the relationship between Li and Sr was positively correlated. Both river shark species had elemental signatures indicative of prolonged use of upper-estuarine environments, whereas adults appear to mainly use lower-estuarine environments rather than marine environments. Decreases in Li:Ba and Sr:Ba at the end of the prenatal growth zone of P. pristis samples indicated that parturition likely occurs in fresh water. There was limited evidence of prolonged riverine habitat use for A. cuspidata. The results of this study support elemental-environment relationships observed in teleost otoliths and indicate that in situ LA-ICP-MS elemental characterization is applicable to a wide range of elasmobranch species as a discriminator for use and movement across salinity gradients. A greater understanding of processes that lead to element incorporation in vertebrae, and relative concentrations in vertebrae with respect to the ambient environment, will improve the applicability of elemental analysis to understand movements across the life history of elasmobranchs into the future.

Widespread diversity deficits of coral reef sharks and rays.

A global survey of coral reefs reveals that overfishing is driving resident shark species toward extinction, causing diversity deficits in reef elasmobranch (shark and ray) assemblages. Our species-level analysis revealed global declines of 60 to 73% for five common resident reef shark species and that individual shark species were not detected at 34 to 47% of surveyed reefs. As reefs become more shark-depleted, rays begin to dominate assemblages. Shark-dominated assemblages persist in wealthy nations with strong governance and in highly protected areas, whereas poverty, weak governance, and a lack of shark management are associated with depauperate assemblages mainly composed of rays. Without action to address these diversity deficits, loss of ecological function and ecosystem services will increasingly affect human communities.

Scaling of Activity Space in Marine Organisms across Latitudinal Gradients.

AbstractUnifying models have shown that the amount of space used by animals (e.g., activity space, home range) scales allometrically with body mass for terrestrial taxa; however, such relationships are far less clear for marine species. We compiled movement data from 1,596 individuals across 79 taxa collected using a continental passive acoustic telemetry network of acoustic receivers to assess allometric scaling of activity space. We found that ectothermic marine taxa do exhibit allometric scaling for activity space, with an overall scaling exponent of 0.64. However, body mass alone explained only 35% of the variation, with the remaining variation best explained by trophic position for teleosts and latitude for sharks, rays, and marine reptiles. Taxon-specific allometric relationships highlighted weaker scaling exponents among teleost fish species (0.07) than sharks (0.96), rays (0.55), and marine reptiles (0.57). The allometric scaling relationship and scaling exponents for the marine taxonomic groups examined were lower than those reported from studies that had collated both marine and terrestrial species data derived using various tracking methods. We propose that these disparities arise because previous work integrated summarized data across many studies that used differing methods for collecting and quantifying activity space, introducing considerable uncertainty into slope estimates. Our findings highlight the benefit of using large-scale, coordinated animal biotelemetry networks to address cross-taxa evolutionary and ecological questions.

Half a century of rising extinction risk of coral reef sharks and rays.

Sharks and rays are key functional components of coral reef ecosystems, yet many populations of a few species exhibit signs of depletion and local extinctions. The question is whether these declines forewarn of a global extinction crisis. We use IUCN Red List to quantify the status, trajectory, and threats to all coral reef sharks and rays worldwide. Here, we show that nearly two-thirds (59%) of the 134 coral-reef associated shark and ray species are threatened with extinction. Alongside marine mammals, sharks and rays are among the most threatened groups found on coral reefs. Overfishing is the main cause of elevated extinction risk, compounded by climate change and habitat degradation. Risk is greatest for species that are larger-bodied (less resilient and higher trophic level), widely distributed across several national jurisdictions (subject to a patchwork of management), and in nations with greater fishing pressure and weaker governance. Population declines have occurred over more than half a century, with greatest declines prior to 2005. Immediate action through local protections, combined with broad-scale fisheries management and Marine Protected Areas, is required to avoid extinctions and the loss of critical ecosystem function condemning reefs to a loss of shark and ray biodiversity and ecosystem services, limiting livelihoods and food security.

Conservation successes and challenges for wide-ranging sharks and rays.

Overfishing is the most significant threat facing sharks and rays. Given the growth in consumption of seafood, combined with the compounding effects of habitat loss, climate change, and pollution, there is a need to identify recovery paths, particularly in poorly managed and poorly monitored fisheries. Here, we document conservation through fisheries management success for 11 coastal sharks in US waters by comparing population trends through a Bayesian state-space model before and after the implementation of the 1993 Fisheries Management Plan for Sharks. We took advantage of the spatial and temporal gradients in fishing exposure and fisheries management in the Western Atlantic to analyze the effect on the Red List status of all 26 wide-ranging coastal sharks and rays. We show that extinction risk was greater where fishing pressure was higher, but this was offset by the strength of management engagement (indicated by strength of National and Regional Plan of Action for sharks and rays). The regional Red List Index (which tracks changes in extinction risk through time) declined in all regions until the 1980s but then improved in the North and Central Atlantic such that the average extinction risk is currently half that in the Southwest. Many sharks and rays are wide ranging, and successful fisheries management in one country can be undone by poorly regulated or unregulated fishing elsewhere. Our study underscores that well-enforced, science-based management of carefully monitored fisheries can achieve conservation success, even for slow-growing species.

Conceptual frameworks and key questions for assessing the contribution of marine protected areas to shark and ray conservation.

Marine protected areas (MPAs) are key tools in addressing the global decline of sharks and rays, and marine parks and shark sanctuaries of various configurations have been established to conserve shark populations. However, assessments of their efficacy are compromised by inconsistent terminology, lack of standardized approaches to assess how MPAs contribute to shark and ray conservation, and ambiguity about how to integrate movement data in assessment processes. We devised a conceptual framework to standardize key terms (e.g., protection, contribution, potential impact, risk, threat) and used the concept of portfolio risk to identify key attributes of sharks and rays (assets), the threats they face (portfolio risk), and the specific role of MPAs in risk mitigation (insurance). Movement data can be integrated into the process by informing risk exposure and mitigation through MPAs. The framework is operationalized by posing 8 key questions that prompt practitioners to consider the assessment scope, MPA type and purpose, range of existing and potential threats, species biology and ecology, and management and operational contexts. Ultimately, MPA contributions to shark and ray conservation differ according to a complex set of human and natural factors and interactions that should be carefully considered in MPA design, implementation, and evaluation.

Marcos conceptuales y preguntas clave para evaluar la contribución de las áreas marinas protegidas a la conservación de tiburones y rayas Resumen Las áreas marinas protegidas (AMP) son herramientas importantes para manejar la declinación mundial de tiburones y rayas, por lo que se han establecido parques marinos y santuarios de diversas configuraciones para conservar las poblaciones de tiburones. Sin embargo, el análisis de su eficiencia está compuesto por una terminología inconstante, la falta de estrategias estandarizadas para evaluar cómo las AMP contribuyen a la conservación de tiburones y rayas, y una ambigüedad sobre cómo integrar la información sobre movimientos en los procesos de evaluación. Diseñamos un marco conceptual para estandarizar los términos más importantes (p. ej.: protección, contribución, impacto potencial, amenaza, riesgo) y usamos el concepto de riesgo de portafolio para identificar los atributos clave de los tiburones y las rayas (activos), las amenazas que enfrentan (riesgo de portafolio) y el papel específico que juegan las AMP en la mitigación del riesgo (seguro). La información sobre los movimientos puede integrarse al proceso al guiar la exposición y mitigación del riesgo con las AMP. El marco conceptual es operado con el planteamiento de ocho preguntas clave que invitan a los practicantes a considerar el enfoque de la evaluación, el tipo de AMP y su propósito, gama de amenazas existentes y potenciales, la biología y ecología de las especies, y los contextos operativos y de manejo. Finalmente, las contribuciones que tienen las AMP a la conservación de los tiburones y las rayas difieren de acuerdo con un conjunto complejo de factores naturales y humanos e interacciones que deberían considerarse cuidadosamente en el diseño, implementación y evaluación de la AMP.

Different Genes are Recruited During Convergent Evolution of Pregnancy and the Placenta.

The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins of live birth in vertebrates, providing a uniquely powerful system to test the mechanisms underpinning convergence in morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within the uterus. Since many previous studies detected qualitative similarities in gene use during independent origins of pregnancy, we expected to find significant overlap in gene use in viviparous taxa. However, we found no more overlap in uterine gene expression associated with viviparity than we would expect by chance alone. Each viviparous lineage exhibits the same core set of uterine physiological functions. Yet, contrary to prevailing assumptions about this trait, we find that none of the same genes are differentially expressed in all viviparous lineages, or even in all viviparous amniote lineages. Therefore, across distantly related vertebrates, different genes have been recruited to support the morphological and physiological changes required for successful pregnancy. We conclude that redundancies in gene function have enabled the repeated evolution of viviparity through recruitment of different genes from genomic "toolboxes", which are uniquely constrained by the ancestries of each lineage.

Structure and permeability of the egg capsule of the placental Australian sharpnose shark, Rhizoprionodon taylori.

Shark placentae are derived from modifications to the fetal yolk sac and the maternal uterine mucosa. In almost all placental sharks, embryonic development occurs in an egg capsule that remains intact for the entire pregnancy, separating the fetal tissues from the maternal tissues at the placental interface. Here, we investigate the structure and permeability of the egg capsules that surround developing embryos of the placental Australian sharpnose shark (Rhizoprionodon taylori) during late pregnancy. The egg capsule is an acellular fibrous structure that is 0.42 ± 0.04 µm thick at the placental interface between the yolk sac and uterine tissues, and 0.67 ± 0.08 µm thick in the paraplacental regions. This is the thinnest egg capsule of any placental shark measured so far, which may increase the diffusion rate of respiratory gases, fetal wastes, water and nutrients between maternal and fetal tissues. Molecules smaller than or equal to ~ 1000 Da can diffuse through the egg capsule, but larger proteins (~ 3000-26,000 Da) cannot. Similar permeability characteristics between the egg capsule of R. taylori and other placental sharks suggest that molecular size is an important determinant of the molecules that can be exchanged between the mother and her embryos during pregnancy.

Global trends in aquatic animal tracking with acoustic telemetry.

Acoustic telemetry (AT) is a rapidly evolving technique used to track the movements of aquatic animals. As the capacity of AT research expands it is important to optimize its relevance to management while still pursuing key ecological questions. A global review of AT literature revealed region-specific research priorities underscoring the breadth of how AT is applied, but collectively demonstrated a lack of management-driven objectives, particularly relating to fisheries, climate change, and protection of species. In addition to the need for more research with direct pertinence to management, AT research should prioritize ongoing efforts to create collaborative opportunities, establish long-term and ecosystem-based monitoring, and utilize technological advancements to bolster aquatic policy and ecological understanding worldwide.

Overfishing drives over one-third of all sharks and rays toward a global extinction crisis.

The scale and drivers of marine biodiversity loss are being revealed by the International Union for Conservation of Nature (IUCN) Red List assessment process. We present the first global reassessment of 1,199 species in Class Chondrichthyes-sharks, rays, and chimeras. The first global assessment (in 2014) concluded that one-quarter (24%) of species were threatened. Now, 391 (32.6%) species are threatened with extinction. When this percentage of threat is applied to Data Deficient species, more than one-third (37.5%) of chondrichthyans are estimated to be threatened, with much of this change resulting from new information. Three species are Critically Endangered (Possibly Extinct), representing possibly the first global marine fish extinctions due to overfishing. Consequently, the chondrichthyan extinction rate is potentially 25 extinctions per million species years, comparable to that of terrestrial vertebrates. Overfishing is the universal threat affecting all 391 threatened species and is the sole threat for 67.3% of species and interacts with three other threats for the remaining third: loss and degradation of habitat (31.2% of threatened species), climate change (10.2%), and pollution (6.9%). Species are disproportionately threatened in tropical and subtropical coastal waters. Science-based limits on fishing, effective marine protected areas, and approaches that reduce or eliminate fishing mortality are urgently needed to minimize mortality of threatened species and ensure sustainable catch and trade of others. Immediate action is essential to prevent further extinctions and protect the potential for food security and ecosystem functions provided by this iconic lineage of predators.

Investigating links between thermal tolerance and oxygen supply capacity in shark neonates from a hyperoxic tropical environment.

Temperature and oxygen limit the distribution of marine ectotherms. Haematological traits underlying blood-oxygen carrying capacity are thought to be correlated with thermal tolerance in certain fishes, and this relationship is hypothesised to be explained by oxygen supply capacity. We tested this hypothesis using reef shark neonates as experimental models because they live near their upper thermal limits and are physiologically sensitive to low oxygen conditions. We first described in situ associations between temperature and oxygen at the study site (Moorea, French Polynesia) and found that the habitats for reef shark neonates (Carcharhinus melanopterus and Negaprion acutidens) were hyperoxic at the maximum recorded temperatures. Next, we tested for in situ associations between thermal habitat characteristics and haematological traits of neonates. Contrary to predictions, we only demonstrated a negative association between haemoglobin concentration and maximum habitat temperatures in C. melanopterus. Next, we tested for ex situ associations between critical thermal maximum (CTMax) and haematological traits, but only demonstrated a negative association between haematocrit and CTMax in C. melanopterus. Finally, we measured critical oxygen tension (pcrit) ex situ and estimated its temperature sensitivity to predict oxygen-dependent values of CTMax. Estimated temperature sensitivity of pcrit was similar to reported values for sharks and skates, and predicted values for CTMax equalled maximum habitat temperatures. These data demonstrate unique associations between haematological traits and thermal tolerance in a reef shark that are likely not explained by oxygen supply capacity. However, a relationship between oxygen supply capacity and thermal tolerance remains to be demonstrated empirically.

Structure of the paraplacenta and the yolk sac placenta of the viviparous Australian sharpnose shark, Rhizoprionodon taylori.

INTRODUCTION: Viviparity (live-birth) has evolved from oviparity (egg-laying) multiple times in sharks. While most transitions from oviparity to viviparity have resulted in non-placental forms of viviparity, some sharks develop a yolk sac placenta during pregnancy. The Australian sharpnose shark (Rhizoprionodon taylori) is a placental species that suspends embryonic development in a diapause for most of pregnancy. METHODS: To identify structures involved in supporting rapid embryonic growth in late pregnancy, we examined uterine and placental morphology by light and electron microscopy. RESULTS: Paraplacental uterine regions have morphological specialisations consistent with secretion and fluid transport between uterine tissues and the lumen. Uterine secretions in the lumen may be absorbed by the outgrowths on the embryonic umbilical cord ('appendiculae'), which are densely covered by microvilli. The placenta consists of uterine villi that interdigitate with the yolk sac and enhance the surface area available for fetomaternal exchange. The yolk sac does not invade the uterine epithelium, and the egg capsule remains intact at the placental interface, separating maternal and fetal tissues. Some placental uterine epithelial cells are secretory, and endocytic vesicles in the opposing yolk sac ectodermal cells suggest that nutrient transport is by histotrophic uterine secretion followed by fetal absorption. Respiratory gases, water and possibly small nutrients likely diffuse across the placenta, where maternal and fetal blood vessels are ~2 µm apart. DISCUSSION: Placental structure in R. taylori is similar to most other sharks, but there are differences in cellular structures between species that may indicate species-specific placental transport mechanisms.

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.

Half a century of global decline in oceanic sharks and rays.

Overfishing is the primary cause of marine defaunation, yet declines in and increasing extinction risks of individual species are difficult to measure, particularly for the largest predators found in the high seas1-3. Here we calculate two well-established indicators to track progress towards Aichi Biodiversity Targets and Sustainable Development Goals4,5: the Living Planet Index (a measure of changes in abundance aggregated from 57 abundance time-series datasets for 18 oceanic shark and ray species) and the Red List Index (a measure of change in extinction risk calculated for all 31 oceanic species of sharks and rays). We find that, since 1970, the global abundance of oceanic sharks and rays has declined by 71% owing to an 18-fold increase in relative fishing pressure. This depletion has increased the global extinction risk to the point at which three-quarters of the species comprising this functionally important assemblage are threatened with extinction. Strict prohibitions and precautionary science-based catch limits are urgently needed to avert population collapse6,7, avoid the disruption of ecological functions and promote species recovery8,9.