Protecting the global ocean for biodiversity, food and climate.

The ocean contains unique biodiversity, provides valuable food resources and is a major sink for anthropogenic carbon. Marine protected areas (MPAs) are an effective tool for restoring ocean biodiversity and ecosystem services1,2, but at present only 2.7% of the ocean is highly protected3. This low level of ocean protection is due largely to conflicts with fisheries and other extractive uses. To address this issue, here we developed a conservation planning framework to prioritize highly protected MPAs in places that would result in multiple benefits today and in the future. We find that a substantial increase in ocean protection could have triple benefits, by protecting biodiversity, boosting the yield of fisheries and securing marine carbon stocks that are at risk from human activities. Our results show that most coastal nations contain priority areas that can contribute substantially to achieving these three objectives of biodiversity protection, food provision and carbon storage. A globally coordinated effort could be nearly twice as efficient as uncoordinated, national-level conservation planning. Our flexible prioritization framework could help to inform both national marine spatial plans4 and global targets for marine conservation, food security and climate action.

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.

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.

Climate change reduces long-term population benefits from no-take marine protected areas through selective pressures on species movement.

Marine protected areas (MPAs) are important conservation tools that confer ecosystem benefits by removing fishing within their borders to allow stocks to rebuild. Fishing mortality outside a traditionally fixed MPA can exert selective pressure for low movement alleles, resulting in enhanced protection. While evolving to move less may be useful for conservation presently, it could be detrimental in the face of climate change for species that need to move to track their thermal optimum. Here, we build a spatially explicit simulation model to assess the impact of movement evolution in and around static MPAs resulting from both fishing mortality and temperature-dependent natural mortality on conservation benefits across five climate scenarios: (i) linear mean temperature shift, (ii) El Niño/La Niña conditions, (iii) heat waves, (iv) heatwaves with a mean temperature shift, and (v) no climate change. While movement evolution allows populations within MPAs to survive longer, we find that over time, climate change degrades the benefits by selecting for higher movement genotypes. Resulting population declines within MPAs are faster than expected based on climate mortality alone, even within the largest MPAs. Our findings suggest that while static MPAs may conserve species for a time, other strategies, such as dynamic MPA networks or assisted migration, may also be required to effectively incorporate climate change into conservation planning.

A global network of marine protected areas for food.

Marine protected areas (MPAs) are conservation tools that are increasingly implemented, with growing national commitments for MPA expansion. Perhaps the greatest challenge to expanded use of MPAs is the perceived trade-off between protection and food production. Since MPAs can benefit both conservation and fisheries in areas experiencing overfishing and since overfishing is common in many coastal nations, we ask how MPAs can be designed specifically to improve fisheries yields. We assembled distribution, life history, and fisheries exploitation data for 1,338 commercially important stocks to derive an optimized network of MPAs globally. We show that strategically expanding the existing global MPA network to protect an additional 5% of the ocean could increase future catch by at least 20% via spillover, generating 9 to 12 million metric tons more food annually than in a business-as-usual world with no additional protection. Our results demonstrate how food provisioning can be a central driver of MPA design, offering a pathway to strategically conserve ocean areas while securing seafood for the future.

Multiyear social stability and social information use in reef sharks with diel fission-fusion dynamics.

Animals across vertebrate taxa form social communities and often exist as fission-fusion groups. Central place foragers (CPF) may form groups from which they will predictably disperse to forage, either individually or in smaller groups, before returning to fuse with the larger group. However, the function and stability of social associations in predatory fish acting as CPFs is unknown, as individuals do not need to return to a shelter yet show fidelity to core areas. Using dynamic social networks generated from acoustic tracking data, we document spatially structured sociality in CPF grey reef sharks at a Pacific Ocean atoll. We show that sharks form stable social groups over multiyear periods, with some dyadic associations consistent for up to 4 years. Groups primarily formed during the day, increasing in size throughout the morning before sharks dispersed from the reef at night. Our simulations suggest that multiple individuals sharing a central place and using social information while foraging (i.e. local enhancement) will outperform non-CPF social foragers. We show multiyear social stability in sharks and suggest that social foraging with information transfer could provide a generalizable mechanism for the emergence of sociality with group central place foraging.

Habitat-specific inter and intraspecific behavioral interactions among reef sharks.

Behavioral interactions such as dominance are critical components of animal social lives, competitive abilities, and resulting distribution patterns with coexisting species. Strong interference competition can drive habitat separation, but less is known of the role of interference if agonistic interactions are weak. While most theoretical models assume interference abilities to be constant in an environment, few consider that the extent of interference can vary by habitat and change model predictions. Using baited underwater cameras, we show a consistent dominance status between two sympatric reef sharks at an uninhabited Pacific atoll. Blacktip reef shark (Carcharhinus melanopterus) and gray reef shark (Carcharhinus amblyrhyncos) relative abundance showed an inverse relationship to each other but the strength of this relationship varied by habitat. Reef shark relative abundance declined more rapidly in the presence of heterospecifics on forereef habitats as opposed to backreefs. In all habitats, gray reef sharks were more likely to bite bait cages than blacktips when both species were present, and appeared to be the dominant species. Intraspecific interactions were also apparent, with individual willingness to bite bait decreasing as the number of conspecifics increased. Gray reef sharks may exert differential control over blacktip foraging success in different habitats. Habitat-specific behavioral interactions may partially explain patterns of spatial separation between competing species where interference is weak.

Mobile marine predators: an understudied source of nutrients to coral reefs in an unfished atoll.

Animal movements can facilitate important ecological processes, and wide-ranging marine predators, such as sharks, potentially contribute significantly towards nutrient transfer between habitats. We applied network theory to 4 years of acoustic telemetry data for grey reef sharks (Carcharhinus amblyrhynchos) at Palmyra, an unfished atoll, to assess their potential role in nutrient dynamics throughout this remote ecosystem. We evaluated the dynamics of habitat connectivity and used network metrics to quantify shark-mediated nutrient distribution. Predator movements were consistent within year, but differed between years and by sex. Females used higher numbers of routes throughout the system, distributing nutrients over a larger proportion of the atoll. Extrapolations of tagged sharks to the population level suggest that prey consumption and subsequent egestion leads to the heterogeneous deposition of 94.5 kg d-1 of nitrogen around the atoll, with approximately 86% of this probably derived from pelagic resources. These results suggest that sharks may contribute substantially to nutrient transfer from offshore waters to near-shore reefs, subsidies that are important for coral reef health.

Functional diversity of catch mitigates negative effects of temperature variability on fisheries yields.

Temperature variation within a year can impact biological processes driving population abundances. The implications for the ecosystem services these populations provide, including food production from marine fisheries, are poorly understood. Whether and how temperature variability impacts fishery yields may depend on the number of harvested species and differences in their responses to varying temperatures. Drawing from previous theoretical and empirical studies, we predict that greater temperature variability within years will reduce yields, but harvesting a larger number of species, especially a more functionally diverse set, will decrease this impact. Using a global marine fisheries dataset, we find that within-year temperature variability reduces yields, but current levels of functional diversity (FD) of targeted species, measured using traits related to species' responses to temperature, largely offset this effect. Globally, high FD of catch could avoid annual losses in yield of 6.8% relative to projections if FD were degraded to the lowest level observed in the data. By contrast, species richness in the catch and in the ecosystem did not provide a similar mitigating effect. This work provides novel empirical evidence that short-term temperature variability can negatively impact the provisioning of ecosystem services, but that FD can buffer these negative impacts.

Age is not just a number: How incorrect ageing impacts close-kin mark-recapture estimates of population size.

Population size is a key parameter for the conservation of animal species. Close-kin mark-recapture (CKMR) relies on the observed frequency and type of kinship among individuals sampled from the population to estimate population size. Knowledge of the age of the individuals, or a surrogate thereof, is essential for inference with acceptable precision. One common approach, particularly in fish studies, is to measure animal length and infer age using an assumed age-length relationship (a 'growth curve'). We used simulation to test the effect of misspecifying the length measurement error and the growth curve on population size estimation. Simulated populations represented two fictional shark species, one with a relatively simple life history and the other with a more complex life history based on the grey reef shark (Carcharhinus amblyrhynchos). We estimated sex-specific adult abundance, which we assumed to be constant in time. We observed small median biases in these estimates ranging from 1.35% to 2.79% when specifying the correct measurement error standard deviation and growth curve. CI coverage was adequate whenever the growth curve was correctly specified. Introducing error via misspecified growth curves resulted in changes in the magnitude of the estimated adult population, where underestimating age negatively biased the abundance estimates. Over- and underestimating the standard deviation of length measurement error did not introduce a bias and had negligible effect on the variance in the estimates. Our findings show that assuming an incorrect standard deviation of length measurement error has little effect on estimation, but having an accurate growth curve is crucial for CKMR whenever ageing is based on length measurements. If ageing could be biased, researchers should be cautious when interpreting CKMR results and consider the potential biases arising from inaccurate age inference.

Could fish aggregation at ocean aquaculture augment wild populations and local fisheries?

The global population consumes more seafood from aquaculture today than from capture fisheries and although the aquaculture industry continues to grow, both seafood sectors will continue to be important to the global food supply into the future. As farming continues to expand into ocean systems, understanding how wild populations and fisheries will interact with farms will be increasingly important to informing sustainable ocean planning and management. Using a spatially explicit population and fishing model we simulate several impacts from ocean aquaculture (i.e., aggregation, protection from fishing, and impacts on fitness) to evaluate the mechanisms underlying interactions between aquaculture, wild populations and fisheries. We find that aggregation of species to farms can increase the benefits of protection from fishing that a farm provides and can have greater impacts on more mobile species. Splitting total farm area into smaller farms can benefit fishery catches, whereas larger farms can provide greater ecological benefits through conservation of wild populations. Our results provide clear lessons on how to design and co-manage expanding ocean aquaculture along with wild capture ecosystem management to benefit fisheries or conservation objectives.

Global shark fishing mortality still rising despite widespread regulatory change.

Over the past two decades, sharks have been increasingly recognized among the world's most threatened wildlife and hence have received heightened scientific and regulatory scrutiny. Yet, the effect of protective regulations on shark fishing mortality has not been evaluated at a global scale. Here we estimate that total fishing mortality increased from at least 76 to 80 million sharks between 2012 and 2019, ~25 million of which were threatened species. Mortality increased by 4% in coastal waters but decreased by 7% in pelagic fisheries, especially across the Atlantic and Western Pacific. By linking fishing mortality data to the global regulatory landscape, we show that widespread legislation designed to prevent shark finning did not reduce mortality but that regional shark fishing or retention bans had some success. These analyses, combined with expert interviews, highlight evidence-based solutions to reverse the continued overexploitation of sharks.

Conservation implications of forage base requirements of a marine predator population at carrying capacity.

Prey depletion may contribute to marine predator declines, yet the forage base required to sustain an unfished population of predatory fish at carrying capacity is unknown. We integrated demographic and physiological data within a Bayesian bioenergetic model to estimate annual consumption of a gray reef shark (Carcharhinus amblyrhynchos) population at a remote Pacific atoll (Palmyra Atoll) that are at carrying capacity. Furthermore, we estimated the proportion of the atoll's reef fish biomass production consumed by the gray reef sharks, assuming sharks either partially foraged pelagically (mean 7%), or solely within the reef environment (mean 52%). We then predicted the gray reef shark population potential of other, less remote Pacific Ocean coral reef islands, illustrating that current populations are substantially smaller than could be supported by their forage base. Our research highlights the utility of modeling how far predator population sizes are from their expected carrying capacity in informing marine conservation.