Inferring the extinction risk of marine fish to inform global conservation priorities.

While extinction risk categorization is fundamental for building robust conservation planning for marine fishes, empirical data on occurrence and vulnerability to disturbances are still lacking for most marine teleost fish species, preventing the assessment of their International Union for the Conservation of Nature (IUCN) status. In this article, we predicted the IUCN status of marine fishes based on two machine learning algorithms, trained with available species occurrences, biological traits, taxonomy, and human uses. We found that extinction risk for marine fish species is higher than initially estimated by the IUCN, increasing from 2.5% to 12.7%. Species predicted as Threatened were mainly characterized by a small geographic range, a relatively large body size, and a low growth rate. Hotspots of predicted Threatened species peaked mainly in the South China Sea, the Philippine Sea, the Celebes Sea, the west coast Australia and North America. We also explored the consequences of including these predicted species' IUCN status in the prioritization of marine protected areas through conservation planning. We found a marked increase in prioritization ranks for subpolar and polar regions despite their low species richness. We suggest to integrate multifactorial ensemble learning to assess species extinction risk and offer a more complete view of endangered taxonomic groups to ultimately reach global conservation targets like the extending coverage of protected areas where species are the most vulnerable.

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.

Protection efforts have resulted in ~10% of existing fish biomass on coral reefs.

The amount of ocean protected from fishing and other human impacts has often been used as a metric of conservation progress. However, protection efforts have highly variable outcomes that depend on local conditions, which makes it difficult to quantify what coral reef protection efforts to date have actually achieved at a global scale. Here, we develop a predictive model of how local conditions influence conservation outcomes on ~2,600 coral reef sites across 44 ecoregions, which we used to quantify how much more fish biomass there is on coral reefs compared to a modeled scenario with no protection. Under the assumptions of our model, our study reveals that without existing protection efforts there would be ~10% less fish biomass on coral reefs. Thus, we estimate that coral reef protection efforts have led to approximately 1 in every 10 kg of existing fish biomass.

The aesthetic value of reef fishes is globally mismatched to their conservation priorities.

Reef fishes are closely connected to many human populations, yet their contributions to society are mostly considered through their economic and ecological values. Cultural and intrinsic values of reef fishes to the public can be critical drivers of conservation investment and success, but remain challenging to quantify. Aesthetic value represents one of the most immediate and direct means by which human societies engage with biodiversity, and can be evaluated from species to ecosystems. Here, we provide the aesthetic value of 2,417 ray-finned reef fish species by combining intensive evaluation of photographs of fishes by humans with predicted values from machine learning. We identified important biases in species' aesthetic value relating to evolutionary history, ecological traits, and International Union for Conservation of Nature (IUCN) threat status. The most beautiful fishes are tightly packed into small parts of both the phylogenetic tree and the ecological trait space. In contrast, the less attractive fishes are the most ecologically and evolutionary distinct species and those recognized as threatened. Our study highlights likely important mismatches between potential public support for conservation and the species most in need of this support. It also provides a pathway for scaling-up our understanding of what are both an important nonmaterial facet of biodiversity and a key component of nature's contribution to people, which could help better anticipate consequences of species loss and assist in developing appropriate communication strategies.

Rarity mediates species-specific responses of tropical reef fishes to protection.

Marine protected areas (MPAs) are the most widely applied tool for marine biodiversity conservation, yet many gaps remain in our understanding of their species-specific effects, partly because the socio-environmental context and spatial autocorrelation may blur and bias perceived conservation outcomes. Based on a large data set of nearly 3000 marine fish surveys spanning all tropical regions of the world, we build spatially explicit models for 658 fish species to estimate species-specific responses to protection while controlling for the environmental, habitat and socio-economic contexts experienced across their geographic ranges. We show that the species responses are highly variable, with ~40% of fishes not benefitting from protection. When investigating how traits influence species' responses, we find that rare top-predators and small herbivores benefit the most from MPAs while mid-trophic level species benefit to a lesser extent, and rare large herbivores experience adverse effects, indicating potential trophic cascades.

The Tree of Life eDNA metabarcoding reveals a similar taxonomic richness but dissimilar evolutionary lineages between seaports and marine reserves.

Coastal areas host a major part of marine biodiversity but are seriously threatened by ever-increasing human pressures. Transforming natural coastlines into urban seascapes through habitat artificialization may result in loss of biodiversity and key ecosystem functions. Yet, the extent to which seaports differ from nearby natural habitats and marine reserves across the whole Tree of Life is still unknown. This study aimed to assess the level of α and ß-diversity between seaports and reserves, and whether these biodiversity patterns are conserved across taxa and evolutionary lineages. For that, we used environmental DNA (eDNA) metabarcoding to survey six seaports on the French Mediterranean coast and four strictly no-take marine reserves nearby. By targeting four different groups-prokaryotes, eukaryotes, metazoans and fish-with appropriate markers, we provide a holistic view of biodiversity on contrasted habitats. In the absence of comprehensive reference databases, we used bioinformatic pipelines to gather similar sequences into molecular operational taxonomic units (MOTUs). In contrast to our expectations, we obtained no difference in MOTU richness (α-diversity) between habitats except for prokaryotes and threatened fishes with higher diversity in reserves than in seaports. However, we observed a marked dissimilarity (ß-diversity) between seaports and reserves for all taxa. Surprisingly, this biodiversity signature of seaports was preserved across the Tree of Life, up to the order. This result reveals that seaports and nearby marine reserves share few taxa and evolutionary lineages along urbanized coasts and suggests major differences in terms of ecosystem functioning between both habitats.

Maximizing regional biodiversity requires a mosaic of protection levels.

Protected areas are the flagship management tools to secure biodiversity from anthropogenic impacts. However, the extent to which adjacent areas with distinct protection levels host different species numbers and compositions remains uncertain. Here, using reef fishes, European alpine plants, and North American birds, we show that the composition of species in adjacent Strictly Protected, Restricted, and Non-Protected areas is highly dissimilar, whereas the number of species is similar, after controlling for environmental conditions, sample size, and rarity. We find that between 12% and 15% of species are only recorded in Non-Protected areas, suggesting that a non-negligible part of regional biodiversity occurs where human activities are less regulated. For imperiled species, the proportion only recorded in Strictly Protected areas reaches 58% for fishes, 11% for birds, and 7% for plants, highlighting the fundamental and unique role of protected areas and their environmental conditions in biodiversity conservation.

Three-dimensional conservation planning of fish biodiversity metrics to achieve the deep-sea 30×30 conservation target.

Accelerating rate of human impact and environmental change severely affects marine biodiversity and increases the urgency to implement the Convention on Biological Diversity (CBD) 30×30 plan for conserving 30% of sea areas by 2030. However, area-based conservation targets are complex to identify in a 3-dimensional (3D) ocean where deep-sea features such as seamounts have been seldom studied mostly due to challenging methodologies to implement at great depths. Yet, the use of emerging technologies, such as environmental DNA combined with modern modeling frameworks, could help address the problem. We collected environmental DNA, echosounder acoustic, and video data at 15 seamounts and deep island slopes across the Coral Sea. We modeled 7 fish community metrics and the abundances of 45 individual species and molecular operational taxonomic units (MOTUs) in benthic and pelagic waters (down to 600-m deep) with boosted regression trees and generalized joint attribute models to describe biodiversity on seamounts and deep slopes and identify 3D protection solutions for achieving the CBD area target in New Caledonia (1.4 million km2). We prioritized the identified conservation units in a 3D space, based on various biodiversity targets, to meet the goal of protecting at least 30% of the spatial domain, with a focus on areas with high biodiversity. The relationship between biodiversity protection targets and the spatial area protected by the solution was linear. The scenario protecting 30% of each biodiversity metric preserved almost 30% of the considered spatial domain and accounted for the 3D distribution of biodiversity. Our study paves the way for the use of combined data collection methodologies to improve biodiversity estimates in 3D structured marine environments for the selection of conservation areas and for the use of biodiversity targets to achieve area-based international targets.

Planeación tridimensional de la conservación de las medidas de biodiversidad de peces para lograr el objetivo de conservación 30x30 de mar profundo Resumen El impacto antropogénico y el cambio ambiental acelerados afectan gravemente a la biodiversidad marina y aumentan la urgencia de aplicar el plan 30x30 del Convenio sobre la Diversidad Biológica (CDB) para conservar el 30% de las zonas marinas para el 2030. Sin embargo, la identificación de objetivos de conservación basados en zonas es compleja en un océano tridimensional (3D) en el que rara vez se han estudiado las características de las profundidades marinas, como los montes marinos, sobre todo por la dificultad de aplicar metodologías a grandes profundidades. No obstante, el uso de tecnologías emergentes, como el ADN ambiental combinado con marcos actuales de modelación, podría ayudar a resolver el problema. Recopilamos datos de ADN ambiental, acústica de ecosonda y video en 15 montes marinos y taludes de islas profundas del mar del Coral. Modelamos siete medidas de comunidades de peces y 45 abundancias de especies individuales y unidades taxonómicas moleculares (UTOM) en aguas bentónicas y pelágicas (hasta 600 m de profundidad) con árboles de regresión reforzada (ARR) y modelos de atributos conjuntos generalizados (MACJ) para describir la biodiversidad en los montes marinos y taludes profundos e identificar soluciones de protección en 3D para alcanzar el objetivo de área del CDB en Nueva Caledonia (1.4 millones de km2). Priorizamos las unidades de conservación identificadas en un espacio 3D con base en varios objetivos de biodiversidad para cumplir el objetivo de proteger al menos el 30% del dominio espacial con un enfoque en las zonas con una gran biodiversidad. La relación entre los objetivos de protección de la biodiversidad y el área espacial protegida por la solución fue lineal. El escenario que protegía el 30% de cada medida de biodiversidad preservó casi el 30% del dominio espacial considerado y consideró la distribución tridimensional de la biodiversidad. Nuestro estudio prepara el camino para el uso de metodologías combinadas de recopilación de datos con el fin de mejorar las estimaciones de biodiversidad en entornos marinos estructurados en 3D para la selección de áreas de conservación y para el uso de objetivos de biodiversidad con el fin de alcanzar objetivos internacionales basados en áreas.

Trait similarity in reef fish faunas across the world's oceans.

Species' traits, rather than taxonomic identities, determine community assembly and ecosystem functioning, yet biogeographic patterns have been far less studied for traits. While both environmental conditions and evolutionary history shape trait biogeography, their relative contributions are largely unknown for most organisms. Here, we explore the global biogeography of reef fish traits for 2,786 species from 89 ecoregions spanning eight marine realms with contrasting environmental conditions and evolutionary histories. Across realms, we found a common structure in the distribution of species traits despite a 10-fold gradient in species richness, with a defined "backbone" of 21 trait combinations shared by all realms globally, both temperate and tropical. Across ecoregions, assemblages under similar environmental conditions had similar trait compositions despite hosting drastically different species pools from separate evolutionary lineages. Thus, despite being separated by thousands of kilometers and millions of years of evolution, similar environments host similar trait compositions in reef fish assemblages worldwide. Our findings suggest that similar trait-based management strategies can be applied among regions with distinct species pools, potentially improving conservation outcomes across diverse jurisdictions.

The ecological causes of functional distinctiveness in communities.

Recent work has shown that evaluating functional trait distinctiveness, the average trait distance of a species to other species in a community offers promising insights into biodiversity dynamics and ecosystem functioning. However, the ecological mechanisms underlying the emergence and persistence of functionally distinct species are poorly understood. Here, we address the issue by considering a heterogeneous fitness landscape whereby functional dimensions encompass peaks representing trait combinations yielding positive population growth rates in a community. We identify four ecological cases contributing to the emergence and persistence of functionally distinct species. First, environmental heterogeneity or alternative phenotypic designs can drive positive population growth of functionally distinct species. Second, sink populations with negative population growth can deviate from local fitness peaks and be functionally distinct. Third, species found at the margin of the fitness landscape can persist but be functionally distinct. Fourth, biotic interactions (positive or negative) can dynamically alter the fitness landscape. We offer examples of these four cases and guidelines to distinguish between them. In addition to these deterministic processes, we explore how stochastic dispersal limitation can yield functional distinctiveness. Our framework offers a novel perspective on the relationship between fitness landscape heterogeneity and the functional composition of ecological assemblages.

Industrial fisheries have reversed the carbon sequestration by tuna carcasses into emissions.

To limit climate warming to 2°C above preindustrial levels, most economic sectors will need a rapid transformation toward a net zero emission of CO2 . Tuna fisheries is a key food production sector that burns fossil fuel to operate but also reduces the deadfall of large-bodied fish so the capacity of this natural carbon pump to deep sea. Yet, the carbon balance of tuna populations, so the net difference between CO2 emission due to industrial exploitation and CO2 sequestration by fish deadfall after natural mortality, is still unknown. Here, by considering the dynamics of two main contrasting tuna species (Katsuwonus pelamis and Thunnus obesus) across the Pacific since the 1980s, we show that most tuna populations became CO2 sources instead of remaining natural sinks. Without considering the supply chain, the main factors associated with this shift are exploitation rate, transshipment intensity, fuel consumption, and climate change. Our study urges for a better global ocean stewardship, by curbing subsidies and limiting transshipment in remote international waters, to quickly rebuild most pelagic fish stocks above their target management reference points and reactivate a neglected carbon pump toward the deep sea as an additional Nature Climate Solution in our portfolio. Even if this potential carbon sequestration by surface unit may appear low compared to that of coastal ecosystems or tropical forests, the ocean covers a vast area and the sinking biomass of dead vertebrates can sequester carbon for around 1000 years in the deep sea. We also highlight the multiple co-benefits and trade-offs from engaging the industrial fisheries sector with carbon neutrality.

A marine protected area network does not confer community structure resilience to a marine heatwave across coastal ecosystems.

Marine protected areas (MPAs) have gained attention as a conservation tool for enhancing ecosystem resilience to climate change. However, empirical evidence explicitly linking MPAs to enhanced ecological resilience is limited and mixed. To better understand whether MPAs can buffer climate impacts, we tested the resistance and recovery of marine communities to the 2014-2016 Northeast Pacific heatwave in the largest scientifically designed MPA network in the world off the coast of California, United States. The network consists of 124 MPAs (48 no-take state marine reserves, and 76 partial-take or special regulation conservation areas) implemented at different times, with full implementation completed in 2012. We compared fish, benthic invertebrate, and macroalgal community structure inside and outside of 13 no-take MPAs across rocky intertidal, kelp forest, shallow reef, and deep reef nearshore habitats in California's Central Coast region from 2007 to 2020. We also explored whether MPA features, including age, size, depth, proportion rock, historic fishing pressure, habitat diversity and richness, connectivity, and fish biomass response ratios (proxy for ecological performance), conferred climate resilience for kelp forest and rocky intertidal habitats spanning 28 MPAs across the full network. Ecological communities dramatically shifted due to the marine heatwave across all four nearshore habitats, and MPAs did not facilitate habitat-wide resistance or recovery. Only in protected rocky intertidal habitats did community structure significantly resist marine heatwave impacts. Community shifts were associated with a pronounced decline in the relative proportion of cold water species and an increase in warm water species. MPA features did not explain resistance or recovery to the marine heatwave. Collectively, our findings suggest that MPAs have limited ability to mitigate the impacts of marine heatwaves on community structure. Given that mechanisms of resilience to climate perturbations are complex, there is a clear need to expand assessments of ecosystem-wide consequences resulting from acute climate-driven perturbations, and the potential role of regulatory protection in mitigating community structure changes.

Plant community impact on productivity: Trait diversity or key(stone) species effects?

Outside controlled experimental plots, the impact of community attributes on primary productivity has rarely been compared to that of individual species. Here, we identified plant species of high importance for productivity (key species) in >29,000 diverse grassland communities in the European Alps, and compared their effects with those of community-level measures of functional composition (weighted means, variances, skewness and kurtosis). After accounting for the environment, the five most important key species jointly explained more deviance of productivity than any measure of functional composition alone. Key species were generally tall with high specific leaf areas. By dividing the observations according to distinct habitats, the explanatory power of key species and functional composition increased and key-species plant types and functional composition-productivity relationships varied systematically, presumably because of changing interactions and trade-offs between traits. Our results advocate for a careful consideration of species' individual effects on ecosystem functioning in complement to community-level measures.

Recovery of carbon benefits by overharvested baleen whale populations is threatened by climate change.

Despite the importance of marine megafauna on ecosystem functioning, their contribution to the oceanic carbon cycle is still poorly known. Here, we explored the role of baleen whales in the biological carbon pump across the southern hemisphere based on the historical and forecasted abundance of five baleen whale species. We modelled whale-mediated carbon sequestration through the sinking of their carcasses after natural death. We provide the first temporal dynamics of this carbon pump from 1890 to 2100, considering both the effects of exploitation and climate change on whale populations. We reveal that at their pre-exploitation abundance, the five species of southern whales could sequester 4.0 × 105 tonnes of carbon per year (tC yr-1). This estimate dropped to 0.6 × 105 tC yr-1 by 1972 following commercial whaling. However, with the projected restoration of whale populations under a RCP8.5 climate scenario, the sequestration would reach 1.7 × 105 tC yr-1 by 2100, while without climate change, recovered whale populations could sequester nearly twice as much (3.2 × 105 tC yr-1) by 2100. This highlights the persistence of whaling damages on whale populations and associated services as well as the predicted harmful impacts of climate change on whale ecosystem services.

Functionally distinct tree species support long-term productivity in extreme environments.

Despite evidence of a positive effect of functional diversity on ecosystem productivity, the importance of functionally distinct species (i.e. species that display an original combination of traits) is poorly understood. To investigate how distinct species affect ecosystem productivity, we used a forest-gap model to simulate realistic temperate forest successions along an environmental gradient and measured ecosystem productivity at the end of the successional trajectories. We performed 10 560 simulations with different sets and numbers of species, bearing either distinct or indistinct functional traits, and compared them to random assemblages, to mimic the consequences of a regional loss of species. Long-term ecosystem productivity dropped when distinct species were lost first from the regional pool of species, under the harshest environmental conditions. On the contrary, productivity was more dependent on ordinary species in milder environments. Our findings show that species functional distinctiveness, integrating multiple trait dimensions, can capture species-specific effects on ecosystem productivity. In a context of an environmentally changing world, they highlight the need to investigate the role of distinct species in sustaining ecosystem processes, particularly in extreme environmental conditions.

Cross-ocean patterns and processes in fish biodiversity on coral reefs through the lens of eDNA metabarcoding.

Increasing speed and magnitude of global change threaten the world's biodiversity and particularly coral reef fishes. A better understanding of large-scale patterns and processes on coral reefs is essential to prevent fish biodiversity decline but it requires new monitoring approaches. Here, we use environmental DNA metabarcoding to reconstruct well-known patterns of fish biodiversity on coral reefs and uncover hidden patterns on these highly diverse and threatened ecosystems. We analysed 226 environmental DNA (eDNA) seawater samples from 100 stations in five tropical regions (Caribbean, Central and Southwest Pacific, Coral Triangle and Western Indian Ocean) and compared those to 2047 underwater visual censuses from the Reef Life Survey in 1224 stations. Environmental DNA reveals a higher (16%) fish biodiversity, with 2650 taxa, and 25% more families than underwater visual surveys. By identifying more pelagic, reef-associated and crypto-benthic species, eDNA offers a fresh view on assembly rules across spatial scales. Nevertheless, the reef life survey identified more species than eDNA in 47 shared families, which can be due to incomplete sequence assignment, possibly combined with incomplete detection in the environment, for some species. Combining eDNA metabarcoding and extensive visual census offers novel insights on the spatial organization of the richest marine ecosystems.

Correction: Remote reefs and seamounts are the last refuges for marine predators across the Indo-Pacific.

[This corrects the article DOI: 10.1371/journal.pbio.3000366.].