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.

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.

Neutral processes and taxonomic scale drive beta species-genetic diversity correlations in a submesophotic tropical reef fish.

If similar evolutionary forces maintain intra- and interspecific diversity, patterns of diversity at both levels of biological organization can be expected to covary across space. Although this prediction of a positive species-genetic diversity correlation (SGDC) has been tested for several taxa in natural landscapes, no study has yet evaluated the influence of the community delineation on these SGDCs. In this study, we focused on tropical fishes of the Indo-Pacific Ocean, using range-wide single nucleotide polymorphism data for a deep-sea fish (Etelis coruscans) and species presence data of 4878 Teleostei species. We investigated whether a diversity continuum occurred, for different community delineations (subfamily, family, order and class) and spatial extents, and which processes explained these diversity patterns. We found no association between genetic diversity and species richness (α-SGDC), regardless of the community and spatial extent. In contrast, we evidenced a positive relationship between genetic and species dissimilarities (ß-SGDC) when the community was defined at the subfamily or family level of the species of interest, and when the Western Indian Ocean was excluded. This relationship was related to the imprint of dispersal processes across levels of biological organization in Lutjanidae. However, this positive ß-SGDC was lost when considering higher taxonomic communities and at the scale of the entire Indo-Pacific, suggesting different responses of populations and communities to evolutionary processes at these scales. This study provides evidence that the taxonomic scale at which communities are defined and the spatial extent are pivotal to better understand the processes shaping diversity across levels of biological organization.

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.

Species ecology explains the spatial components of genetic diversity in tropical reef fishes.

Generating genomic data for 19 tropical reef fish species of the Western Indian Ocean, we investigate how species ecology influences genetic diversity patterns from local to regional scales. We distinguish between the α, ß and γ components of genetic diversity, which we subsequently link to six ecological traits. We find that the α and γ components of genetic diversity are strongly correlated so that species with a high total regional genetic diversity display systematically high local diversity. The α and γ diversity components are negatively associated with species abundance recorded using underwater visual surveys and positively associated with body size. Pelagic larval duration is found to be negatively related to genetic ß diversity supporting its role as a dispersal trait in marine fishes. Deviation from the neutral theory of molecular evolution motivates further effort to understand the processes shaping genetic diversity and ultimately the diversification of the exceptional diversity of tropical reef fishes.

Ecological constraints coupled with deep-time habitat dynamics predict the latitudinal diversity gradient in reef fishes.

We develop a spatially explicit model of diversification based on palaeohabitat to explore the predictions of four major hypotheses potentially explaining the latitudinal diversity gradient (LDG), namely, the 'time-area', 'tropical niche conservatism', 'ecological limits' and 'evolutionary speed' hypotheses. We compare simulation outputs to observed diversity gradients in the global reef fish fauna. Our simulations show that these hypotheses are non-mutually exclusive and that their relative influence depends on the time scale considered. Simulations suggest that reef habitat dynamics produced the LDG during deep geological time, while ecological constraints shaped the modern LDG, with a strong influence of the reduction in the latitudinal extent of tropical reefs during the Neogene. Overall, this study illustrates how mechanistic models in ecology and evolution can provide a temporal and spatial understanding of the role of speciation, extinction and dispersal in generating biodiversity patterns.

On the risks of using dendrograms to measure functional diversity and multidimensional spaces to measure phylogenetic diversity: a comment on Sobral et al. (2016).

Sobral et al. (Ecology Letters, 19, 2016, 1091) reported that the loss of bird functional and phylogenetic diversity due to species extinctions was not compensated by exotic species introductions. Here, we demonstrate that the reported changes in biodiversity were underestimated because of methodological pitfalls.

Selective extinction drives taxonomic and functional alpha and beta diversities in island bird assemblages.

Taxonomic diversity considers all species being equally different from each other and thus disregards species' different ecological functions. Exploring taxonomic and functional aspects of biodiversity simultaneously can better understand the processes of community assembly. We analysed taxonomic and functional alpha and beta diversities of breeding bird assemblages on land-bridge islands in the Thousand Island Lake, China. Given the high dispersal ability of most birds at this spatial scale (several kilometres), we predicted (i) selective extinction driving alpha and beta diversities after the creation of land-bridge islands of varying area and (ii) low taxonomic and functional beta diversities that were not correlated to spatial distance. Breeding birds were surveyed on 37 islands annually from 2007 to 2014. We decomposed beta diversity of breeding birds into spatial turnover and nestedness-resultant components, and related taxonomic and functional diversities to island area and isolation using power regression models (for alpha diversity) and multiple regression models on distance matrices (for beta diversity). We then ran simulations to assess the strength of the correlations between taxonomic and functional diversities. Results revealed that both taxonomic and functional alpha diversities increased with island area. The taxonomic nestedness-resultant and turnover components increased and decreased with difference in area, respectively, but functional counterparts did not. Isolation played a minor role in explaining alpha- and beta-diversity patterns. By partitioning beta diversity, we found low levels of overall taxonomic and functional beta diversities. The functional nestedness-resultant component dominated overall functional beta diversity, whereas taxonomic turnover was the dominant component for taxonomic beta diversity. The simulation showed that functional alpha and beta diversities were significantly correlated with taxonomic diversities, and the observed values of correlations were significantly different from null expectations of random extinction. Our assessment of island bird assemblages validated the predictions of no distance effects and low beta diversity due to pervasive dispersal events among islands and also suggested that selective extinction drives taxonomic and functional alpha and beta diversities. The contrasting turnover and nestedness-resultant components of taxonomic and functional beta diversities demonstrate the importance of considering the multifaceted nature of biodiversity when examining community assembly.

Forecasted coral reef decline in marine biodiversity hotspots under climate change.

Coral bleaching events threaten coral reef habitats globally and cause severe declines of local biodiversity and productivity. Related to high sea surface temperatures (SST), bleaching events are expected to increase as a consequence of future global warming. However, response to climate change is still uncertain as future low-latitude climatic conditions have no present-day analogue. Sea surface temperatures during the Eocene epoch were warmer than forecasted changes for the coming century, and distributions of corals during the Eocene may help to inform models forecasting the future of coral reefs. We coupled contemporary and Eocene coral occurrences with information on their respective climatic conditions to model the thermal niche of coral reefs and its potential response to projected climate change. We found that under the RCP8.5 climate change scenario, the global suitability for coral reefs may increase up to 16% by 2100, mostly due to improved suitability of higher latitudes. In contrast, in its current range, coral reef suitability may decrease up to 46% by 2100. Reduction in thermal suitability will be most severe in biodiversity hotspots, especially in the Indo-Australian Archipelago. Our results suggest that many contemporary hotspots for coral reefs, including those that have been refugia in the past, spatially mismatch with future suitable areas for coral reefs posing challenges to conservation actions under climate change.

Global imprint of historical connectivity on freshwater fish biodiversity.

The relative importance of contemporary and historical processes is central for understanding biodiversity patterns. While several studies show that past conditions can partly explain the current biodiversity patterns, the role of history remains elusive. We reconstructed palaeo-drainage basins under lower sea level conditions (Last Glacial Maximum) to test whether the historical connectivity between basins left an imprint on the global patterns of freshwater fish biodiversity. After controlling for contemporary and past environmental conditions, we found that palaeo-connected basins displayed greater species richness but lower levels of endemism and beta diversity than did palaeo-disconnected basins. Palaeo-connected basins exhibited shallower distance decay of compositional similarity, suggesting that palaeo-river connections favoured the exchange of fish species. Finally, we found that a longer period of palaeo-connection resulted in lower levels of beta diversity. These findings reveal the first unambiguous results of the role played by history in explaining the global contemporary patterns of biodiversity.

A unifying quantitative framework for exploring the multiple facets of microbial biodiversity across diverse scales.

Recent developments of molecular tools have revolutionized our knowledge of microbial biodiversity by allowing detailed exploration of its different facets and generating unprecedented amount of data. One key issue with such large datasets is the development of diversity measures that cope with different data outputs and allow comparison of biodiversity across different scales. Diversity has indeed three components: local (α), regional (γ) and the overall difference between local communities (ß). Current measures of microbial diversity, derived from several approaches, provide complementary but different views. They only capture the ß component of diversity, compare communities in a pairwise way, consider all species as equivalent or lack a mathematically explicit relationship among the α, ß and γ components. We propose a unified quantitative framework based on the Rao quadratic entropy, to obtain an additive decomposition of diversity (γ = α + ß), so the three components can be compared, and that integrate the relationship (phylogenetic or functional) among Microbial Diversity Units that compose a microbial community. We show how this framework is adapted to all types of molecular data, and we highlight crucial issues in microbial ecology that would benefit from this framework and propose ready-to-use R-functions to easily set up our approach.

Functional diversity of sharks and rays is highly vulnerable and supported by unique species and locations worldwide.

Elasmobranchs (sharks, rays and skates) are among the most threatened marine vertebrates, yet their global functional diversity remains largely unknown. Here, we use a trait dataset of >1000 species to assess elasmobranch functional diversity and compare it against other previously studied biodiversity facets (taxonomic and phylogenetic), to identify species- and spatial- conservation priorities. We show that threatened species encompass the full extent of functional space and disproportionately include functionally distinct species. Applying the conservation metric FUSE (Functionally Unique, Specialised, and Endangered) reveals that most top-ranking species differ from the top Evolutionarily Distinct and Globally Endangered (EDGE) list. Spatial analyses further show that elasmobranch functional richness is concentrated along continental shelves and around oceanic islands, with 18 distinguishable hotspots. These hotspots only marginally overlap with those of other biodiversity facets, reflecting a distinct spatial fingerprint of functional diversity. Elasmobranch biodiversity facets converge with fishing pressure along the coast of China, which emerges as a critical frontier in conservation. Meanwhile, several components of elasmobranch functional diversity fall in high seas and/or outside the global network of marine protected areas. Overall, our results highlight acute vulnerability of the world's elasmobranchs' functional diversity and reveal global priorities for elasmobranch functional biodiversity previously overlooked.

Major shifts in biogeographic regions of freshwater fishes as evidence of the Anthropocene epoch.

Animals and plants worldwide are structured in global biogeographic regions, which were shaped by major geologic forces during Earth history. Recently, humans have changed the course of events by multiplying global pathways of introduction for nonindigenous species and propagating local species extirpations. Here, we report on how introductions and extirpations have changed the distributions of freshwater fishes worldwide and how it affected their natural biogeographic regions. We found major shifts in natural regions, with the emergence of an intercontinental region arising from the fusion of multiple faunas, which we named Pan-Anthropocenian Global North and East Asia (PAGNEA). The PAGNEA region is evocative of the Pangea supercontinent, as flows of introductions show that dispersal has become possible again across multiple continents, suggesting that human activities have superseded natural geological forces. Our results constitute evidence on the expected modification of biostratigraphic boundaries based on freshwater fish, which are abundant in the fossil record, thereby supporting the concept of the Anthropocene epoch.

Combining projected changes in species richness and composition reveals climate change impacts on coastal Mediterranean fish assemblages.

Species Temporal Turnover (STT) is one of the most familiar metrics to assess changes in assemblage composition as a consequence of climate change. However, STT mixes two components in one metric, changes in assemblage composition caused by a process of species loss or gain (i.e. the nestedness component) and changes in assemblage composition caused by a process of species replacement (i.e. the species replacement component). Drawing on previous studies investigating spatial patterns of beta diversity, we propose measures of STT that allow analysing each component (species replacement vs. nestedness), separately. We also present a mapping strategy to simultaneously visualize changes in species richness and assemblage composition. To illustrate our approach, we used the Mediterranean coastal fish fauna as a case study. Using Bioclimatic Envelope Models (BEMs) we first projected the potential future climatic niches of 288 coastal Mediterranean fish species based on a global warming scenario. We then aggregated geographically the species-level projections to analyse the projected changes in species richness and composition. Our results show that projected changes in assemblage composition are caused by different processes (species replacement vs. nestedness) in several areas of the Mediterranean Sea. In addition, our mapping strategy highlights that the coastal fish fauna in several regions of the Mediterranean Sea could experience a 'cul-de-sac' effect if exposed to climate warming. Overall, the joint exploration of changes in species richness and composition coupled with the distinction between species replacement and nestedness bears important information for understanding the nature of climate change impacts on biodiversity. These methodological advances should help decision-makers in prioritizing action in the areas facing the greatest vulnerability to climate.

Influence of phylogenetic scale on the relationships of taxonomic and phylogenetic turnovers with environment for angiosperms in China.

We aim to assess the influence of phylogenetic scale on the relationships of taxonomic and phylogenetic turnovers with environment for angiosperms in China. Specifically, we quantify the effects of contemporary climate on ß-diversity at different phylogenetic scales representing different evolutionary depths of angiosperms. We sampled a latitudinal gradient and a longitudinal gradient of angiosperm assemblages across China (each ≥3400 km). Species composition in each assemblage was documented. Three metrics of ß-diversity (ßsim.tax measuring taxonomic ß-diversity; ßsim.phy and Dpw measuring tip- and basal-weighted phylogenetic ß-diversity, respectively) were quantified among assemblages at sequential depths in the evolutionary history of angiosperms from the tips to deeper branches. This was done by slicing the angiosperm phylogenetic tree at six evolutionary depths (0, 15, 30, 45, 60, and 75 million years ago). ß-diversity at each evolutionary depth was related to geographic and climatic distances between assemblages. In general, the relationship between ß-diversity and climatic distance decreased from shallow to deep evolutionary time slice for all the three metrics. The slopes of the decreasing trends for ßsim.tax and ßsim.phy were much steeper for the latitudinal gradient than for the longitudinal gradient. The decreasing trend of the strength of the relationship was monotonic in all cases except for Dpw across the longitudinal gradient. Geographic distance between assemblages explained little variation in ß-diversity that was not explained by climatic distance. Our study shows that the strength of the relationship between ß-diversity and climatic distance decreases conspicuously from shallow to deep evolutionary depth for the latitudinal gradient, but this decreasing trend is less steep for the longitudinal gradient than for the latitudinal gradient, which likely reflects the influence of historical processes (e.g., the collision of the Indian plate with the Eurasian plate) on ß-diversity.

Partitioning global patterns of freshwater fish beta diversity reveals contrasting signatures of past climate changes.

Here, we employ an additive partitioning framework to disentangle the contribution of spatial turnover and nestedness to beta diversity patterns in the global freshwater fish fauna. We find that spatial turnover and nestedness differ geographically in their contribution to freshwater fish beta diversity, a pattern that results from contrasting influences of Quaternary climate changes. Differences in fish faunas characterized by nestedness are greater in drainage basins that experienced larger amplitudes of Quaternary climate oscillations. Conversely, higher levels of spatial turnover are found in historically unglaciated drainage basins with high topographic relief, these having experienced greater Quaternary climate stability. Such an historical climate signature is not clearly detected when considering the overall level of beta diversity. Quantifying the relative roles of historical and ecological factors in explaining present-day patterns of beta diversity hence requires considering the different processes generating these patterns and not solely the overall level of beta diversity.