Continent-wide declines in shallow reef life over a decade of ocean warming.

Human society is dependent on nature1,2, but whether our ecological foundations are at risk remains unknown in the absence of systematic monitoring of species' populations3. Knowledge of species fluctuations is particularly inadequate in the marine realm4. Here we assess the population trends of 1,057 common shallow reef species from multiple phyla at 1,636 sites around Australia over the past decade. Most populations decreased over this period, including many tropical fishes, temperate invertebrates (particularly echinoderms) and southwestern Australian macroalgae, whereas coral populations remained relatively stable. Population declines typically followed heatwave years, when local water temperatures were more than 0.5 °C above temperatures in 2008. Following heatwaves5,6, species abundances generally tended to decline near warm range edges, and increase near cool range edges. More than 30% of shallow invertebrate species in cool latitudes exhibited high extinction risk, with rapidly declining populations trapped by deep ocean barriers, preventing poleward retreat as temperatures rise. Greater conservation effort is needed to safeguard temperate marine ecosystems, which are disproportionately threatened and include species with deep evolutionary roots. Fundamental among such efforts, and broader societal needs to efficiently adapt to interacting anthropogenic and natural pressures, is greatly expanded monitoring of species' population trends7,8.

A diverse portfolio of marine protected areas can better advance global conservation and equity.

Marine protected areas (MPAs) are widely used for ocean conservation, yet the relative impacts of various types of MPAs are poorly understood. We estimated impacts on fish biomass from no-take and multiple-use (fished) MPAs, employing a rigorous matched counterfactual design with a global dataset of >14,000 surveys in and around 216 MPAs. Both no-take and multiple-use MPAs generated positive conservation outcomes relative to no protection (58.2% and 12.6% fish biomass increases, respectively), with smaller estimated differences between the two MPA types when controlling for additional confounding factors (8.3% increase). Relative performance depended on context and management: no-take MPAs performed better in areas of high human pressure but similar to multiple-use in remote locations. Multiple-use MPA performance was low in high-pressure areas but improved significantly with better management, producing similar outcomes to no-take MPAs when adequately staffed and appropriate use regulations were applied. For priority conservation areas where no-take restrictions are not possible or ethical, our findings show that a portfolio of well-designed and well-managed multiple-use MPAs represents a viable and potentially equitable pathway to advance local and global conservation.

Changes in sea floor productivity are crucial to understanding the impact of climate change in temperate coastal ecosystems according to a new size-based model.

The multifaceted effects of climate change on physical and biogeochemical processes are rapidly altering marine ecosystems but often are considered in isolation, leaving our understanding of interactions between these drivers of ecosystem change relatively poor. This is particularly true for shallow coastal ecosystems, which are fuelled by a combination of distinct pelagic and benthic energy pathways that may respond to climate change in fundamentally distinct ways. The fish production supported by these systems is likely to be impacted by climate change differently to those of offshore and shelf ecosystems, which have relatively simpler food webs and mostly lack benthic primary production sources. We developed a novel, multispecies size spectrum model for shallow coastal reefs, specifically designed to simulate potential interactive outcomes of changing benthic and pelagic energy inputs and temperatures and calculate the relative importance of these variables for the fish community. Our model, calibrated using field data from an extensive temperate reef monitoring program, predicts that changes in resource levels will have much stronger impacts on fish biomass and yields than changes driven by physiological responses to temperature. Under increased plankton abundance, species in all fish trophic groups were predicted to increase in biomass, average size, and yields. By contrast, changes in benthic resources produced variable responses across fish trophic groups. Increased benthic resources led to increasing benthivorous and piscivorous fish biomasses, yields, and mean body sizes, but biomass decreases among herbivore and planktivore species. When resource changes were combined with warming seas, physiological responses generally decreased species' biomass and yields. Our results suggest that understanding changes in benthic production and its implications for coastal fisheries should be a priority research area. Our modified size spectrum model provides a framework for further study of benthic and pelagic energy pathways that can be easily adapted to other ecosystems.

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.

Mean reef fish body size decreases towards warmer waters.

Aquatic ectotherms often attain smaller body sizes at higher temperatures. By analysing ~15,000 coastal-reef fish surveys across a 15°C spatial sea surface temperature (SST) gradient, we found that the mean length of fish in communities decreased by ~5% for each 1°C temperature increase across space, or 50% decrease in mean length from 14 to 29°C mean annual SST. Community mean body size change was driven by differential temperature responses within trophic groups and temperature-driven change in their relative abundance. Herbivores, invertivores and planktivores became smaller on average in warmer temperatures, but no trend was found in piscivores. Nearly 25% of the temperature-related community mean size trend was attributable to trophic composition at the warmest sites, but at colder temperatures, this was <1% due to trophic groups being similarly sized. Our findings suggest that small changes in temperature are associated with large changes in fish community composition and body sizes, with important ecological implications.

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.

Ecosystem restructuring along the Great Barrier Reef following mass coral bleaching.

Global warming is markedly changing diverse coral reef ecosystems through an increasing frequency and magnitude of mass bleaching events1-3. How local impacts scale up across affected regions depends on numerous factors, including patchiness in coral mortality, metabolic effects of extreme temperatures on populations of reef-dwelling species4 and interactions between taxa. Here we use data from before and after the 2016 mass bleaching event to evaluate ecological changes in corals, algae, fishes and mobile invertebrates at 186 sites along the full latitudinal span of the Great Barrier Reef and western Coral Sea. One year after the bleaching event, reductions in live coral cover of up to 51% were observed on surveyed reefs that experienced extreme temperatures; however, regional patterns of coral mortality were patchy. Consistent declines in coral-feeding fishes were evident at the most heavily affected reefs, whereas few other short-term responses of reef fishes and invertebrates could be attributed directly to changes in coral cover. Nevertheless, substantial region-wide ecological changes occurred that were mostly independent of coral loss, and instead appeared to be linked directly to sea temperatures. Community-wide trophic restructuring was evident, with weakening of strong pre-existing latitudinal gradients in the diversity of fishes, invertebrates and their functional groups. In particular, fishes that scrape algae from reef surfaces, which are considered to be important for recovery after bleaching2, declined on northern reefs, whereas other herbivorous groups increased on southern reefs. The full impact of the 2016 bleaching event may not be realized until dead corals erode during the next decade5,6. However, our short-term observations suggest that the recovery processes, and the ultimate scale of impact, are affected by functional changes in communities, which in turn depend on the thermal affinities of local reef-associated fauna. Such changes will vary geographically, and may be particularly acute at locations where many fishes and invertebrates are close to their thermal distribution limits7.

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.

Delineating reef fish trophic guilds with global gut content data synthesis and phylogeny.

Understanding species' roles in food webs requires an accurate assessment of their trophic niche. However, it is challenging to delineate potential trophic interactions across an ecosystem, and a paucity of empirical information often leads to inconsistent definitions of trophic guilds based on expert opinion, especially when applied to hyperdiverse ecosystems. Using coral reef fishes as a model group, we show that experts disagree on the assignment of broad trophic guilds for more than 20% of species, which hampers comparability across studies. Here, we propose a quantitative, unbiased, and reproducible approach to define trophic guilds and apply recent advances in machine learning to predict probabilities of pairwise trophic interactions with high accuracy. We synthesize data from community-wide gut content analyses of tropical coral reef fishes worldwide, resulting in diet information from 13,961 individuals belonging to 615 reef fish. We then use network analysis to identify 8 trophic guilds and Bayesian phylogenetic modeling to show that trophic guilds can be predicted based on phylogeny and maximum body size. Finally, we use machine learning to test whether pairwise trophic interactions can be predicted with accuracy. Our models achieved a misclassification error of less than 5%, indicating that our approach results in a quantitative and reproducible trophic categorization scheme, as well as high-resolution probabilities of trophic interactions. By applying our framework to the most diverse vertebrate consumer group, we show that it can be applied to other organismal groups to advance reproducibility in trait-based ecology. Our work thus provides a viable approach to account for the complexity of predator-prey interactions in highly diverse ecosystems.

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.

Reef communities show predictable undulations in linear abundance size spectra from copepods to sharks.

Among the more widely accepted general hypotheses in ecology is that community relationships between abundance and body size follow a log-linear size spectrum, from the smallest consumers to the largest predators (i.e. 'bacteria to whales'). Nevertheless, most studies only investigate small subsets of this spectrum, and note that extreme size classes in survey data deviate from linear expectations. In this study, we fit size spectra to field data from 45 rocky and coral reef sites along a 28° latitudinal gradient, comprising individuals from 0.125 mm to 2 m in body size. We found that 96% of the variation in abundance along this 'extended' size gradient was described by a single linear function across all sites. However, consistent 'wobbles' were also observed, with subtle peaks and troughs in abundance along the spectrum, which varied with sea temperature, as predicted by theory relating to trophic cascades.

Globally consistent reef size spectra integrating fishes and invertebrates.

The frequency distribution of individual body sizes in animal communities (i.e. the size spectrum) provides powerful insights for understanding the energy flux through food webs. However, studies of size spectra in rocky and coral reef communities typically focus only on fishes or invertebrates due to taxonomic and data constraints, and consequently ignore energy pathways involving the full range of macroscopic consumer taxa. We analyse size spectra with co-located fish and mobile macroinvertebrate data from 3369 reef sites worldwide, specifically focusing on how the addition of invertebrate data alters patterns. The inclusion of invertebrates steepens the size spectrum, more so in temperate regions, resulting in a consistent size spectrum slope across latitudes, and bringing slopes closer to theoretical expectations based on energy flow through the system. These results highlight the importance of understanding contributions of both invertebrates and fishes to reef food webs worldwide.

Direct and indirect effects of heatwaves on a coral reef fishery.

Marine heatwaves are increasing in frequency and intensity, and indirectly impacting coral reef fisheries through bleaching-induced degradation of live coral habitats. Marine heatwaves also affect fish metabolism and catchability, but such direct effects of elevated temperatures on reef fisheries are largely unknown. We investigated direct and indirect effects of the devastating 2016 marine heatwave on the largest reef fishery operating along the Great Barrier Reef (GBR). We used a combination of fishery-independent underwater census data on coral trout biomass (Plectropomus and Variola spp.) and catch-per-unit-effort (CPUE) data from the commercial fishery to evaluate changes in the fishery resulting from the 2016 heatwave. The heatwave caused widespread, yet locally patchy, declines in coral cover, but we observed little effect of local coral loss on coral trout biomass. Instead, a pattern of decreasing biomass at northern sites and stable or increasing biomass at southern sites suggested a direct response of populations to the heatwave. Analysis of the fishery-independent data and CPUE found that in-water coral trout biomass estimates were positively related to CPUE, and that coral trout catch rates increased with warmer temperatures. Temperature effects on catch rates were consistent with the thermal affinities of the multiple species contributing to this fishery. Scaling-up the effect of temperature on coral trout catch rates across the region suggests that GBR-wide catches were 18% higher for a given level of effort during the heatwave year relative to catch rates under the mean temperatures in the preceding 6 years. These results highlight a potentially large effect of heatwaves on catch rates of reef fishes, independent of changes in reef habitats, that can add substantial uncertainty to estimates of stock trends inferred from fishery-dependent (CPUE) data. Overestimation of CPUE could initiate declines in reef fisheries that are currently fully exploited, and threaten sustainable management of reef stocks.

Thermal biases and vulnerability to warming in the world's marine fauna.

A critical assumption underlying projections of biodiversity change associated with global warming is that ecological communities comprise balanced mixes of warm-affinity and cool-affinity species which, on average, approximate local environmental temperatures. Nevertheless, here we find that most shallow water marine species occupy broad thermal distributions that are aggregated in either temperate or tropical realms. These distributional trends result in ocean-scale spatial thermal biases, where communities are dominated by species with warmer or cooler affinity than local environmental temperatures. We use community-level thermal deviations from local temperatures as a form of sensitivity to warming, and combine these with projected ocean warming data to predict warming-related loss of species from present-day communities over the next century. Large changes in local species composition appear likely, and proximity to thermal limits, as inferred from present-day species' distributional ranges, outweighs spatial variation in warming rates in contributing to predicted rates of local species loss.

Gravity of human impacts mediates coral reef conservation gains.

Coral reefs provide ecosystem goods and services for millions of people in the tropics, but reef conditions are declining worldwide. Effective solutions to the crisis facing coral reefs depend in part on understanding the context under which different types of conservation benefits can be maximized. Our global analysis of nearly 1,800 tropical reefs reveals how the intensity of human impacts in the surrounding seascape, measured as a function of human population size and accessibility to reefs ("gravity"), diminishes the effectiveness of marine reserves at sustaining reef fish biomass and the presence of top predators, even where compliance with reserve rules is high. Critically, fish biomass in high-compliance marine reserves located where human impacts were intensive tended to be less than a quarter that of reserves where human impacts were low. Similarly, the probability of encountering top predators on reefs with high human impacts was close to zero, even in high-compliance marine reserves. However, we find that the relative difference between openly fished sites and reserves (what we refer to as conservation gains) are highest for fish biomass (excluding predators) where human impacts are moderate and for top predators where human impacts are low. Our results illustrate critical ecological trade-offs in meeting key conservation objectives: reserves placed where there are moderate-to-high human impacts can provide substantial conservation gains for fish biomass, yet they are unlikely to support key ecosystem functions like higher-order predation, which is more prevalent in reserve locations with low human impacts.

Global conservation outcomes depend on marine protected areas with five key features.

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km(2)), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.

The shape of abundance distributions across temperature gradients in reef fishes.

Improving predictions of ecological responses to climate change requires understanding how local abundance relates to temperature gradients, yet many factors influence local abundance in wild populations. We evaluated the shape of thermal-abundance distributions using 98 422 abundance estimates of 702 reef fish species worldwide. We found that curved ceilings in local abundance related to sea temperatures for most species, where local abundance declined from realised thermal 'optima' towards warmer and cooler environments. Although generally supporting the abundant-centre hypothesis, many species also displayed asymmetrical thermal-abundance distributions. For many tropical species, abundances did not decline at warm distribution edges due to an unavailability of warmer environments at the equator. Habitat transitions from coral to macroalgal dominance in subtropical zones also influenced abundance distribution shapes. By quantifying the factors constraining species' abundance, we provide an important empirical basis for improving predictions of community re-structuring in a warmer world.

Integrating abundance and functional traits reveals new global hotspots of fish diversity.

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao's Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites ('community evenness'), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

Biodiversity enhances reef fish biomass and resistance to climate change.

Fishes are the most diverse group of vertebrates, play key functional roles in aquatic ecosystems, and provide protein for a billion people, especially in the developing world. Those functions are compromised by mounting pressures on marine biodiversity and ecosystems. Because of its economic and food value, fish biomass production provides an unusually direct link from biodiversity to critical ecosystem services. We used the Reef Life Survey's global database of 4,556 standardized fish surveys to test the importance of biodiversity to fish production relative to 25 environmental drivers. Temperature, biodiversity, and human influence together explained 47% of the global variation in reef fish biomass among sites. Fish species richness and functional diversity were among the strongest predictors of fish biomass, particularly for the large-bodied species and carnivores preferred by fishers, and these biodiversity effects were robust to potentially confounding influences of sample abundance, scale, and environmental correlations. Warmer temperatures increased biomass directly, presumably by raising metabolism, and indirectly by increasing diversity, whereas temperature variability reduced biomass. Importantly, diversity and climate interact, with biomass of diverse communities less affected by rising and variable temperatures than species-poor communities. Biodiversity thus buffers global fish biomass from climate change, and conservation of marine biodiversity can stabilize fish production in a changing ocean.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.