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.

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.

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.

Marine protected areas promote stability of reef fish communities under climate warming.

Protection from direct human impacts can safeguard marine life, yet ocean warming crosses marine protected area boundaries. Here, we test whether protection offers resilience to marine heatwaves from local to network scales. We examine 71,269 timeseries of population abundances for 2269 reef fish species surveyed in 357 protected versus 747 open sites worldwide. We quantify the stability of reef fish abundance from populations to metacommunities, considering responses of species and functional diversity including thermal affinity of different trophic groups. Overall, protection mitigates adverse effects of marine heatwaves on fish abundance, community stability, asynchronous fluctuations and functional richness. We find that local stability is positively related to distance from centers of high human density only in protected areas. We provide evidence that networks of protected areas have persistent reef fish communities in warming oceans by maintaining large populations and promoting stability at different levels of biological organization.

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.

Sustainable reference points for multispecies coral reef fisheries.

Sustainably managing fisheries requires regular and reliable evaluation of stock status. However, most multispecies reef fisheries around the globe tend to lack research and monitoring capacity, preventing the estimation of sustainable reference points against which stocks can be assessed. Here, combining fish biomass data for >2000 coral reefs, we estimate site-specific sustainable reference points for coral reef fisheries and use these and available catch estimates to assess the status of global coral reef fish stocks. We reveal that >50% of sites and jurisdictions with available information have stocks of conservation concern, having failed at least one fisheries sustainability benchmark. We quantify the trade-offs between biodiversity, fish length, and ecosystem functions relative to key benchmarks and highlight the ecological benefits of increasing sustainability. Our approach yields multispecies sustainable reference points for coral reef fisheries using environmental conditions, a promising means for enhancing the sustainability of the world's coral reef fisheries.

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.

Safeguarding nutrients from coral reefs under climate change.

The sustainability of coral reef fisheries is jeopardized by complex and interacting socio-ecological stressors that undermine their contribution to food and nutrition security. Climate change has emerged as one of the key stressors threatening coral reefs and their fish-associated services. How fish nutrient concentrations respond to warming oceans remains unclear but these responses are probably affected by both direct (metabolism and trophodynamics) and indirect (habitat and species range shifts) effects. Climate-driven coral habitat loss can cause changes in fish abundance and biomass, revealing potential winners and losers among major fisheries targets that can be predicted using ecological indicators and biological traits. A critical next step is to extend research focused on the quantity of available food (fish biomass) to also consider its nutritional quality, which is relevant to progress in the fields of food security and malnutrition. Biological traits are robust predictors of fish nutrient content and thus potentially indicate how climate-driven changes are expected to impact nutrient availability within future food webs on coral reefs. Here, we outline future research priorities and an anticipatory framework towards sustainable reef fisheries contributing to nutrition-sensitive food systems in a warming ocean.

Tracking widespread climate-driven change on temperate and tropical reefs.

Warming seas, marine heatwaves, and habitat degradation are increasingly widespread phenomena affecting marine biodiversity, yet our understanding of their broader impacts is largely derived from collective insights from independent localized studies. Insufficient systematic broadscale monitoring limits our understanding of the true extent of these impacts and our capacity to track these at scales relevant to national policies and international agreements. Using an extensive time series of co-located reef fish community structure and habitat data spanning 12 years and the entire Australian continent, we found that reef fish community responses to changing temperatures and habitats are dynamic and widespread but regionally patchy. Shifts in composition and abundance of the fish community often occurred within 2 years of environmental or habitat change, although the relative importance of these two mechanisms of climate impact tended to differ between tropical and temperate zones. The clearest of these changes on temperate and subtropical reefs were temperature related, with responses measured by the reef fish thermal index indicating reshuffling according to the thermal affinities of species present. On low latitude coral reefs, the community generalization index indicated shifting dominance of habitat generalist fishes through time, concurrent with changing coral cover. Our results emphasize the importance of maintaining local ecological detail when scaling up datasets to inform national policies and global biodiversity targets. Scaled-up ecological monitoring is needed to discriminate among increasingly diverse drivers of large-scale biodiversity change and better connect presently disjointed systems of biodiversity observation, indicator research, and governance.

Anthropogenic disruptions to longstanding patterns of trophic-size structure in vertebrates.

Diet and body mass are inextricably linked in vertebrates: while herbivores and carnivores have converged on much larger sizes, invertivores and omnivores are, on average, much smaller, leading to a roughly U-shaped relationship between body size and trophic guild. Although this U-shaped trophic-size structure is well documented in extant terrestrial mammals, whether this pattern manifests across diverse vertebrate clades and biomes is unknown. Moreover, emergence of the U-shape over geological time and future persistence are unknown. Here we compiled a comprehensive dataset of diet and body size spanning several vertebrate classes and show that the U-shaped pattern is taxonomically and biogeographically universal in modern vertebrate groups, except for marine mammals and seabirds. We further found that, for terrestrial mammals, this U-shape emerged by the Palaeocene and has thus persisted for at least 66 million years. Yet disruption of this fundamental trophic-size structure in mammals appears likely in the next century, based on projected extinctions. Actions to prevent declines in the largest animals will sustain the functioning of Earth's wild ecosystems and biomass energy distributions that have persisted through deep time.

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.

Community size structure varies with predator-prey size relationships and temperature across Australian reefs.

Climate change and fisheries exploitation are dramatically changing the abundances, species composition, and size spectra of fish communities. We explore whether variation in 'abundance size spectra', a widely studied ecosystem feature, is influenced by a parameter theorized to govern the shape of size-structured ecosystems-the relationship between the sizes of predators and their prey (predator-prey mass ratios, or PPMRs). PPMR estimates are lacking for avast number of fish species, including at the scale of trophic guilds. Using measurements of 8128 prey items in gut contents of 97 reef fish species, we established predator-prey mass ratios (PPMRs) for four major trophic guilds (piscivores, invertivores, planktivores, and herbivores) using linear mixed effects models. To assess the theoretical predictions that higher community-level PPMRs leads to shallower size spectrum slopes, we compared observations of both ecosystem metrics for ~15,000 coastal reef sites distributed around Australia. PPMRs of individual fishes were remarkably high (median ~71,000), with significant variation between different trophic guilds (~890 for piscivores; ~83,000 for planktivores), and ~8700 for whole communities. Community-level PPMRs were positively related to size spectrum slopes, broadly consistent with theory, however, this pattern was also influenced by the latitudinal temperature gradient. Tropical reefs showed a stronger relationship between community-level PPMRs and community size spectrum slopes than temperate reefs. The extent that these patterns apply outside Australia and consequences for community structure and dynamics are key areas for future investigation.

Biological trade-offs underpin coral reef ecosystem functioning.

Human impact increasingly alters global ecosystems, often reducing biodiversity and disrupting the provision of essential ecosystem services to humanity. Therefore, preserving ecosystem functioning is a critical challenge of the twenty-first century. Coral reefs are declining worldwide due to the pervasive effects of climate change and intensive fishing, and although research on coral reef ecosystem functioning has gained momentum, most studies rely on simplified proxies, such as fish biomass. This lack of quantitative assessments of multiple process-based ecosystem functions hinders local and regional conservation efforts. Here we combine global coral reef fish community surveys and bioenergetic models to quantify five key ecosystem functions mediated by coral reef fishes. We show that functions exhibit critical trade-offs driven by varying community structures, such that no community can maximize all functions. Furthermore, functions are locally dominated by few species, but the identity of dominant species substantially varies at the global scale. In fact, half of the 1,110 species in our dataset are functionally dominant in at least one location. Our results reinforce the need for a nuanced, locally tailored approach to coral reef conservation that considers multiple ecological functions beyond the effect of standing stock biomass.

Species richness and identity both determine the biomass of global reef fish communities.

Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relationship depends on the taxonomic identities rather than the number of species remains untested at broad scales. Here, we partition the effects of declining species richness and changing community composition on fish community biomass across >3000 coral and rocky reef sites globally. We find that high biodiversity is 5.7x more important in maximizing biomass than the remaining influence of other ecological and environmental factors. Differences in fish community biomass across space are equally driven by both reductions in the total number of species and the disproportionate loss of larger-than-average species, which is exacerbated at sites impacted by humans. Our results confirm that sustaining biomass and associated ecosystem functions requires protecting diversity, most importantly of multiple large-bodied species in areas subject to strong human influences.

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.

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.

Habitat loss and range shifts contribute to ecological generalization among reef fishes.

Human activities are altering the structure of ecological communities, often favouring generalists over specialists. For reef fishes, increasingly degraded habitats and climate-driven range shifts may independently augment generalization, particularly if fishes with least-specific habitat requirements are more likely to shift geographic ranges to track their thermal niche. Using a unique global dataset on temperate and tropical reef fishes and habitat composition, we calculated a species generalization index that empirically estimates the habitat niche breadth of each fish species. We then applied the species generalization index to evaluate potential impacts of habitat loss and range shifts across large scales, on coral and rocky reefs. Our analyses revealed consistent habitat-induced shifts in community structure that favoured generalist fishes following regional coral mortality events and between adjacent sea urchin barrens and kelp habitats. Analysis of the distribution of tropical fishes also identified the species generalization index as the most important trait in predicting their poleward range extent, more so than body or range size. Generalist tropical reef fishes penetrate further into subtropical and temperate zones than specialists. Dynamic responses of reef fishes to habitat degradation imply loss of specialists at local scales, while generalists will be broadly favoured under intensifying anthropogenic pressures. An increased focus on individual requirements of specialists could provide useful guidance for species threat assessments and conservation actions, while ecosystem and multi-species fisheries models should recognize increasing prevalence of generalists.

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.

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.