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.

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.

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.

Population parameters and conservation implications for one of the world's rarest marine fishes, the red handfish (Thymichthys politus).

Population estimates are required for effective conservation of many rare marine species, but can be difficult to obtain. The critically endangered red handfish (Thymichthys politus) is a coastal anglerfish known only from two fragmented populations in southeast Tasmania, Australia. It is at a high risk of extinction due to low numbers, loss of habitat, and the impacts of climate change. To aid conservation efforts, we provide the first empirical population size estimates of red handfish and investigate other important aspects of the species' life history, such as growth, habitat association, and movement. We surveyed both red handfish local populations via underwater visual census on scuba over 3 years and used photographic mark-recapture techniques to estimate biological parameters. In 2020, the local adult population size was estimated to be 94 (95% confidence interval [CI] 40-231) adults at one site, and 7 (95% CI 5-10) at the other site, suggesting an estimated global population of 101 adults. Movement of individuals was extremely limited at 48.5 m (± 77.7 S.D.) per year. We also found evidence of declining fish density, a declining proportion of juveniles, and increasing average fish size during the study. These results provide a serious warning that red handfish are likely sliding toward extinction, and highlight the urgent need to expand efforts for ex situ captive breeding to bolster numbers in the wild and maintain captive insurance populations, and to protect vital habitat to safeguard the species' ongoing survival in the wild.

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.

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.

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.

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.

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.

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.

A community and functional comparison of coral and reef fish assemblages between four decades of coastal urbanisation and thermal stress.

Urbanized coral reefs experience anthropogenic disturbances caused by coastal development, pollution, and nutrient runoff, resulting in turbid, marginal conditions in which only certain species can persist. Mortality effects are exacerbated by increasingly regular thermal stress events, leading to shifts towards novel communities dominated by habitat generalists and species with low structural complexity.There is limited data on the turnover processes that occur due to this convergence of anthropogenic stressors, and how novel urban ecosystems are structured both at the community and functional levels. As such, it is unclear how they will respond to future disturbance events.Here, we examine the patterns of coral reef community change and determine whether ecosystem functions provided by specialist species are lost post-disturbance. We present a comparison of community and functional trait-based changes for scleractinian coral genera and reef fish species assemblages subject to coastal development, coastal modification, and mass bleaching between two time periods, 1975-1976 and 2018, in Nakagusuku Bay, Okinawa, Japan.We observed an increase in fish habitat generalists, a dominance shift from branching to massive/sub-massive corals and increasing site-based coral genera richness between years. Fish and coral communities significantly reassembled, but functional trait-based multivariate space remained constant, indicating a turnover of species with similar traits. A compression of coral habitat occurred, with shallow (<5 m) and deep (>8 m) coral genera shifting towards the mid-depths (5-8 m).We show that although reef species assemblages altered post disturbance, new communities retained similar ecosystem functions. This result could be linked to the stressors experienced by urban reefs, which reflect those that will occur at an increasing frequency globally in the near future. Yet, even after shifts to disturbed communities, these fully functioning reef systems may maintain high conservation value.

Persistent thermally driven shift in the functional trait structure of herbivorous fishes: Evidence of top-down control on the rebound potential of temperate seaweed forests?

Extreme climatic events can reshape the functional structure of ecological communities, potentially altering ecological interactions and ecosystem functioning. While these shifts have been widely documented, evidence of their persistence and potential flow-on effects on ecosystem structure following relaxation of extreme events remains limited. Here, we investigate changes in the functional trait structure - encompassing dimensions of resource use, thermal affinity, and body size - of herbivorous fishes in a temperate reef system that experienced an extreme marine heatwave (MHW) and subsequent return to cool conditions. We quantify how changes in the trait structure modified the nature and intensity of herbivory-related functions (macroalgae, turf, and sediment removal), and explored the potential flow-on effects on the recovery dynamics of macroalgal foundation species. The trait structure of the herbivorous fish assemblage shifted as a result of the MHW, from dominance of cool-water browsing species to increased evenness in the distribution of abundance among temperate and tropical guilds supporting novel herbivory roles (i.e. scraping, cropping, and sediment sucking). Despite the abundance of tropical herbivorous fishes and intensity of herbivory-related functions declined following a period of cooling after the MHW, the underlying trait structure displayed limited recovery. Concomitantly, algal assemblages displayed a lack of recovery of the formerly dominant foundational species, the kelp Ecklonia radiata, transitioning to an alternative state dominated by turf and Sargassum spp. Our study demonstrates a legacy effect of an extreme MHW and exemplified the value of monitoring phenotypic (trait mediated) changes in the nature of core ecosystem processes to predict and adapt to the future configurations of changing reef ecosystems.

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.

Climate change: Large-scale abundance shifts in fishes.

Warming seas are driving a mass-scale restructuring of marine life, with observed responses expanding beyond species' range shifts. New evidence highlights large regions where ecological change has been dominated by the declining abundance of species that prefer cooler waters.

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.