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

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

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

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

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

Since the 1950s, industrial fisheries have expanded globally, as fishing vessels are required to travel further afield for fishing opportunities. Technological advancements and fishery subsidies have granted ever-increasing access to populations of sharks, tunas, billfishes, and other predators. Wilderness refuges, defined here as areas beyond the detectable range of human influence, are therefore increasingly rare. In order to achieve marine resources sustainability, large no-take marine protected areas (MPAs) with pelagic components are being implemented. However, such conservation efforts require knowledge of the critical habitats for predators, both across shallow reefs and the deeper ocean. Here, we fill this gap in knowledge across the Indo-Pacific by using 1,041 midwater baited videos to survey sharks and other pelagic predators such as rainbow runner (Elagatis bipinnulata), mahi-mahi (Coryphaena hippurus), and black marlin (Istiompax indica). We modeled three key predator community attributes: vertebrate species richness, mean maximum body size, and shark abundance as a function of geomorphology, environmental conditions, and human pressures. All attributes were primarily driven by geomorphology (35%-62% variance explained) and environmental conditions (14%-49%). While human pressures had no influence on species richness, both body size and shark abundance responded strongly to distance to human markets (12%-20%). Refuges were identified at more than 1,250 km from human markets for body size and for shark abundance. These refuges were identified as remote and shallow seabed features, such as seamounts, submerged banks, and reefs. Worryingly, hotpots of large individuals and of shark abundance are presently under-represented within no-take MPAs that aim to effectively protect marine predators, such as the British Indian Ocean Territory. Population recovery of predators is unlikely to occur without strategic placement and effective enforcement of large no-take MPAs in both coastal and remote locations.

Genomic insights into the historical and contemporary demographics of the grey reef shark.

Analyses of genetic diversity can shed light on both the origins of biodiversity hotspots, as well as the conservation status of species that are impacted by human activities. With these objectives, we assembled a genomic dataset of 14,935 single nucleotide polymorphisms from 513 grey reef sharks (Carcharhinus amblyrhynchos) sampled across 17 locations in the tropical Indo-Pacific. We analysed geographic variation in genetic diversity, estimated ancient and contemporary effective population size (Ne) across sampling locations (using coalescent and linkage disequilibrium methods) and modelled the history of gene flow between the Coral Triangle and the Coral Sea. Genetic diversity decreased with distance away from the Coral Triangle and north-western Australia, implying that C. amblyrhynchos may have originated in this region. Increases in Ne were detected across almost all sampling locations 40,000-90,000 generations ago (approximately 0.6-1.5 mya, given an estimated generation time of 16.4 years), suggesting a range expansion around this time. More recent, secondary increases in Ne were inferred for the Misool and North Great Barrier Reef sampling locations, but joint modelling did not clarify whether these were due to population growth, migration, or both. Despite the greater genetic diversity and ancient Ne observed at sites around Australia and the Coral Triangle, remote reefs around north-western New Caledonia had the highest contemporary Ne, demonstrating the importance of using multiple population size assessment methods. This study provides insight into both the past and present demographics of C. amblyrhynchos and contributes to our understanding of evolution in marine biodiversity hotspots.

Leveraging social media and deep learning to detect rare megafauna in video surveys.

Deep learning has become a key tool for the automated monitoring of animal populations with video surveys. However, obtaining large numbers of images to train such models is a major challenge for rare and elusive species because field video surveys provide few sightings. We designed a method that takes advantage of videos accumulated on social media for training deep-learning models to detect rare megafauna species in the field. We trained convolutional neural networks (CNNs) with social media images and tested them on images collected from field surveys. We applied our method to aerial video surveys of dugongs (Dugong dugon) in New Caledonia (southwestern Pacific). CNNs trained with 1303 social media images yielded 25% false positives and 38% false negatives when tested on independent field video surveys. Incorporating a small number of images from New Caledonia (equivalent to 12% of social media images) in the training data set resulted in a nearly 50% decrease in false negatives. Our results highlight how and the extent to which images collected on social media can offer a solid basis for training deep-learning models for rare megafauna detection and that the incorporation of a few images from the study site further boosts detection accuracy. Our method provides a new generation of deep-learning models that can be used to rapidly and accurately process field video surveys for the monitoring of rare megafauna.

El aprendizaje profundo se ha convertido en una importante herramienta para el monitoreo automatizado de las poblaciones animales con video-censos. Sin embargo, la obtención de cantidades abundantes de imágenes para preparar dichos modelos es un reto primordial para las especies elusivas e infrecuentes porque los video-censos de campo proporcionan pocos avistamientos. Diseñamos un método que aprovecha los videos acumulados en las redes sociales para preparar a los modelos de aprendizaje profundo para detectar especies infrecuentes de megafauna en el campo. Preparamos algunas redes neurales convolucionales con imágenes tomadas de las redes sociales y las pusimos a prueba con imágenes tomadas en los censos de campo. Aplicamos nuestro método a los censos aéreos en video de dugongos (Dugong dugon) en Nueva Caledonia (Pacífico sudoccidental). Las redes neurales convolucionales preparadas con 1,303 imágenes de las redes sociales produjeron 25% de falsos positivos y 38% de falsos negativos cuando las probamos en video-censos de campo independientes. La incorporación de un número pequeño de imágenes tomadas en Nueva Caledonia (equivalente al 12% de las imágenes de las redes sociales) dentro del conjunto de datos usados en la preparación dio como resultado una disminución de casi el 50% en los falsos negativos. Nuestros resultados destacan cómo y a qué grado las imágenes recolectadas en las redes sociales pueden ofrecer una base sólida para la preparación de modelos de aprendizaje profundo para la detección de megafauna infrecuente. También resaltan que la incorporación de unas cuantas imágenes del sitio de estudio aumenta mucho más la certeza de detección. Nuestro método proporciona una nueva generación de modelos de aprendizaje profundo que pueden usarse para procesar rápida y acertadamente los video-censos de campo para el monitoreo de megafauna infrecuente.

Bright spots among the world's coral reefs.

Ongoing declines in the structure and function of the world's coral reefs require novel approaches to sustain these ecosystems and the millions of people who depend on them3. A presently unexplored approach that draws on theory and practice in human health and rural development is to systematically identify and learn from the 'outliers'­places where ecosystems are substantially better ('bright spots') or worse ('dark spots') than expected, given the environmental conditions and socioeconomic drivers they are exposed to. Here we compile data from more than 2,500 reefs worldwide and develop a Bayesian hierarchical model to generate expectations of how standing stocks of reef fish biomass are related to 18 socioeconomic drivers and environmental conditions. We identify 15 bright spots and 35 dark spots among our global survey of coral reefs, defined as sites that have biomass levels more than two standard deviations from expectations. Importantly, bright spots are not simply comprised of remote areas with low fishing pressure; they include localities where human populations and use of ecosystem resources is high, potentially providing insights into how communities have successfully confronted strong drivers of change. Conversely, dark spots are not necessarily the sites with the lowest absolute biomass and even include some remote, uninhabited locations often considered near pristine6. We surveyed local experts about social, institutional, and environmental conditions at these sites to reveal that bright spots are characterized by strong sociocultural institutions such as customary taboos and marine tenure, high levels of local engagement in management, high dependence on marine resources, and beneficial environmental conditions such as deep-water refuges. Alternatively, dark spots are characterized by intensive capture and storage technology and a recent history of environmental shocks. Our results suggest that investments in strengthening fisheries governance, particularly aspects such as participation and property rights, could facilitate innovative conservation actions that help communities defy expectations of global reef degradation.

Evaluating Age and Growth Relationship to Ciguatoxicity in Five Coral Reef Fish Species from French Polynesia.

Ciguatera poisoning (CP) results from the consumption of coral reef fish or marine invertebrates contaminated with potent marine polyether compounds, namely ciguatoxins. In French Polynesia, 220 fish specimens belonging to parrotfish (Chlorurus microrhinos, Scarus forsteni, and Scarus ghobban), surgeonfish (Naso lituratus), and groupers (Epinephelus polyphekadion) were collected from two sites with contrasted risk of CP, i.e., Kaukura Atoll versus Mangareva Island. Fish age and growth were assessed from otoliths' yearly increments and their ciguatoxic status (negative, suspect, or positive) was evaluated by neuroblastoma cell-based assay. Using permutational multivariate analyses of variance, no significant differences in size and weight were found between negative and suspect specimens while positive specimens showed significantly greater size and weight particularly for E. polyphekadion and S. ghobban. However, eating small or low-weight specimens remains risky due to the high variability in size and weight of positive fish. Overall, no relationship could be evidenced between fish ciguatoxicity and age and growth characteristics. In conclusion, size, weight, age, and growth are not reliable determinants of fish ciguatoxicity which appears to be rather species and/or site-specific, although larger fish pose an increased risk of poisoning. Such findings have important implications in current CP risk management programs.

Confronting Deep-Learning and Biodiversity Challenges for Automatic Video-Monitoring of Marine Ecosystems.

With the availability of low-cost and efficient digital cameras, ecologists can now survey the world's biodiversity through image sensors, especially in the previously rather inaccessible marine realm. However, the data rapidly accumulates, and ecologists face a data processing bottleneck. While computer vision has long been used as a tool to speed up image processing, it is only since the breakthrough of deep learning (DL) algorithms that the revolution in the automatic assessment of biodiversity by video recording can be considered. However, current applications of DL models to biodiversity monitoring do not consider some universal rules of biodiversity, especially rules on the distribution of species abundance, species rarity and ecosystem openness. Yet, these rules imply three issues for deep learning applications: the imbalance of long-tail datasets biases the training of DL models; scarce data greatly lessens the performances of DL models for classes with few data. Finally, the open-world issue implies that objects that are absent from the training dataset are incorrectly classified in the application dataset. Promising solutions to these issues are discussed, including data augmentation, data generation, cross-entropy modification, few-shot learning and open set recognition. At a time when biodiversity faces the immense challenges of climate change and the Anthropocene defaunation, stronger collaboration between computer scientists and ecologists is urgently needed to unlock the automatic monitoring of biodiversity.

Seascape genomics reveals candidate molecular targets of heat stress adaptation in three coral species.

Anomalous heat waves are causing a major decline of hard corals around the world and threatening the persistence of coral reefs. There are, however, reefs that have been exposed to recurrent thermal stress over the years and whose corals appear to have been tolerant against heat. One of the mechanisms that could explain this phenomenon is local adaptation, but the underlying molecular mechanisms are poorly known. In this work, we applied a seascape genomics approach to study heat stress adaptation in three coral species of New Caledonia (southwestern Pacific) and to uncover the molecular actors potentially involved. We used remote sensing data to characterize the environmental trends across the reef system, and sampled corals living at the most contrasted sites. These samples underwent next generation sequencing to reveal single nucleotide polymorphisms (SNPs), frequencies of which were associated with heat stress gradients. As these SNPs might underpin an adaptive role, we characterized the functional roles of the genes located in their genomic region. In each of the studied species, we found heat stress-associated SNPs located in proximity of genes involved in pathways well known to contribute to the cellular responses against heat, such as protein folding, oxidative stress homeostasis, inflammatory and apoptotic pathways, and DNA damage-repair. In some cases, the same candidate molecular targets of heat stress adaptation recurred among species. Together, these results underline the relevance and the power of the seascape genomics approach for the discovery of adaptive traits that could allow corals to persist across wider thermal ranges.

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.

Community-wide scan identifies fish species associated with coral reef services across the Indo-Pacific.

Determining whether many functionally complementary species or only a subset of key species are necessary to maintain ecosystem functioning and services is a critical question in community ecology and biodiversity conservation. Identifying such key species remains challenging, especially in the tropics where many species co-occur and can potentially support the same or different processes. Here, we developed a new community-wide scan (CWS) approach, analogous to the genome-wide scan, to identify fish species that significantly contribute, beyond the socio-environmental and species richness effects, to the biomass and coral cover on Indo-Pacific reefs. We found that only a limited set of species (51 out of approx. 400, approx. 13%), belonging to various functional groups and evolutionary lineages, are strongly and positively associated with fish biomass and live coral cover. Many of these species have not previously been identified as functionally important, and thus may be involved in unknown, yet important, biological mechanisms that help sustain healthy and productive coral reefs. CWS has the potential to reveal species that are key to ecosystem functioning and services and to guide management strategies as well as new experiments to decipher underlying causal ecological processes.

Human activities as a driver of spatial variation in the trophic structure of fish communities on Pacific coral reefs.

Anthropogenic activities such as land-use change, pollution and fishing impact the trophic structure of coral reef fishes, which can influence ecosystem health and function. Although these impacts may be ubiquitous, they are not consistent across the tropical Pacific Ocean. Using an extensive database of fish biomass sampled using underwater visual transects on coral reefs, we modelled the impact of human activities on food webs at Pacific-wide and regional (1,000s-10,000s km) scales. We found significantly lower biomass of sharks and carnivores, where there were higher densities of human populations (hereafter referred to as human activity); however, these patterns were not spatially consistent as there were significant differences in the trophic structures of fishes among biogeographic regions. Additionally, we found significant changes in the benthic structure of reef environments, notably a decline in coral cover where there was more human activity. Direct human impacts were the strongest in the upper part of the food web, where we found that in a majority of the Pacific, the biomass of reef sharks and carnivores were significantly and negatively associated with human activity. Finally, although human-induced stressors varied in strength and significance throughout the coral reef food web across the Pacific, socioeconomic variables explained more variation in reef fish trophic structure than habitat variables in a majority of the biogeographic regions. Notably, economic development (measured as GDP per capita) did not guarantee healthy reef ecosystems (high coral cover and greater fish biomass). Our results indicate that human activities are significantly shaping patterns of trophic structure of reef fishes in a spatially nonuniform manner across the Pacific Ocean, by altering processes that organize communities in both "top-down" (fishing of predators) and "bottom-up" (degradation of benthic communities) contexts.

Fishing degrades size structure of coral reef fish communities.

Fishing pressure on coral reef ecosystems has been frequently linked to reductions of large fishes and reef fish biomass. Associated impacts on overall community structure are, however, less clear. In size-structured aquatic ecosystems, fishing impacts are commonly quantified using size spectra, which describe the distribution of individual body sizes within a community. We examined the size spectra and biomass of coral reef fish communities at 38 US-affiliated Pacific islands that ranged in human presence from near pristine to human population centers. Size spectra 'steepened' steadily with increasing human population and proximity to market due to a reduction in the relative biomass of large fishes and an increase in the dominance of small fishes. Reef fish biomass was substantially lower on inhabited islands than uninhabited ones, even at inhabited islands with the lowest levels of human presence. We found that on populated islands size spectra exponents decreased (analogous to size spectra steepening) linearly with declining biomass, whereas on uninhabited islands there was no relationship. Size spectra were steeper in regions of low sea surface temperature but were insensitive to variation in other environmental and geomorphic covariates. In contrast, reef fish biomass was highly sensitive to oceanographic conditions, being influenced by both oceanic productivity and sea surface temperature. Our results suggest that community size structure may be a more robust indicator than fish biomass to increasing human presence and that size spectra are reliable indicators of exploitation impacts across regions of different fish community compositions, environmental drivers, and fisheries types. Size-based approaches that link directly to functional properties of fish communities, and are relatively insensitive to abiotic variation across biogeographic regions, offer great potential for developing our understanding of fishing impacts in coral reef ecosystems.

Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs.

When tropical systems lose species, they are often assumed to be buffered against declines in functional diversity by the ability of the species-rich biota to display high functional redundancy: i.e., a high number of species performing similar functions. We tested this hypothesis using a ninefold richness gradient in global fish faunas on tropical reefs encompassing 6,316 species distributed among 646 functional entities (FEs): i.e., unique combinations of functional traits. We found that the highest functional redundancy is located in the Central Indo-Pacific with a mean of 7.9 species per FE. However, this overall level of redundancy is disproportionately packed into few FEs, a pattern termed functional over-redundancy (FOR). For instance, the most speciose FE in the Central Indo-Pacific contains 222 species (out of 3,689) whereas 38% of FEs (180 out of 468) have no functional insurance with only one species. Surprisingly, the level of FOR is consistent across the six fish faunas, meaning that, whatever the richness, over a third of the species may still be in overrepresented FEs whereas more than one third of the FEs are left without insurance, these levels all being significantly higher than expected by chance. Thus, our study shows that, even in high-diversity systems, such as tropical reefs, functional diversity remains highly vulnerable to species loss. Although further investigations are needed to specifically address the influence of redundant vs. vulnerable FEs on ecosystem functioning, our results suggest that the promised benefits from tropical biodiversity may not be as strong as previously thought.

How accessible are coral reefs to people? A global assessment based on travel time.

The depletion of natural resources has become a major issue in many parts of the world, with the most accessible resources being most at risk. In the terrestrial realm, resource depletion has classically been related to accessibility through road networks. In contrast, in the marine realm, the impact on living resources is often framed into the Malthusian theory of human density around ecosystems. Here, we develop a new framework to estimate the accessibility of global coral reefs using potential travel time from the nearest human settlement or market. We show that 58% of coral reefs are located < 30 min from the nearest human settlement. We use a case study from New Caledonia to demonstrate that travel time from the market is a strong predictor of fish biomass on coral reefs. We also highlight a relative deficit of protection on coral reef areas near people, with disproportional protection on reefs far from people. This suggests that conservation efforts are targeting low-conflict reefs or places that may already be receiving de facto protection due to their isolation. Our global assessment of accessibility in the marine realm is a critical step to better understand the interplay between humans and resources.

Unexpected high vulnerability of functions in wilderness areas: evidence from coral reef fishes.

High species richness is thought to support the delivery of multiple ecosystem functions and services under changing environments. Yet, some species might perform unique functional roles while others are redundant. Thus, the benefits of high species richness in maintaining ecosystem functioning are uncertain if functions have little redundancy, potentially leading to high vulnerability of functions. We studied the natural propensity of assemblages to be functionally buffered against loss prior to fishing activities, using functional trait combinations, in coral reef fish assemblages across unfished wilderness areas of the Indo-Pacific: Chagos Archipelago, New Caledonia and French Polynesia. Fish functional diversity in these wilderness areas is highly vulnerable to fishing, explained by species- and abundance-based redundancy packed into a small combination of traits, leaving most other trait combinations (60%) sensitive to fishing, with no redundancy. Functional vulnerability peaks for mobile and sedentary top predators, and large species in general. Functional vulnerability decreases for certain functional entities in New Caledonia, where overall functional redundancy was higher. Uncovering these baseline patterns of functional vulnerability can offer early warning signals of the damaging effects from fishing, and may serve as baselines to guide precautionary and even proactive conservation actions.

Adult and larval traits as determinants of geographic range size among tropical reef fishes.

Most marine organisms disperse via ocean currents as larvae, so it is often assumed that larval-stage duration is the primary determinant of geographic range size. However, empirical tests of this relationship have yielded mixed results, and alternative hypotheses have rarely been considered. Here we assess the relative influence of adult and larval-traits on geographic range size using a global dataset encompassing 590 species of tropical reef fishes in 47 families, the largest compilation of such data to date for any marine group. We analyze this database using linear mixed-effect models to control for phylogeny and geographical limits on range size. Our analysis indicates that three adult traits likely to affect the capacity of new colonizers to survive and establish reproductive populations (body size, schooling behavior, and nocturnal activity) are equal or better predictors of geographic range size than pelagic larval duration. We conclude that adult life-history traits that affect the postdispersal persistence of new populations are primary determinants of successful range extension and, consequently, of geographic range size among tropical reef fishes.

Global mismatch between species richness and vulnerability of reef fish assemblages.

The impact of anthropogenic activity on ecosystems has highlighted the need to move beyond the biogeographical delineation of species richness patterns to understanding the vulnerability of species assemblages, including the functional components that are linked to the processes they support. We developed a decision theory framework to quantitatively assess the global taxonomic and functional vulnerability of fish assemblages on tropical reefs using a combination of sensitivity to species loss, exposure to threats and extent of protection. Fish assemblages with high taxonomic and functional sensitivity are often exposed to threats but are largely missed by the global network of marine protected areas. We found that areas of high species richness spatially mismatch areas of high taxonomic and functional vulnerability. Nevertheless, there is strong spatial match between taxonomic and functional vulnerabilities suggesting a potential win-win conservation-ecosystem service strategy if more protection is set in these locations.

Divergent responses of pelagic and benthic fish body-size structure to remoteness and protection from humans.

Animal body-size variation influences multiple processes in marine ecosystems, but habitat heterogeneity has prevented a comprehensive assessment of size across pelagic (midwater) and benthic (seabed) systems along anthropic gradients. In this work, we derive fish size indicators from 17,411 stereo baited-video deployments to test for differences between pelagic and benthic responses to remoteness from human pressures and effectiveness of marine protected areas (MPAs). From records of 823,849 individual fish, we report divergent responses between systems, with pelagic size structure more profoundly eroded near human markets than benthic size structure, signifying greater vulnerability of pelagic systems to human pressure. Effective protection of benthic size structure can be achieved through MPAs placed near markets, thereby contributing to benthic habitat restoration and the recovery of associated fishes. By contrast, recovery of the world's largest and most endangered fishes in pelagic systems requires the creation of highly protected areas in remote locations, including on the High Seas, where protection efforts lag.

The coral sea: physical environment, ecosystem status and biodiversity assets.

The Coral Sea, located at the southwestern rim of the Pacific Ocean, is the only tropical marginal sea where human impacts remain relatively minor. Patterns and processes identified within the region have global relevance as a baseline for understanding impacts in more disturbed tropical locations. Despite 70 years of documented research, the Coral Sea has been relatively neglected, with a slower rate of increase in publications over the past 20 years than total marine research globally. We review current knowledge of the Coral Sea to provide an overview of regional geology, oceanography, ecology and fisheries. Interactions between physical features and biological assemblages influence ecological processes and the direction and strength of connectivity among Coral Sea ecosystems. To inform management effectively, we will need to fill some major knowledge gaps, including geographic gaps in sampling and a lack of integration of research themes, which hinder the understanding of most ecosystem processes.