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Changes in disturbance regimes due to climate change are increasingly challenging the capacity of ecosystems to absorb recurrent shocks and reassemble afterwards, escalating the risk of widespread ecological collapse of current ecosystems and the emergence of novel assemblages 1 – 3 . In marine systems, the production of larvae and recruitment of functionally important species are fundamental processes for rebuilding depleted adult populations, maintaining resilience and avoiding regime shifts in the face of rising environmental pressures 4 , 5 . Here we document a regional-scale shift in stock–recruitment relationships of corals along the Great Barrier Reef—the world’s largest coral reef system—following unprecedented back-to-back mass bleaching events caused by global warming. As a consequence of mass mortality of adult brood stock in 2016 and 2017 owing to heat stress 6 , the amount of larval recruitment declined in 2018 by 89% compared to historical levels. For the first time, brooding pocilloporids replaced spawning acroporids as the dominant taxon in the depleted recruitment pool. The collapse in stock–recruitment relationships indicates that the low resistance of adult brood stocks to repeated episodes of coral bleaching is inexorably tied to an impaired capacity for recovery, which highlights the multifaceted processes that underlie the global decline of coral reefs. The extent to which the Great Barrier Reef will be able to recover from the collapse in stock–recruitment relationships remains uncertain, given the projected increased frequency of extreme climate events over the next two decades 7 . A regional-scale shift in the relationships between adult stock and recruitment of corals occurred along the Great Barrier Reef, following mass bleaching events in 2016 and 2017 caused by global warming.

Global warming is markedly changing diverse coral reef ecosystems through an increasing frequency and magnitude of mass bleaching events 1 – 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 species 4 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 bleaching 2 , 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 decade 5 , 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 limits 7 . Fish and invertebrate communities transformed across the span of the Great Barrier Reef following the 2016 bleaching event due to a decline in coral-feeding fishes resulting from coral loss, and because of different regional responses of key trophic groups to the direct effect of temperature.

An analysis of 21 coral reefs in the Indian Ocean using data across 17 years that spanned a major climatic disturbance reveals factors that predispose a coral reef to recovery or regime shift from hard corals to macroalgae; these results could foreshadow the likely outcomes of tropical coral reefs to the effects of climate change, informing management and adaptation plans. Coral reef adaptation to change When coral reefs are damaged, their ecosystem can change so radically that a new stable state is reached. This process, known as regime shift, is occurring globally: previously super-diverse reefs are becoming dominated by macroalgae instead of coral, losing animal biodiversity and potentially ecosystem services as a result. Regime shift is not ubiquitous however, and perturbed reefs can also recover to their coral-dominated state. Nicholas Graham and colleagues used long-term data from 21 perturbed reefs in the Indo-Pacific region to examine the factors predisposing a reef to recovery or regime shift. By way of this natural experiment, they identify thresholds for characteristics such as structural complexity, water depth and fish density that predict reef responses to an extreme weather event. These results improve our understanding of one of the greatest threats to marine biodiversity and could enable pre-emptive action to mitigate climate change effects on tropical coral reefs. Climate-induced coral bleaching is among the greatest current threats to coral reefs, causing widespread loss of live coral cover 1 . Conditions under which reefs bounce back from bleaching events or shift from coral to algal dominance are unknown, making it difficult to predict and plan for differing reef responses under climate change 2 . Here we document and predict long-term reef responses to a major climate-induced coral bleaching event that caused unprecedented region-wide mortality of Indo-Pacific corals. Following loss of >90% live coral cover, 12 of 21 reefs recovered towards pre-disturbance live coral states, while nine reefs underwent regime shifts to fleshy macroalgae. Functional diversity of associated reef fish communities shifted substantially following bleaching, returning towards pre-disturbance structure on recovering reefs, while becoming progressively altered on regime shifting reefs. We identified threshold values for a range of factors that accurately predicted ecosystem response to the bleaching event. Recovery was favoured when reefs were structurally complex and in deeper water, when density of juvenile corals and herbivorous fishes was relatively high and when nutrient loads were low. Whether reefs were inside no-take marine reserves had no bearing on ecosystem trajectory. Although conditions governing regime shift or recovery dynamics were diverse, pre-disturbance quantification of simple factors such as structural complexity and water depth accurately predicted ecosystem trajectories. These findings foreshadow the likely divergent but predictable outcomes for reef ecosystems in response to climate change, thus guiding improved management and adaptation.

Global warming is rapidly emerging as a universal threat to ecological integrity and function, highlighting the urgent need for a better understanding of the impact of heat exposure on the resilience of ecosystems and the people who depend on them 1 . Here we show that in the aftermath of the record-breaking marine heatwave on the Great Barrier Reef in 2016 2 , corals began to die immediately on reefs where the accumulated heat exposure exceeded a critical threshold of degree heating weeks, which was 3–4 °C-weeks. After eight months, an exposure of 6 °C-weeks or more drove an unprecedented, regional-scale shift in the composition of coral assemblages, reflecting markedly divergent responses to heat stress by different taxa. Fast-growing staghorn and tabular corals suffered a catastrophic die-off, transforming the three-dimensionality and ecological functioning of 29% of the 3,863 reefs comprising the world’s largest coral reef system. Our study bridges the gap between the theory and practice of assessing the risk of ecosystem collapse, under the emerging framework for the International Union for Conservation of Nature (IUCN) Red List of Ecosystems 3 , by rigorously defining both the initial and collapsed states, identifying the major driver of change, and establishing quantitative collapse thresholds. The increasing prevalence of post-bleaching mass mortality of corals represents a radical shift in the disturbance regimes of tropical reefs, both adding to and far exceeding the influence of recurrent cyclones and other local pulse events, presenting a fundamental challenge to the long-term future of these iconic ecosystems. Acute heat stress from the extended marine heatwave of 2016 is a potent driver of the transformation of coral assemblages, which affects even the most remote and well-protected reefs of the Great Barrier Reef.

Many corals harbour symbiotic dinoflagellate algae. The algae live inside coral cells in a specialized membrane compartment known as the symbiosome, which shares the photosynthetically fixed carbon with coral host cells while host cells provide inorganic carbon to the algae for photosynthesis 1 . This endosymbiosis—which is critical for the maintenance of coral reef ecosystems—is increasingly threatened by environmental stressors that lead to coral bleaching (that is, the disruption of endosymbiosis), which in turn leads to coral death and the degradation of marine ecosystems 2 . The molecular pathways that orchestrate the recognition, uptake and maintenance of algae in coral cells remain poorly understood. Here we report the chromosome-level genome assembly of a Xenia species of fast-growing soft coral 3 , and use this species as a model to investigate coral–alga endosymbiosis. Single-cell RNA sequencing identified 16 cell clusters, including gastrodermal cells and cnidocytes, in Xenia sp. We identified the endosymbiotic cell type, which expresses a distinct set of genes that are implicated in the recognition, phagocytosis and/or endocytosis, and maintenance of algae, as well as in the immune modulation of host coral cells. By coupling Xenia sp. regeneration and single-cell RNA sequencing, we observed a dynamic lineage progression of the endosymbiotic cells. The conserved genes associated with endosymbiosis that are reported here may help to reveal common principles by which different corals take up or lose their endosymbionts. Single-cell RNA sequencing identifies the pattern of gene expression during lineage progression in endosymbiotic cells of the fast-growing soft coral Xenia , revealing principles that underlie uptake and maintenance of endosymbionts by this coral.

The health and condition of the world’s reefs are in steep decline. This has triggered the development of fledgling micro-scale coral reef restoration projects along many reef coastlines. However, it is increasingly recognised that the scale and productivity of micro-scale coral gardening projects will be insufficient to meet the growing global threats to reefs. More recently, efforts to develop and implement restoration techniques for application at regional scales have been pursued by research organisations. Coral reefs are mostly located in the unindustrialised world. Yet, most of the funding, and scientific and engineering method development for larger-scale methods will likely be sourced and created in the industrialised world. Therefore, the development of the emerging at-scale global reef restoration sector will inevitably involve the transfer of methods, approaches, finances, labour and skills from the industrialised world to the unindustrialised world. This opens the door to the industrialised world negatively impacting the unindustrialised world and, in some cases, First Nations peoples. In Western scientific parlance, ecological imperialism occurs when people from industrialised nations seek to recreate environments and ecosystems in unindustrialised nations that are familiar and comfortable to them. How a coral reef ’should’ look depends on one’s background and perspective. While predominately Western scientific approaches provide guidance on the ecological principles for reef restoration, these methods might not be applicable in every scenario in unindustrialised nations. Imposing such views on Indigenous coastal communities without the local technical and leadership resources to scale-up restoration of their reefs can lead to unwanted consequences. The objective of this paper is to introduce this real and emerging risk into the broader reef restoration discussion.

During 2015–2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs. Aerial and underwater survey data combined with satellite-derived measurements of sea surface temperature over the past two decades show that multiple mass-bleaching events have expanded to encompass virtually all of the Great Barrier Reef. Barrier reef bleaching The Great Barrier Reef is the world's largest reef system, but is being increasingly affected by climate change. Terry Hughes and colleagues examine changes in the geographic footprint of mass bleaching events on the Great Barrier Reef over the last two decades, using aerial and underwater survey data combined with satellite-derived measurements of sea surface temperature. They show that the cumulative footprint of multiple bleaching events has expanded to encompass virtually all of the Great Barrier Reef, reducing the number and size of potential refuges. The 2016 bleaching event proved the most severe, affecting 91% of individual reefs. The authors call for immediate global action to reduce the magnitude of climate warming in order to secure a future for coral reefs.

The tropics contain the overwhelming majority of Earth’s biodiversity: their terrestrial, freshwater and marine ecosystems hold more than three-quarters of all species, including almost all shallow-water corals and over 90% of terrestrial birds. However, tropical ecosystems are also subject to pervasive and interacting stressors, such as deforestation, overfishing and climate change, and they are set within a socio-economic context that includes growing pressure from an increasingly globalized world, larger and more affluent tropical populations, and weak governance and response capacities. Concerted local, national and international actions are urgently required to prevent a collapse of tropical biodiversity. The immense biodiversity of tropical ecosystems is threatened by multiple interacting local and global stressors that can only be addressed by the concerted efforts of grassroots organizations, researchers, national governments and the international community.

Abstract As coral reef ecosystems experience unprecedented change, effective monitoring of reef features supports management, conservation, and intervention efforts. Omic techniques show promise in quantifying key components of reef ecosystems including dissolved metabolites and microorganisms that may serve as invisible sensors for reef ecosystem dynamics. Dissolved metabolites are released by reef organisms and transferred among microorganisms, acting as chemical currencies and contributing to nutrient cycling and signaling on reefs. Here, we applied four omic techniques (taxonomic microbiome via amplicon sequencing, functional microbiome via shotgun metagenomics, targeted metabolomics, and untargeted metabolomics) to waters overlying Florida's Coral Reef, as well as microbiome profiling on individual coral colonies from these reefs to understand how microbes and dissolved metabolites reflect biogeographical, benthic, and nutrient properties of this 500-km barrier reef. We show that the microbial and metabolite omic approaches each differentiated reef habitats based on geographic zone. Further, seawater microbiome profiling and targeted metabolomics were significantly related to more reef habitat characteristics, such as amount of hard and soft coral, compared to metagenomic sequencing and untargeted metabolomics. Across five coral species, microbiomes were also significantly related to reef zone, followed by species and disease status, suggesting that the geographic water circulation patterns in Florida also impact the microbiomes of reef builders. A combination of differential abundance and indicator species analyses revealed metabolite and microbial signatures of specific reef zones, which demonstrates the utility of these techniques to provide new insights into reef microbial and metabolite features that reflect broader ecosystem processes.