Emergent properties in the responses of tropical corals to recurrent climate extremes.

The frequency, intensity, and spatial scale of climate extremes are changing rapidly due to anthropogenic global warming.1,2 A growing research challenge is to understand how multiple climate-driven disturbances interact with each other over multi-decadal time frames, generating combined effects that cannot be predicted from single events alone.3-5 Here we examine the emergent dynamics of five coral bleaching events along the 2,300 km length of the Great Barrier Reef that affected >98% of the Reef between 1998 and 2020. We show that the bleaching responses of corals to a given level of heat exposure differed in each event and were strongly influenced by contingency and the spatial overlap and strength of interactions between events. Naive regions that escaped bleaching for a decade or longer were the most susceptible to bouts of heat exposure. Conversely, when pairs of successive bleaching episodes were close together (1-3 years apart), the thermal threshold for severe bleaching increased because the earlier event hardened regions of the Great Barrier Reef to further impacts. In the near future, the biological responses to recurrent bleaching events may become stronger as the cumulative geographic footprint expands further, potentially impairing the stock-recruitment relationships among lightly and severely bleached reefs with diverse recent histories. Understanding the emergent properties and collective dynamics of recurrent disturbances will be critical for predicting spatial refuges and cumulative ecological responses, and for managing the longer-term impacts of anthropogenic climate change on ecosystems.

The spatial footprint and patchiness of large-scale disturbances on coral reefs.

Ecosystems have always been shaped by disturbances, but many of these events are becoming larger, more severe and more frequent. The recovery capacity of depleted populations depends on the frequency of disturbances, the spatial distribution of mortality and the scale of dispersal. Here, we show that four mass coral bleaching events on the Great Barrier Reef (in 1998, 2002, 2016 and 2017) each had markedly larger disturbance footprints and were less patchy than a severe category 5 tropical cyclone (Cyclone Yasi, 2011). Severely bleached reefs in 2016 and 2017 were isolated from the nearest lightly affected reefs by up to 146 and 200 km, respectively. In contrast, reefs damaged by Cyclone Yasi were on average 20 km away from relatively undisturbed reefs, well within the estimated range of larval dispersal for most corals. Based on these results, we present a model of coral reef disturbance and recovery to examine (1) how the spatial clustering of disturbances modifies large-scale recovery rates; and (2) how recovery rates are shaped by species' dispersal abilities. Our findings illustrate that the spatial footprint of the recent mass bleaching events poses an unprecedented threat to the resilience of coral species in human history, a threat that is even larger than the amount of mortality suggests.

The population sizes and global extinction risk of reef-building coral species at biogeographic scales.

Knowledge of a species' abundance is critically important for assessing its risk of extinction, but for the vast majority of wild animal and plant species such data are scarce at biogeographic scales. Here, we estimate the total number of reef-building corals and the population sizes of more than 300 individual species on reefs spanning the Pacific Ocean biodiversity gradient, from Indonesia to French Polynesia. Our analysis suggests that approximately half a trillion corals (0.3 × 1012-0.8 × 1012) inhabit these coral reefs, similar to the number of trees in the Amazon. Two-thirds of the examined species have population sizes exceeding 100 million colonies, and one-fifth of the species even have population sizes greater than 1 billion colonies. Our findings suggest that, while local depletions pose imminent threats that can have ecologically devastating impacts to coral reefs, the global extinction risk of most coral species is lower than previously estimated.

Long-term shifts in the colony size structure of coral populations along the Great Barrier Reef.

The age or size structure of a population has a marked influence on its demography and reproductive capacity. While declines in coral cover are well documented, concomitant shifts in the size-frequency distribution of coral colonies are rarely measured at large spatial scales. Here, we document major shifts in the colony size structure of coral populations along the 2300 km length of the Great Barrier Reef relative to historical baselines (1995/1996). Coral colony abundances on reef crests and slopes have declined sharply across all colony size classes and in all coral taxa compared to historical baselines. Declines were particularly pronounced in the northern and central regions of the Great Barrier Reef, following mass coral bleaching in 2016 and 2017. The relative abundances of large colonies remained relatively stable, but this apparent stability masks steep declines in absolute abundance. The potential for recovery of older fecund corals is uncertain given the increasing frequency and intensity of disturbance events. The systematic decline in smaller colonies across regions, habitats and taxa, suggests that a decline in recruitment has further eroded the recovery potential and resilience of coral populations.

Rebuilding marine life.

Sustainable Development Goal 14 of the United Nations aims to "conserve and sustainably use the oceans, seas and marine resources for sustainable development". Achieving this goal will require rebuilding the marine life-support systems that deliver the many benefits that society receives from a healthy ocean. Here we document the recovery of marine populations, habitats and ecosystems following past conservation interventions. Recovery rates across studies suggest that substantial recovery of the abundance, structure and function of marine life could be achieved by 2050, if major pressures-including climate change-are mitigated. Rebuilding marine life represents a doable Grand Challenge for humanity, an ethical obligation and a smart economic objective to achieve a sustainable future.

Deficits in functional trait diversity following recovery on coral reefs.

The disturbance regimes of ecosystems are changing, and prospects for continued recovery remain unclear. New assemblages with altered species composition may be deficient in key functional traits. Alternatively, important traits may be sustained by species that replace those in decline (response diversity). Here, we quantify the recovery and response diversity of coral assemblages using case studies of disturbance in three locations. Despite return trajectories of coral cover, the original assemblages with diverse functional attributes failed to recover at each location. Response diversity and the reassembly of trait space was limited, and varied according to biogeographic differences in the attributes of dominant, rapidly recovering species. The deficits in recovering assemblages identified here suggest that the return of coral cover cannot assure the reassembly of reef trait diversity, and that shortening intervals between disturbances can limit recovery among functionally important species.

Climate change, ecosystems and abrupt change: science priorities.

Ecologists have long studied patterns, directions and tempos of change, but there is a pressing need to extend current understanding to empirical observations of abrupt changes as climate warming accelerates. Abrupt changes in ecological systems (ACES)-changes that are fast in time or fast relative to their drivers-are ubiquitous and increasing in frequency. Powerful theoretical frameworks exist, yet applications in real-world landscapes to detect, explain and anticipate ACES have lagged. We highlight five insights emerging from empirical studies of ACES across diverse ecosystems: (i) ecological systems show ACES in some dimensions but not others; (ii) climate extremes may be more important than mean climate in generating ACES; (iii) interactions among multiple drivers often produce ACES; (iv) contingencies, such as ecological memory, frequency and sequence of disturbances, and spatial context are important; and (v) tipping points are often (but not always) associated with ACES. We suggest research priorities to advance understanding of ACES in the face of climate change. Progress in understanding ACES requires strong integration of scientific approaches (theory, observations, experiments and process-based models) and high-quality empirical data drawn from a diverse array of ecosystems. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Global warming impairs stock-recruitment dynamics of corals.

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 assemblages1-3. 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 pressures4,5. 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 stress6, 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 decades7.

Global warming transforms coral reef assemblages.

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.

Biogeographical disparity in the functional diversity and redundancy of corals.

Corals are major contributors to a range of key ecosystem functions on tropical reefs, including calcification, photosynthesis, nutrient cycling, and the provision of habitat structure. The abundance of corals is declining at multiple scales, and the species composition of assemblages is responding to escalating human pressures, including anthropogenic global warming. An urgent challenge is to understand the functional consequences of these shifts in abundance and composition in different biogeographical contexts. While global patterns of coral species richness are well known, the biogeography of coral functions in provinces and domains with high and low redundancy is poorly understood. Here, we quantify the functional traits of all currently recognized zooxanthellate coral species (n = 821) in both the Indo-Pacific and Atlantic domains to examine the relationships between species richness and the diversity and redundancy of functional trait space. We find that trait diversity is remarkably conserved (>75% of the global total) along latitudinal and longitudinal gradients in species richness, falling away only in species-poor provinces (n < 200), such as the Persian Gulf (52% of the global total), Hawaii (37%), the Caribbean (26%), and the East-Pacific (20%), where redundancy is also diminished. In the more species-poor provinces, large and ecologically important areas of trait space are empty, or occupied by just a few, highly distinctive species. These striking biogeographical differences in redundancy could affect the resilience of critical reef functions and highlight the vulnerability of relatively depauperate, peripheral locations, which are often a low priority for targeted conservation efforts.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño-Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.

Coral reefs in the Anthropocene.

Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.

A unified model explains commonness and rarity on coral reefs.

Abundance patterns in ecological communities have important implications for biodiversity maintenance and ecosystem functioning. However, ecological theory has been largely unsuccessful at capturing multiple macroecological abundance patterns simultaneously. Here, we propose a parsimonious model that unifies widespread ecological relationships involving local aggregation, species-abundance distributions, and species associations, and we test this model against the metacommunity structure of reef-building corals and coral reef fishes across the western and central Pacific. For both corals and fishes, the unified model simultaneously captures extremely well local species-abundance distributions, interspecific variation in the strength of spatial aggregation, patterns of community similarity, species accumulation, and regional species richness, performing far better than alternative models also examined here and in previous work on coral reefs. Our approach contributes to the development of synthetic theory for large-scale patterns of community structure in nature, and to addressing ongoing challenges in biodiversity conservation at macroecological scales.

Global warming and recurrent mass bleaching of corals.

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.

China's Degraded Environment Enters A New Normal.

China is undergoing unprecedented social and ecological shifts, a harbinger of similar changes that will unfold in developing nations over coming decades. Many of China's degraded environments represent a new normal. Acknowledging this reality will allow societies to make informed decisions that recognize the undervalued costs of environment degradation.