Research priorities for the sustainability of coral-rich western Pacific seascapes.

Nearly a billion people depend on tropical seascapes. The need to ensure sustainable use of these vital areas is recognised, as one of 17 policy commitments made by world leaders, in Sustainable Development Goal (SDG) 14 ('Life below Water') of the United Nations. SDG 14 seeks to secure marine sustainability by 2030. In a time of increasing social-ecological unpredictability and risk, scientists and policymakers working towards SDG 14 in the Asia-Pacific region need to know: (1) How are seascapes changing? (2) What can global society do about these changes? and (3) How can science and society together achieve sustainable seascape futures? Through a horizon scan, we identified nine emerging research priorities that clarify potential research contributions to marine sustainability in locations with high coral reef abundance. They include research on seascape geological and biological evolution and adaptation; elucidating drivers and mechanisms of change; understanding how seascape functions and services are produced, and how people depend on them; costs, benefits, and trade-offs to people in changing seascapes; improving seascape technologies and practices; learning to govern and manage seascapes for all; sustainable use, justice, and human well-being; bridging communities and epistemologies for innovative, equitable, and scale-crossing solutions; and informing resilient seascape futures through modelling and synthesis. Researchers can contribute to the sustainability of tropical seascapes by co-developing transdisciplinary understandings of people and ecosystems, emphasising the importance of equity and justice, and improving knowledge of key cross-scale and cross-level processes, feedbacks, and thresholds.

Intraspecific variation reshapes coral assemblages under elevated temperature and acidity.

Insights into assemblages that can persist in extreme environments are still emerging. Ocean warming and acidification select against species with low physiological tolerance (trait-based 'filtering'). However, intraspecific trait variation can promote species adaptation and persistence, with potentially large effects on assemblage structure. By sampling nine coral traits (four morphological, four tissue and one skeletal) along an offshore-inshore gradient in temperature and pH, we show that distantly related coral species undergo consistent intraspecific changes as they cross into warm, acidic environments. Intraspecific variation and species turnover each favoured colonies with greater tissue biomass, higher symbiont densities and reduced skeletal investments, indicating strong filtering on colony physiology within and across species. Physiological tissue traits were highly variable within species and were independent of morphology, enabling morphologically diverse species to cross into sites of elevated temperature and acidity. Widespread intraspecific change can therefore counter the loss of biodiversity and morphological structure across a steep environmental gradient.

Coral adaptation to climate change: Meta-analysis reveals high heritability across multiple traits.

Anthropogenic climate change is a rapidly intensifying selection pressure on biodiversity across the globe and, particularly, on the world's coral reefs. The rate of adaptation to climate change is proportional to the amount of phenotypic variation that can be inherited by subsequent generations (i.e., narrow-sense heritability, h2 ). Thus, traits that have higher heritability (e.g., h2  > 0.5) are likely to adapt to future conditions faster than traits with lower heritability (e.g., h2  < 0.1). Here, we synthesize 95 heritability estimates across 19 species of reef-building corals. Our meta-analysis reveals low heritability (h2 < 0.25) of gene expression metrics, intermediate heritability (h2  = 0.25-0.50) of photochemistry, growth, and bleaching, and high heritability (h2  > 0.50) for metrics related to survival and immune responses. Some of these values are higher than typically observed in other taxa, such as survival and growth, while others were more comparable, such as gene expression and photochemistry. There was no detectable effect of temperature on heritability, but narrow-sense heritability estimates were generally lower than broad-sense estimates, indicative of significant non-additive genetic variation across traits. Trait heritability also varied depending on coral life stage, with bleaching and growth in juveniles generally having lower heritability compared to bleaching and growth in larvae and adults. These differences may be the result of previous stabilizing selection on juveniles or may be due to constrained evolution resulting from genetic trade-offs or genetic correlations between growth and thermotolerance. While we find no evidence that heritability decreases under temperature stress, explicit tests of the heritability of thermal tolerance itself-such as coral thermal reaction norm shape-are lacking. Nevertheless, our findings overall reveal high trait heritability for the majority of coral traits, suggesting corals may have a greater potential to adapt to climate change than has been assumed in recent evolutionary models.

Climate change doubles sedimentation-induced coral recruit mortality.

Coral reef replenishment is threatened by global climate change and local water-quality degradation, including smothering of coral recruits by sediments generated by anthropogenic activities. Here we show that the ability of Acropora millepora recruits to remove sediments diminishes under future climate conditions, leading to increased mortality. Recruits raised under future climate scenarios for fourteen weeks (highest treatment: +1.2 °C, pCO2: 950 ppm) showed twofold higher mortality following repeated sediment deposition (50% lethal sediment concentration LC50: 14-24 mg cm-2) compared to recruits raised under current climate conditions (LC50: 37-51 mg cm-2), depending on recruit age at the time of sedimentation. Older and larger recruits were more resistant to sedimentation and only ten-week-old recruits grown under current climate conditions survived sediment loads possible during dredging operations. This demonstrates that water-quality guidelines for managing sediment concentrations will need to be climate-adjusted to protect future coral recruitment.

A geometric basis for surface habitat complexity and biodiversity.

Structurally complex habitats tend to contain more species and higher total abundances than simple habitats. This ecological paradigm is grounded in first principles: species richness scales with area, and surface area and niche density increase with three-dimensional complexity. Here we present a geometric basis for surface habitats that unifies ecosystems and spatial scales. The theory is framed by fundamental geometric constraints between three structure descriptors-surface height, rugosity and fractal dimension-and explains 98% of surface variation in a structurally complex test system: coral reefs. Then, we show how coral biodiversity metrics (species richness, total abundance and probability of interspecific encounter) vary over the theoretical structure descriptor plane, demonstrating the value of the theory for predicting the consequences of natural and human modifications of surface structure.

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.

Impacts of microplastics on growth and health of hermatypic corals are species-specific.

Coral reefs are increasingly affected by the consequences of global change such as increasing temperatures or pollution. Lately, microplastics (i.e., fragments < 5 mm) have been identified as another potential threat. While previous studies have assessed short-term effects caused by high concentrations of microplastics, nothing is known about the long-term effects of microplastics under realistic concentrations. Therefore, a microcosm study was conducted and corals of the genera Acropora, Pocillopora, Porites, and Heliopora were exposed to microplastics in a concentration of 200 particles L-1, relating to predicted pollution levels. Coral growth and health, as well as symbiont properties were studied over a period of six months. The exposure caused species-specific effects on coral growth and photosynthetic performance. Signs of compromised health were observed for Acropora and Pocillopora, those taxa that frequently interact with the particles. The results indicate elevated energy demands in the affected species, likely due to physical contact of the corals to the microplastics. The study shows that microplastic pollution can have negative impacts on hermatypic corals. These effects might amplify corals' susceptibility to other stressors, further contributing to community shifts in coral reef assemblages.

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.

Neighbor Diversity Regulates the Productivity of Coral Assemblages.

Sustaining ecological functions as biodiversity changes will be a major challenge in the 21st century [1]. However, our understanding of the relationship between biodiversity and ecosystem function is still emerging on tropical coral reefs [2], where reef-building corals form highly productive assemblages [3, 4] and species respond in different ways to their neighbors [5] and their environment (e.g., water flow) [6]. Experimental coral communities were assembled to quantify the performance of coral colonies with and without neighbors and in the presence of conspecifics versus heterospecifics. Under higher flow, we identified a positive effect of coral species richness on primary productivity (gross and net photosynthesis) indicated by a 53% increase in productivity in multispecies assemblages (2-4 species) relative to monocultures. Productivity in monocultures was predicted by surface areas associated with different species morphologies. In contrast, multispecies assemblages maintained high levels of productivity even in the absence of the most productive species, reflecting non-additive effects of species richness on community functioning. Assemblage performances were regulated by positive and negative interactions between colonies, with many colonies performing better among heterospecific neighbors than in isolation (facilitation). Facilitation occurred primarily among flow-sensitive taxa with simple morphologies and did not occur under lower flow, suggesting that modifications to flow microclimates by corals generated beneficial, interspecific interactions. Our results show that competition and facilitation among neighbors may be important mechanisms regulating coral assemblage productivity in variable environments. Furthermore, shifts in the diversity and identity of neighbors can impair these interactions, with potentially widespread consequences for coral community functioning.

The bioeroding sponge Cliona orientalis will not tolerate future projected ocean warming.

Coral reefs face many stressors associated with global climate change, including increasing sea surface temperature and ocean acidification. Excavating sponges, such as Cliona spp., are expected to break down reef substrata more quickly as seawater becomes more acidic. However, increased bioerosion requires that Cliona spp. maintain physiological performance and health under continuing ocean warming. In this study, we exposed C. orientalis to temperature increments increasing from 23 to 32 °C. At 32 °C, or 3 °C above the maximum monthly mean (MMM) temperature, sponges bleached and the photosynthetic capacity of Symbiodinium was compromised, consistent with sympatric corals. Cliona orientalis demonstrated little capacity to recover from thermal stress, remaining bleached with reduced Symbiodinium density and energy reserves after one month at reduced temperature. In comparison, C. orientalis was not observed to bleach during the 2017 coral bleaching event on the Great Barrier Reef, when temperatures did not reach the 32 °C threshold. While C. orientalis can withstand current temperature extremes (<3 °C above MMM) under laboratory and natural conditions, this species would not survive ocean temperatures projected for 2100 without acclimatisation or adaptation (≥3 °C above MMM). Hence, as ocean temperatures increase above local thermal thresholds, C. orientalis will have a negligible impact on reef erosion.

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.

Effects of microplastic exposure on the body condition and behaviour of planktivorous reef fish (Acanthochromis polyacanthus).

The effect of a pollutant on the base of the food web can have knock-on effects for trophic structure and ecosystem functioning. In this study we assess the effect of microplastic exposure on juveniles of a planktivorous fish (Acanthochromis polyacanthus), a species that is widespread and abundant on Indo-Pacific coral reefs. Under five different plastic concentration treatments, with plastics the same size as the natural food particles (mean 2mm diameter), there was no significant effect of plastic exposure on fish growth, body condition or behaviour. The amount of plastics found in the gastro-intestinal (GI) tract was low, with a range of one to eight particles remaining in the gut of individual fish at the end of a 6-week plastic-exposure period, suggesting that these fish are able to detect and avoid ingesting microplastics in this size range. However, in a second experiment the number of plastics in the GI tract vastly increased when plastic particle size was reduced to approximately one quarter the size of the food particles, with a maximum of 2102 small (< 300µm diameter) particles present in the gut of individual fish after a 1-week plastic exposure period. Under conditions where food was replaced by plastic, there was a negative effect on the growth and body condition of the fish. These results suggest plastics could become more of a problem as they break up into smaller size classes, and that environmental changes that lead to a decrease in plankton concentrations combined with microplastic presence is likely have a greater influence on fish populations than microplastic presence alone.

Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge.

Bioeroding sponges break down calcium carbonate substratum, including coral skeleton, and their capacity for reef erosion is expected to increase in warmer and more acidic oceans. However, elevated temperature can disrupt the functionally important microbial symbionts of some sponge species, often with adverse consequences for host health. Here, we provide the first detailed description of the microbial community of the bioeroding sponge Cliona orientalis and assess how the community responds to seawater temperatures incrementally increasing from 23°C to 32°C. The microbiome, identified using 16S rRNA gene sequencing, was dominated by Alphaproteobacteria, including a single operational taxonomic unit (OTU; Rhodothalassium sp.) that represented 21% of all sequences. The "core" microbial community (taxa present in >80% of samples) included putative nitrogen fixers and ammonia oxidizers, suggesting that symbiotic nitrogen metabolism may be a key function of the C. orientalis holobiont. The C. orientalis microbiome was generally stable at temperatures up to 27°C; however, a community shift occurred at 29°C, including changes in the relative abundance and turnover of microbial OTUs. Notably, this microbial shift occurred at a lower temperature than the 32°C threshold that induced sponge bleaching, indicating that changes in the microbiome may play a role in the destabilization of the C. orientalis holobiont. C. orientalis failed to regain Symbiodinium or restore its baseline microbial community following bleaching, suggesting that the sponge has limited ability to recover from extreme thermal exposure, at least under aquarium conditions.

Corrigendum: The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

This corrects the article DOI: 10.1038/sdata.2016.17.

Cyphastrea salae, a new species of hard coral from Lord Howe Island, Australia (Scleractinia, Merulinidae).

A new zooxanthellate reef-dwelling scleractinian coral species, Cyphastrea salaesp. n. (Scleractinia, Merulinidae), is described from Lord Howe Island Australia. The new species can be distinguished morphologically from the only other congeneric species on Lord Howe Island, C. microphthalma, by the number of primary septa (12 vs. 10) and the much taller corallites (mean ± SE: 1.0 ± 0.07 mm v 0.4 ± 0.04 mm). The relationship of C. salae to four of the other eleven currently accepted species in the genus was explored through analyses of nuclear (28S rDNA) and mitochondrial (noncoding intergenic region) gene sequences. Cyphastrea salaesp. n. forms a strongly supported clade that is distinct from a clade containing three species found commonly in Australia, C. chalcidicum, C. serailia, and C. microphthalma. One specimen was also found in the Solitary Islands, another high latitude location in south-eastern Australia. The discovery of a new species in the genus Cyphastrea on high latitude reefs in south-eastern Australia suggests that other new species might be found among more diverse genera represented here and that the scleractinian fauna of these isolated locations is more distinct than previously recognised.

A decadal analysis of bioeroding sponge cover on the inshore Great Barrier Reef.

Decreasing coral cover on the Great Barrier Reef (GBR) may provide opportunities for rapid growth and expansion of other taxa. The bioeroding sponges Cliona spp. are strong competitors for space and may take advantage of coral bleaching, damage, and mortality. Benthic surveys of the inshore GBR (2005-2014) revealed that the percent cover of the most abundant bioeroding sponge species, Cliona orientalis, has not increased. However, considerable variation in C. orientalis cover, and change in cover over time, was evident between survey locations. We assessed whether biotic or environmental characteristics were associated with variation in C. orientalis distribution and abundance. The proportion of fine particles in the sediments was negatively associated with the presence-absence and the percent cover of C. orientalis, indicating that the sponge requires exposed habitat. The cover of corals and other sponges explained little variation in C. orientalis cover or distribution. The fastest increases in C. orientalis cover coincided with the lowest macroalgal cover and chlorophyll a concentration, highlighting the importance of macroalgal competition and local environmental conditions for this bioeroding sponge. Given the observed distribution and habitat preferences of C. orientalis, bioeroding sponges likely represent site-specific - rather than regional - threats to corals and reef accretion.

Effects of coal contamination on early life history processes of a reef-building coral, Acropora tenuis.

Successful reproduction and larval dispersal are important for the persistence of marine invertebrate populations, and these early life history processes can be sensitive to marine pollution. Coal is emerging as a contaminant of interest due to the proximity of ports and shipping lanes to coral reefs. To assess the potential hazard of this contaminant, gametes, newly developed embryos, larvae and juveniles of the coral Acropora tenuis were exposed to a range of coal leachate, suspended coal, and coal smothering treatments. Fertilisation was the most sensitive reproductive process tested. Embryo survivorship decreased with increasing suspended coal concentrations and exposure duration, effects on larval settlement varied between treatments, while effects on juvenile survivorship were minimal. Leachate exposures had negligible effects on fertilisation and larval settlement. These results indicate that coral recruitment could be affected by spills that produce plumes of suspended coal particles which interact with gametes and embryos soon after spawning.

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.

Spatial competition dynamics between reef corals under ocean acidification.

Climate change, including ocean acidification (OA), represents a major threat to coral-reef ecosystems. Although previous experiments have shown that OA can negatively affect the fitness of reef corals, these have not included the long-term effects of competition for space on coral growth rates. Our multispecies year-long study subjected reef-building corals from the Gulf of Aqaba (Red Sea) to competitive interactions under present-day ocean pH (pH 8.1) and predicted end-of-century ocean pH (pH 7.6). Results showed coral growth is significantly impeded by OA under intraspecific competition for five out of six study species. Reduced growth from OA, however, is negligible when growth is already suppressed in the presence of interspecific competition. Using a spatial competition model, our analysis indicates shifts in the competitive hierarchy and a decrease in overall coral cover under lowered pH. Collectively, our case study demonstrates how modified competitive performance under increasing OA will in all likelihood change the composition, structure and functionality of reef coral communities.