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.

Shifting paradigms in restoration of the world's coral reefs.

Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine-protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014-2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.

Cumulative risk of future bleaching for the world's coral reefs.

Spatial and temporal patterns of future coral bleaching are uncertain, hampering global conservation efforts to protect coral reefs against climate change. Our analysis of daily projections of ocean warming establishes the severity, annual duration, and onset of severe bleaching risk for global coral reefs this century, pinpointing vital climatic refugia. We show that low-latitude coral regions are most vulnerable to thermal stress and will experience little reprieve from climate mitigation. By 2080, coral bleaching is likely to start on most reefs in spring, rather than late summer, with year-round bleaching risk anticipated to be high for some low-latitude reefs regardless of global efforts to mitigate harmful greenhouse gasses. By identifying Earth's reef regions that are at lowest risk of accelerated bleaching, our results will prioritize efforts to limit future loss of coral reef biodiversity.

Colocalization and potential interactions of Endozoicomonas and chlamydiae in microbial aggregates of the coral Pocillopora acuta.

Corals are associated with a variety of bacteria, which occur in the surface mucus layer, gastrovascular cavity, skeleton, and tissues. Some tissue-associated bacteria form clusters, termed cell-associated microbial aggregates (CAMAs), which are poorly studied. Here, we provide a comprehensive characterization of CAMAs in the coral Pocillopora acuta. Combining imaging techniques, laser capture microdissection, and amplicon and metagenome sequencing, we show that (i) CAMAs are located in the tentacle tips and may be intracellular; (ii) CAMAs contain Endozoicomonas (Gammaproteobacteria) and Simkania (Chlamydiota) bacteria; (iii) Endozoicomonas may provide vitamins to its host and use secretion systems and/or pili for colonization and aggregation; (iv) Endozoicomonas and Simkania occur in distinct, but adjacent, CAMAs; and (v) Simkania may receive acetate and heme from neighboring Endozoicomonas. Our study provides detailed insight into coral endosymbionts, thereby improving our understanding of coral physiology and health and providing important knowledge for coral reef conservation in the climate change era.

Assessing multiproxy approaches (Sr/Ca, U/Ca, Li/Mg, and B/Mg) to reconstruct sea surface temperature from coral skeletons throughout the Great Barrier Reef.

Due to the increasing concerns of global warming and short instrumental records of sea surface temperature (SST), coral-based proxies, such as δ18O, Sr/Ca, U/Ca, and Li/Mg have been developed and applied to reconstruct SST in paleoclimate studies. However, these proxies are not universally applicable in different environments, because they are affected by coral physiology and various environmental factors. In this study, seven long-lived Porites corals were collected from the southern sector of the Great Barrier Reef (GBR) off the coast of Gladstone and the central sector of the GBR within the Whitsunday Islands in 2017 and 2018. Coral sites were selected to cover a wide latitudinal range with different annual temperature ranges. Century-long geochemical records (Li/Ca, B/Ca, Mg/Ca, Sr/Ca, and U/Ca) were generated using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) at weekly resolution. This study has tested the robustness of two traditional temperature proxies (Sr/Ca and U/Ca), a recently developed temperature proxy (Li/Mg), and an additional potential temperature proxy (B/Mg). U/Ca was found to be the most robust and stable temperature proxy for corals from the GBR over long-term timescales. Sr/Ca is a close second, however due to the lower response of Sr fractionation per 1 °C, it is more sensitive to analytical methods and less sensitive to annual SST changes than U/Ca. Li/Mg and B/Mg have clearer periodicity compared to Li/Ca and B/Ca. Both Li/Mg and B/Mg are strongly correlated with SST, which is due to the cancellation of temperature-independent commonality. Empirical calibrations established from this multi-proxy approach increase the certainty of temperature reconstruction when a single proxy does not perform well. These site- and colony-specific SST calibrations also provide an opportunity to revisit the universal multi-trace element calibration of sea surface temperatures (UMTECS) model, which does not require the knowledge of local SST for calibration.

The effect of natural and anthropogenic nutrient and sediment loads on coral oxidative stress on runoff-exposed reefs.

Recently, corals on the Great Barrier (GBR) have suffered mass bleaching. The link between ocean warming and coral bleaching is understood to be due to temperature-dependence of complex physiological processes in the coral host and algal symbiont. Here we use a coupled catchment-hydrodynamic-biogeochemical model, with detailed zooxanthellae photophysiology including photoadaptation, photoacclimation and reactive oxygen build-up, to investigate whether natural and anthropogenic catchment loads impact on coral bleaching on the GBR. For the wet season of 2017, simulations show the cross-shelf water quality gradient, driven by both natural and anthropogenic loads, generated a contrasting zooxanthellae physiological state on inshore versus mid-shelf reefs. The relatively small catchment flows and loads delivered during 2017, however, generated small river plumes with limited impact on water quality. Simulations show the removal of the anthropogenic fraction of the catchment loads delivered in 2017 would have had a negligible impact on bleaching rates.

Population genetics of the coral Acropora millepora: Toward genomic prediction of bleaching.

Although reef-building corals are declining worldwide, responses to bleaching vary within and across species and are partly heritable. Toward predicting bleaching response from genomic data, we generated a chromosome-scale genome assembly for the coral Acropora millepora We obtained whole-genome sequences for 237 phenotyped samples collected at 12 reefs along the Great Barrier Reef, among which we inferred little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin We conducted a genome-wide association study of visual bleaching score for 213 samples, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for genomics-based approaches in conservation strategies.

Temporal Variation in the Microbiome of Acropora Coral Species Does Not Reflect Seasonality.

The coral microbiome is known to fluctuate in response to environmental variation and has been suggested to vary seasonally. However, most studies to date, particularly studies on bacterial communities, have examined temporal variation over a time frame of less than 1 year, which is insufficient to establish if microbiome variations are indeed seasonal in nature. The present study focused on expanding our understanding of long-term variability in microbial community composition using two common coral species, Acropora hyacinthus, and Acropora spathulata, at two mid-shelf reefs on the Great Barrier Reef. By sampling over a 2-year time period, this study aimed to determine whether temporal variations reflect seasonal cycles. Community composition of both bacteria and Symbiodiniaceae was characterized through 16S rRNA gene and ITS2 rDNA metabarcoding. We observed significant variations in community composition of both bacteria and Symbiodiniaceae among time points for A. hyacinthus and A. spathulata. However, there was no evidence to suggest that temporal variations were cyclical in nature and represented seasonal variation. Clear evidence for differences in the microbial communities found between reefs suggests that reef location and coral species play a larger role than season in driving microbial community composition in corals. In order to identify the basis of temporal patterns in coral microbial community composition, future studies should employ longer time series of sampling at sufficient temporal resolution to identify the environmental correlates of microbiome variation.

Variation in growth rates of branching corals along Australia's Great Barrier Reef.

Coral growth is an important component of reef health and resilience. However, few studies have investigated temporal and/or spatial variation in growth of branching corals, which are important contributors to the structure and function of reef habitats. This study assessed growth (linear extension, density, and calcification) of three branching coral species (Acropora muricata, Pocillopora damicornis and Isopora palifera) at three distinct locations (Lizard Island, Davies/Trunk Reef, and Heron Island) along Australia's Great Barrier Reef (GBR). Annual growth rates of all species were highest at Lizard Island and declined with increasing latitude, corresponding with differences in temperature. Within locations, however, seasonal variation in growth did not directly correlate with temperature. Between October 2012 and October 2014, the highest growth of A. muricata was in the 2013-14 summer at Lizard Island, which was unusually cool and ~0.5 °C less than the long-term summer average temperature. At locations where temperatures reached or exceeded the long-term summer maxima, coral growth during summer periods was equal to, if not lower than, winter periods. This study shows that temperature has a significant influence on spatiotemporal patterns of branching coral growth, and high summer temperatures in the northern GBR may already be constraining coral growth and reef resilience.

Surviving coral bleaching events: porites growth anomalies on the Great Barrier Reef.

Mass coral bleaching affected large parts of the Great Barrier Reef (GBR) in 1998 and 2002. In this study, we assessed if signatures of these major thermal stress events were recorded in the growth characteristics of massive Porites colonies. In 2005 a suite of short (<50 cm) cores were collected from apparently healthy, surviving Porites colonies, from reefs in the central GBR (18-19°S) that have documented observations of widespread bleaching. Sites included inshore (Nelly Bay, Pandora Reef), annually affected by freshwater flood events, midshelf (Rib Reef), only occasionally affected by freshwater floods and offshore (Myrmidon Reef) locations primarily exposed to open ocean conditions. Annual growth characteristics (extension, density and calcification) were measured in 144 cores from 79 coral colonies and analysed over the common 24-year period, 1980-2003. Visual examination of the annual density bands revealed growth hiatuses associated with the bleaching years in the form of abrupt decreases in annual linear extension rates, high density stress bands and partial mortality. The 1998 mass-bleaching event reduced Porites calcification by 13 and 18% on the two inshore locations for 4 years, followed by recovery to baseline calcification rates in 2002. Evidence of partial mortality was apparent in 10% of the offshore colonies in 2002; however no significant effects of the bleaching events were evident in the calcification rates at the mid shelf and offshore sites. These results highlight the spatial variation of mass bleaching events and that all reef locations within the GBR were not equally stressed by the 1998 and 2002 mass bleaching events, as some models tend to suggest, which enabled recovery of calcification on the GBR within 4 years. The dynamics in annual calcification rates and recovery displayed here should be used to improve model outputs that project how coral calcification will respond to ongoing warming of the tropical oceans.

Perspectives on massive coral growth rates in a changing ocean.

The tropical ocean environment is changing at an unprecedented rate, with warming and severe tropical cyclones creating obvious impacts to coral reefs within the last few decades and projections of acidification raising concerns for the future of these iconic and economically important ecosystems. Documenting variability and detecting change in global and regional climate relies upon high-quality observational records of climate variables supplemented, prior to the mid-19th century, with reconstructions from various sources of proxy climate information. Here we review how annual density banding patterns that are recorded in the skeletons of massive reef-building corals have been used to document environmental change and impacts within coral reefs. Massive corals provide a historical perspective of continuous calcification processes that pre-date most ecological observations of coral reefs. High-density stress bands, abrupt declines in annual linear extension, and evidence of partial mortality within the skeletal growth record reveal signatures of catastrophic stress events that have recently been attributed to mass bleaching events caused by unprecedented thermal stress. Comparison of recent trends in annual calcification with century-scale baseline calcification rates reveals that the frequency of growth anomalies has increased since the late 1990s throughout most of the world's coral reef ecosystems. Continuous coral growth histories provide valuable retrospective information on the coral response to environmental change and the consequences of anthropogenic climate change. Co-ordinated efforts to synthesize and combine global calcification histories will greatly enhance our understanding of current calcification responses to a changing ocean.

Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci.

Coral reefs are marine biodiversity hotspots, but their existence is threatened by global change and local pressures such as land-runoff and overfishing. Population explosions of coral-eating crown of thorns sea stars (COTS) are a major contributor to recent decline in coral cover on the Great Barrier Reef. Here, we investigate how projected near-future ocean acidification (OA) conditions can affect early life history stages of COTS, by investigating important milestones including sperm motility, fertilisation rates, and larval development and settlement. OA (increased pCO2 to 900-1200 µatm pCO2) significantly reduced sperm motility and, to a lesser extent, velocity, which strongly reduced fertilization rates at environmentally relevant sperm concentrations. Normal development of 10 d old larvae was significantly lower under elevated pCO2 but larval size was not significantly different between treatments. Settlement of COTS larvae was significantly reduced on crustose coralline algae (known settlement inducers of COTS) that had been exposed to OA conditions for 85 d prior to settlement assays. Effect size analyses illustrated that reduced settlement may be the largest bottleneck for overall juvenile production. Results indicate that reductions in fertilisation and settlement success alone would reduce COTS population replenishment by over 50%. However, it is unlikely that this effect is sufficient to provide respite for corals from other negative anthropogenic impacts and direct stress from OA and warming on corals.

Ocean warming slows coral growth in the central Red Sea.

Sea surface temperature (SST) across much of the tropics has increased by 0.4 degrees to 1 degrees C since the mid-1970s. A parallel increase in the frequency and extent of coral bleaching and mortality has fueled concern that climate change poses a major threat to the survival of coral reef ecosystems worldwide. Here we show that steadily rising SSTs, not ocean acidification, are already driving dramatic changes in the growth of an important reef-building coral in the central Red Sea. Three-dimensional computed tomography analyses of the massive coral Diploastrea heliopora reveal that skeletal growth of apparently healthy colonies has declined by 30% since 1998. The same corals responded to a short-lived warm event in 1941/1942, but recovered within 3 years as the ocean cooled. Combining our data with climate model simulations by the Intergovernmental Panel on Climate Change, we predict that should the current warming trend continue, this coral could cease growing altogether by 2070.