Tom C. L. Bridge

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.

The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts.

Despite being one of the simplest metazoans, corals harbor some of the most highly diverse and abundant microbial communities. Differentiating core, symbiotic bacteria from this diverse host-associated consortium is essential for characterizing the functional contributions of bacteria but has not been possible yet. Here we characterize the coral core microbiome and demonstrate clear phylogenetic and functional divisions between the micro-scale, niche habitats within the coral host. In doing so, we discover seven distinct bacterial phylotypes that are universal to the core microbiome of coral species, separated by thousands of kilometres of oceans. The two most abundant phylotypes are co-localized specifically with the corals’ endosymbiotic algae and symbiont-containing host cells. These bacterial symbioses likely facilitate the success of the dinoflagellate endosymbiosis with corals in diverse environmental regimes.

The broad footprint of climate change from genes to biomes to people

Accumulating impacts Anthropogenic climate change is now in full swing, our global average temperature already having increased by 1°C from preindustrial levels. Many studies have documented individual impacts of the changing climate that are particular to species or regions, but individual impacts are accumulating and being amplified more broadly. Scheffers et al. review the set of impacts that have been observed across genes, species, and ecosystems to reveal a world already undergoing substantial change. Understanding the causes, consequences, and potential mitigation of these changes will be essential as we move forward into a warming world. Science, this issue p. 10.1126/science.aaf7671 BACKGROUND Climate change impacts have now been documented across every ecosystem on Earth, despite an average warming of only ~1°C so far. Here, we describe the full range and scale of climate change effects on global biodiversity that have been observed in natural systems. To do this, we identify a set of core ecological processes (32 in terrestrial and 31 each in marine and freshwater ecosystems) that underpin ecosystem functioning and support services to people. Of the 94 processes considered, 82% show evidence of impact from climate change in the peer-reviewed literature. Examples of observed impacts from meta-analyses and case studies go beyond well-established shifts in species ranges and changes to phenology and population dynamics to include disruptions that scale from the gene to the ecosystem. ADVANCES Species are undergoing evolutionary adaptation to temperature extremes, and climate change has substantial impacts on species physiology that include changes in tolerances to high temperatures, shifts in sex ratios in species with temperature-dependent sex determination, and increased metabolic costs of living in a warmer world. These physiological adjustments have observable impacts on morphology, with many species in both aquatic and terrestrial systems shrinking in body size because large surface-to-volume ratios are generally favored under warmer conditions. Other morphological changes include reductions in melanism to improve thermoregulation, and altered wing and bill length in birds. Broader-scale responses to climate change include changes in the phenology, abundance, and distribution of species. Temperate plants are budding and flowering earlier in spring and later in autumn. Comparable adjustments have been observed in marine and freshwater fish spawning events and in the timing of seasonal migrations of animals worldwide. Changes in the abundance and age structure of populations have also been observed, with widespread evidence of range expansion in warm-adapted species and range contraction in cold-adapted species. As a by-product of species redistributions, novel community interactions have emerged. Tropical and boreal species are increasingly incorporated into temperate and polar communities, respectively, and when possible, lowland species are increasingly assimilating into mountain communities. Multiplicative impacts from gene to community levels scale up to produce ecological regime shifts, in which one ecosystem state shifts to an alternative state. OUTLOOK The many observed impacts of climate change at different levels of biological organization point toward an increasingly unpredictable future for humans. Reduced genetic diversity in crops, inconsistent crop yields, decreased productivity in fisheries from reduced body size, and decreased fruit yields from fewer winter chill events threaten food security. Changes in the distribution of disease vectors alongside the emergence of novel pathogens and pests are a direct threat to human health as well as to crops, timber, and livestock resources. Humanity depends on intact, functioning ecosystems for a range of goods and services. Enhanced understanding of the observed impacts of climate change on core ecological processes is an essential first step to adapting to them and mitigating their influence on biodiversity and ecosystem service provision. Climate change impacts on ecological processes in marine, freshwater, and terrestrial ecosystems. Impacts can be measured on multiple processes at different levels of biological organization within ecosystems. In total, 82% of 94 ecological processes show evidence of being affected by climate change. Within levels of organization, the percentage of processes impacted varies from 60% for genetics to 100% for species distribution. Most ecological processes now show responses to anthropogenic climate change. In terrestrial, freshwater, and marine ecosystems, species are changing genetically, physiologically, morphologically, and phenologically and are shifting their distributions, which affects food webs and results in new interactions. Disruptions scale from the gene to the ecosystem and have documented consequences for people, including unpredictable fisheries and crop yields, loss of genetic diversity in wild crop varieties, and increasing impacts of pests and diseases. In addition to the more easily observed changes, such as shifts in flowering phenology, we argue that many hidden dynamics, such as genetic changes, are also taking place. Understanding shifts in ecological processes can guide human adaptation strategies. In addition to reducing greenhouse gases, climate action and policy must therefore focus equally on strategies that safeguard biodiversity and ecosystems.

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

Not enough time for recovery Coral bleaching occurs when stressful conditions result in the expulsion of the algal partner from the coral. Before anthropogenic climate warming, such events were relatively rare, allowing for recovery of the reef between events. Hughes et al. looked at 100 reefs globally and found that the average interval between bleaching events is now less than half what it was before. Such narrow recovery windows do not allow for full recovery. Furthermore, warming events such as El Niño are warmer than previously, as are general ocean conditions. Such changes are likely to make it more and more difficult for reefs to recover between stressful events. Science, this issue p. 80 Coral reefs in the present day have less time than in earlier periods to recover from bleaching events. 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.

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

Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism’s function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.

Mesophotic coral ecosystems on the walls of Coral Sea atolls

A research cruise was undertaken in October 2010 to explore potential mesophotic coral communities (30–150 m) in the recently established Coral Sea Conservation Zone (CSCZ). The CSCZ covers an area of almost one million square kilometres east of the Great Barrier Reef (Australia), with its reefs and atolls located hundreds of kilometres from the nearest landmass and surrounded by deep oceanic water. Three of the atolls in the CSCZ (West Holmes Reef [16.243°S, 147.874°E], East Holmes Reef [16.459°S, 148.024°E] and Flora Reef [16.755°S, 147.738°E]) were assessed using SCUBA and a Seabotix ROV. Shallow reef areas (<30 m) consisted largely of bare substrate with predominantly juvenile corals and very low coral cover due to past cyclone damage and thermal bleaching events. In contrast, the steep walls in 40–100 m depth were covered by extensive Halimeda curtains (Fig. 1a), which harboured diverse scleractinian coral communities, including Acropora, Astreopora, Fungia, Galaxea, Goniastrea, Porites, Mycedium (Fig. 1c), Seriatopora and Turbinaria spp., with Pachyseris (Fig. 1d), Leptoseris and Montipora spp. recorded to 102 m depth. At least one of the collected specimens represents a new species record for Australia: Echino- morpha nishihirai (Fig. 1b). Diverse communities of azooxanthellate octocorals were also observed to 150 m, the maximum depth of the ROV. These observations confirm the presence of mesophotic coral ecosystems (MCEs) along the walls of Coral Sea atolls and indicate that MCEs may form extensive features in the CSCZ. The deep-water coral communities may play an important role in the recovery of shallow reef areas on these isolated atolls by functioning as refugia from the repeated disturbances that have affected these reefs.

From Corals to Canyons: The Great Barrier Reef Margin

The significance of submerged fossil coral reefs as important archives of abrupt global sea level rise and climate change has been confirmed by investigations in the Caribbean [Fairbanks, 1989] and the Indo-Pacific (see Montaggioni [2005] for a summary) and by recent Integrated Ocean Drilling Program (IODP) activities in Tahiti [Camoin et al., 2007]. Similar submerged (40-130 meters) reef structures are preserved along the margin of the Great Barrier Reef (GBR), but they have not yet been systematically studied. The submerged reefs have the potential to provide critical new information about the nature of past global sea level and climate variability and about the response of the GBR to these past and perhaps future environmental changes [Beaman et al., 2008]. Equally important for GBR Marine Park managers is information about the role of the reefs as habitats and substrates for modern biological communities. Here we summarize the highlights and broader implications of a September- October 2007 expedition on the R/V Southern Surveyor (Australian Marine National Facility, voyage SS07/2007) to investigate the shelf edge, upper slope, and submarine canyons along the GBR margin.

Quantifying the response of structural complexity and community composition to environmental change in marine communities

Habitat structural complexity is a key factor shaping marine communities. However, accurate methods for quantifying structural complexity underwater are currently lacking. Loss of structural complexity is linked to ecosystem declines in biodiversity and resilience. We developed new methods using underwater stereo-imagery spanning 4 years (2010-2013) to reconstruct 3D models of coral reef areas and quantified both structural complexity at two spatial resolutions (2.5 and 25 cm) and benthic community composition to characterize changes after an unprecedented thermal anomaly on the west coast of Australia in 2011. Structural complexity increased at both resolutions in quadrats (4 m(2)) that bleached, but not those that did not bleach. Changes in complexity were driven by species-specific responses to warming, highlighting the importance of identifying small-scale dynamics to disentangle ecological responses to disturbance. We demonstrate an effective, repeatable method for quantifying the relationship among community composition, structural complexity and ocean warming, improving predictions of the response of marine ecosystems to environmental change.

Predicting the Location and Spatial Extent of Submerged Coral Reef Habitat in the Great Barrier Reef World Heritage Area, Australia

Aim Coral reef communities occurring in deeper waters have received little research effort compared to their shallow-water counterparts, and even such basic information as their location and extent are currently unknown throughout most of the world. Using the Great Barrier Reef as a case study, habitat suitability modelling is used to predict the distribution of deep-water coral reef communities on the Great Barrier Reef, Australia. We test the effectiveness of a range of geophysical and environmental variables for predicting the location of deep-water coral reef communities on the Great Barrier Reef. Location Great Barrier Reef, Australia. Methods Maximum entropy modelling is used to identify the spatial extent of two broad communities of habitat-forming megabenthos phototrophs and heterotrophs. Models were generated using combinations of geophysical substrate properties derived from multibeam bathymetry and environmental data derived from Bio-ORACLE, combined with georeferenced occurrence records of mesophotic coral communities from autonomous underwater vehicle, remotely operated vehicle and SCUBA surveys. Model results are used to estimate the total amount of mesophotic coral reef habitat on the GBR. Results Our models predict extensive but previously undocumented coral communities occurring both along the continental shelf-edge of the Great Barrier Reef and also on submerged reefs inside the lagoon. Habitat suitability for phototrophs is highest on submerged reefs along the outer-shelf and the deeper flanks of emergent reefs inside the GBR lagoon, while suitability for heterotrophs is highest in the deep waters along the shelf-edge. Models using only geophysical variables consistently outperformed models incorporating environmental data for both phototrophs and heterotrophs. Main Conclusion Extensive submerged coral reef communities that are currently undocumented are likely to occur throughout the Great Barrier Reef. High-quality bathymetry data can be used to identify these reefs, which may play an important role in resilience of the GBR ecosystem to climate change.

Diverse staghorn coral fauna on the mesophotic reefs of north-east Australia

Concern for the future of reef-building corals in conditions of rising sea temperatures combined with recent technological advances has led to a renewed interest in documenting the biodiversity of mesophotic coral ecosystems (MCEs) and their potential to provide lineage continuation for coral taxa. Here, we examine species diversity of staghorn corals (genera Acropora and Isopora) in the mesophotic zone (below 30 m depth) of the Great Barrier Reef and western Coral Sea. Using specimen-based records we found 38 staghorn species in the mesophotic zone, including three species newly recorded for Australia and five species that only occurred below 30 m. Staghorn corals became scarce at depths below 50 m but were found growing in-situ to 73 m depth. Of the 76 staghorn coral species recorded for shallow waters (depth ≤ 30 m) in north-east Australia, 21% extended to mesophotic depths with a further 22% recorded only rarely to 40 m depth. Extending into the mesophotic zone provided shallow water species no significant advantage in terms of their estimated global range-size relative to species restricted to shallow waters (means 86.2 X 106 km2 and 85.7 X 106 km2 respectively, p = 0.98). We found four staghorn coral species at mesophotic depths on the Great Barrier Reef that were previously considered rare and endangered on the basis of their limited distribution in central Indonesia and the far western Pacific. Colonies below 40 m depth showed laterally flattened branches, light and fragile skeletal structure and increased spacing between branches and corallites. The morphological changes are discussed in relation to decreased light, water movement and down-welling coarse sediments. Staghorn corals have long been regarded as typical shallow-water genera, but here we demonstrate the significant contribution of this group to the region’s mesophotic fauna and the importance of considering MCEs in reef biodiversity estimates and management.