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.

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.

Evidence for climate-driven synchrony of marine and terrestrial ecosystems in northwest Australia.

The effects of climate change are difficult to predict for many marine species because little is known of their response to climate variations in the past. However, long-term chronologies of growth, a variable that integrates multiple physical and biological factors, are now available for several marine taxa. These allow us to search for climate-driven synchrony in growth across multiple taxa and ecosystems, identifying the key processes driving biological responses at very large spatial scales. We hypothesized that in northwest (NW) Australia, a region that is predicted to be strongly influenced by climate change, the El Niño Southern Oscillation (ENSO) phenomenon would be an important factor influencing the growth patterns of organisms in both marine and terrestrial environments. To test this idea, we analyzed existing growth chronologies of the marine fish Lutjanus argentimaculatus, the coral Porites spp. and the tree Callitris columellaris and developed a new chronology for another marine fish, Lethrinus nebulosus. Principal components analysis and linear model selection showed evidence of ENSO-driven synchrony in growth among all four taxa at interannual time scales, the first such result for the Southern Hemisphere. Rainfall, sea surface temperatures, and sea surface salinities, which are linked to the ENSO system, influenced the annual growth of fishes, trees, and corals. All four taxa had negative relationships with the Niño-4 index (a measure of ENSO status), with positive growth patterns occurring during strong La Niña years. This finding implies that future changes in the strength and frequency of ENSO events are likely to have major consequences for both marine and terrestrial taxa. Strong similarities in the growth patterns of fish and trees offer the possibility of using tree-ring chronologies, which span longer time periods than those of fish, to aid understanding of both historical and future responses of fish populations to climate variation.

Ocean acidification: Linking science to management solutions using the Great Barrier Reef as a case study.

Coral reefs are one of the most vulnerable ecosystems to ocean acidification. While our understanding of the potential impacts of ocean acidification on coral reef ecosystems is growing, gaps remain that limit our ability to translate scientific knowledge into management action. To guide solution-based research, we review the current knowledge of ocean acidification impacts on coral reefs alongside management needs and priorities. We use the world's largest continuous reef system, Australia's Great Barrier Reef (GBR), as a case study. We integrate scientific knowledge gained from a variety of approaches (e.g., laboratory studies, field observations, and ecosystem modelling) and scales (e.g., cell, organism, ecosystem) that underpin a systems-level understanding of how ocean acidification is likely to impact the GBR and associated goods and services. We then discuss local and regional management options that may be effective to help mitigate the effects of ocean acidification on the GBR, with likely application to other coral reef systems. We develop a research framework for linking solution-based ocean acidification research to practical management options. The framework assists in identifying effective and cost-efficient options for supporting ecosystem resilience. The framework enables on-the-ground OA management to be the focus, while not losing sight of CO2 mitigation as the ultimate solution.

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.

Growth responses of branching versus massive corals to ocean warming on the Great Barrier Reef, Australia.

As oceans continue to warm under climate change, understanding the differential growth responses of corals is increasingly important. Scleractinian corals exhibit a broad range of life-history strategies, yet few studies have explored interspecific variation in long-term growth rates under a changing climate. Here we studied growth records of two coral species with different growth forms, namely branching Isopora palifera and massive Porites spp. at an offshore reef (Myrmidon Reef) of the central Great Barrier Reef (GBR), Australia. Skeletal growth chronologies were constructed using a combination of X-radiographs, gamma densitometry, and trace element (Sr/Ca) analysis. General additive mixed-effect models (GAMMs) revealed that skeletal density of I. palifera declined linearly and significantly at a rate of 1.2% yr-1 between 2002 and 2012. Calcification was stable between 2002 and 2009, yet declined significantly at a rate of 12% yr-1 between 2009 and 2012 following anomalously high sea surface temperatures (SST). Skeletal density of massive Porites exhibited a significant non-linear response over the 11-year study period (2002-2012) in that density was temporarily reduced during the 2009-2010 anomalously hot years, while linear extension and calcification showed no significant trends. Linear extension, density and calcification rates of I. palifera increased to maximum growth of 26.7-26.9 °C, beyond which they declined. In contrast, calcification and linear extension of Porites exhibited no response to SST, but exhibited a significant linear decline in skeletal density with increasing SST. Our results reveal significant differences in coral growth patterns among coral growth forms, and highlight both the resistant nature of massive Porites and sensitivity of branching I. palifera. Future research should target a broad range of coral taxa within similar environments to provide a community-level response of ocean warming on coral reef communities.

Coral skeletons reveal the history of nitrogen cycling in the coastal Great Barrier Reef.

Anthropogenic nutrient discharge to coastal marine environments is commonly associated with excessive algal growth and ecosystem degradation. However in the world's largest coral reef ecosystem, the Great Barrier Reef (GBR), the response to enhanced terrestrial nutrient inputs since European settlement in the 1850's remains unclear. Here we use a 333 year old composite record (1680-2012) of 15N/14N in coral skeleton-bound organic matter to understand how nitrogen cycling in the coastal GBR has responded to increased anthropogenic nutrient inputs. Our major robust finding is that the coral record shows a long-term decline in skeletal 15N/14N towards the present. We argue that this decline is evidence for increased coastal nitrogen fixation rather than a direct reflection of anthropogenic nitrogen inputs. Reducing phosphorus discharge and availability would short-circuit the nitrogen fixation feedback loop and help avoid future acute and chronic eutrophication in the coastal GBR.

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.

Presence of skeletal banding in a reef-building tropical crustose coralline alga.

The presence of banding in the skeleton of coralline algae has been reported in many species, primarily from temperate and polar regions. Similar to tree rings, skeletal banding can provide information on growth rate, age, and longevity; as well as records of past environmental conditions and the coralline alga's growth responses to such changes. The aim of this study was to explore the presence and characterise the nature of banding in the tropical coralline alga Porolithon onkodes, an abundant and key reef-building species on the Great Barrier Reef (GBR) Australia, and the Indo-Pacific in general. To achieve this we employed various methods including X-ray diffraction (XRD) to determine seasonal mol% magnesium (Mg), mineralogy mapping to investigate changes in dominant mineral phases, scanning electron microscopy-electron dispersive spectroscopy (SEM-EDS), and micro-computed tomography (micro-CT) scanning to examine changes in cell size and density banding, and UV light to examine reproductive (conceptacle) banding. Seasonal variation in the Mg content of the skeleton did occur and followed previously recorded variations with the highest mol% MgCO3 in summer and lowest in winter, confirming the positive relationship between seawater temperature and mol% MgCO3. Rows of conceptacles viewed under UV light provided easily distinguishable bands that could be used to measure vertical growth rate (1.4 mm year-1) and age of the organism. Micro-CT scanning showed obvious banding patterns in relation to skeletal density, and mineralogical mapping revealed patterns of banding created by changes in Mg content. Thus, we present new evidence for seasonal banding patterns in the tropical coralline alga P. onkodes. This banding in the P. onkodes skeleton can provide valuable information into the present and past life history of this important reef-building species, and is essential to assess and predict the response of these organisms to future climate and environmental changes.

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.

The paleoclimate context and future trajectory of extreme summer hydroclimate in eastern Australia.

Eastern Australia recently experienced an intense drought (Millennium Drought, 2003-2009) and record-breaking rainfall and flooding (austral summer 2010-2011). There is some limited evidence for a climate change contribution to these events, but such analyses are hampered by the paucity of information on long-term natural variability. Analyzing a new reconstruction of summer (December-January-February) Palmer Drought Severity Index (the Australia-New Zealand Drought Atlas; ANZDA, 1500-2012 CE), we find moisture deficits during the Millennium Drought fall within the range of the last 500 years of natural hydroclimate variability. This variability includes periods of multi-decadal drought in the 1500s more persistent than any event in the historical record. However, the severity of the Millennium Drought, which was caused by autumn (March-April-May) precipitation declines, may be underestimated in the ANZDA because the reconstruction is biased towards summer and antecedent spring (September-October-November) precipitation. The pluvial in 2011, however, which was characterized by extreme summer rainfall faithfully captured by the ANZDA, is likely the wettest year in the reconstruction for Coastal Queensland. Climate projections (RCP 8.5 scenario) suggest that eastern Australia will experience long-term drying during the 21st century. While the contribution of anthropogenic forcing to recent extremes remains an open question, these projections indicate an amplified risk of multi-year drought anomalies matching or exceeding the intensity of the Millennium Drought.

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.

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.

Growth of Western Australian corals in the anthropocene.

Anthropogenic increases of atmospheric carbon dioxide lead to warmer sea surface temperatures and altered ocean chemistry. Experimental evidence suggests that coral calcification decreases as aragonite saturation drops but increases as temperatures rise toward thresholds optimal for coral growth. In situ studies have documented alarming recent declines in calcification rates on several tropical coral reef ecosystems. We show there is no widespread pattern of consistent decline in calcification rates of massive Porites during the 20th century on reefs spanning an 11° latitudinal range in the southeast Indian Ocean off Western Australia. Increasing calcification rates on the high-latitude reefs contrast with the downward trajectory reported for corals on Australia's Great Barrier Reef and provide additional evidence that recent changes in coral calcification are responses to temperature rather than ocean acidification.

Assessing amino acid racemization variability in coral intra-crystalline protein for geochronological applications.

Over 500 Free Amino Acid (FAA) and corresponding Total Hydrolysed Amino Acid (THAA) analyses were completed from eight independently-dated, multi-century coral cores of massive Porites sp. colonies. This dataset allows us to re-evaluate the application of amino acid racemization (AAR) for dating late Holocene coral material, 20 years after Goodfriend et al. (GCA56 (1992), 3847) first showed AAR had promise for developing chronologies in coral cores. This re-assessment incorporates recent method improvements, including measurement by RP-HPLC, new quality control approaches (e.g. sampling and sub-sampling protocols, statistically-based data screening criteria), and cleaning steps to isolate the intra-crystalline skeletal protein. We show that the removal of the extra-crystalline contaminants and matrix protein is the most critical step for reproducible results and recommend a protocol of bleaching samples in NaOCl for 48 h to maximise removal of open system proteins while minimising the induced racemization. We demonstrate that AAR follows closed system behaviour in the intra-crystalline fraction of the coral skeletal proteins. Our study is the first to assess the natural variability in intra-crystalline AAR between colonies, and we use coral cores taken from the Great Barrier Reef, Australia, and Jarvis Island in the equatorial Pacific to explore variability associated with different environmental conditions and thermal histories. Chronologies were developed from THAA Asx D/L, Ala D/L, Glx D/L and FAA Asx D/L for each core and least squares Monte Carlo modelling applied in order to quantify uncertainty of AAR age determinations and assess the level of dating resolution possible over the last 5 centuries. AAR within colonies follow consistent stratigraphic aging. However, there are systematic differences in rates between the colonies, which would preclude direct comparison from one colony to another for accurate age estimation. When AAR age models are developed from a combined dataset to include this natural inter-colony variability THAA Asx D/L, Glx D/L and Ala D/L give a 2σ age uncertainty of ±19, ±38 and ±29 year, for the 20th C respectively; in comparison 2σ age uncertainties from a single colony are ±12, ±12 and ±14 year. This is the first demonstration of FAA D/L for dating coral and following strict protocols 2σ precisions of ±24 years can be achieved across different colonies in samples from the last 150 years, and can be ±10 years within a core from a single colony. Despite these relatively large error estimates, AAR would be a valuable tool in situations where a large number of samples need to be screened rapidly and cheaply (e.g. identifying material from mixed populations in beach or uplift deposits), prior to and complementing the more time-consuming geochronological tools of U/Th or seasonal isotopic timeseries.

Declining coral calcification on the Great Barrier Reef.

Reef-building corals are under increasing physiological stress from a changing climate and ocean absorption of increasing atmospheric carbon dioxide. We investigated 328 colonies of massive Porites corals from 69 reefs of the Great Barrier Reef (GBR) in Australia. Their skeletal records show that throughout the GBR, calcification has declined by 14.2% since 1990, predominantly because extension (linear growth) has declined by 13.3%. The data suggest that such a severe and sudden decline in calcification is unprecedented in at least the past 400 years. Calcification increases linearly with increasing large-scale sea surface temperature but responds nonlinearly to annual temperature anomalies. The causes of the decline remain unknown; however, this study suggests that increasing temperature stress and a declining saturation state of seawater aragonite may be diminishing the ability of GBR corals to deposit calcium carbonate.

10th Anniversary Review: a changing climate for coral reefs.

Tropical coral reefs are charismatic ecosystems that house a significant proportion of the world's marine biodiversity. Their valuable goods and services are fundamental to the livelihood of large coastal populations in the tropics. The health of many of the world's coral reefs, and the goods and services they provide, have already been severely compromised, largely due to over-exploitation by a range of human activities. These local-scale impacts, with the appropriate government instruments, support and management actions, can potentially be controlled and even ameliorated. Unfortunately, other human actions (largely in countries outside of the tropics), by changing global climate, have added additional global-scale threats to the continued survival of present-day coral reefs. Moderate warming of the tropical oceans has already resulted in an increase in mass coral bleaching events, affecting nearly all of the world's coral reef regions. The frequency of these events will only increase as global temperatures continue to rise. Weakening of coral reef structures will be a more insidious effect of changing ocean chemistry, as the oceans absorb part of the excess atmospheric carbon dioxide. More intense tropical cyclones, changed atmospheric and ocean circulation patterns will all affect coral reef ecosystems and the many associated plants and animals. Coral reefs will not disappear but their appearance, structure and community make-up will radically change. Drastic greenhouse gas mitigation strategies are necessary to prevent the full consequences of human activities causing such alterations to coral reef ecosystems.

Preindustrial to modern interdecadal variability in coral reef pH.

The oceans are becoming more acidic due to absorption of anthropogenic carbon dioxide from the atmosphere. The impact of ocean acidification on marine ecosystems is unclear, but it will likely depend on species adaptability and the rate of change of seawater pH relative to its natural variability. To constrain the natural variability in reef-water pH, we measured boron isotopic compositions in a approximately 300-year-old massive Porites coral from the southwestern Pacific. Large variations in pH are found over approximately 50-year cycles that covary with the Interdecadal Pacific Oscillation of ocean-atmosphere anomalies, suggesting that natural pH cycles can modulate the impact of ocean acidification on coral reef ecosystems.