Unified methods in collecting, preserving, and archiving coral bleaching and restoration specimens to increase sample utility and interdisciplinary collaboration.

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at -80 °C to -20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

Climate-assisted persistence of tropical fish vagrants in temperate marine ecosystems.

Rising temperatures and extreme climate events are propelling tropical species into temperate marine ecosystems, but not all species can persist. Here, we used the heatwave-driven expatriation of tropical Black Rabbitfish (Siganus fuscescens) to the temperate environments of Western Australia to assess the ecological and evolutionary mechanisms that may entail their persistence. Population genomic assays for this rabbitfish indicated little genetic differentiation between tropical residents and vagrants to temperate environments due to high migration rates, which were likely enhanced by the marine heatwave. DNA metabarcoding revealed a diverse diet for this species based on phytoplankton and algae, as well as an ability to feed on regional resources, including kelp. Irrespective of future climate scenarios, these macroalgae-consuming vagrants may self-recruit in temperate environments and further expand their geographic range by the year 2100. This expansion may compromise the health of the kelp forests that form Australia's Great Southern Reef. Overall, our study demonstrates that projected favourable climate conditions, continued large-scale genetic connectivity between populations, and diet versatility are key for tropical range-shifting fish to establish in temperate ecosystems.

Global declines in coral reef calcium carbonate production under ocean acidification and warming.

Ocean warming and acidification threaten the future growth of coral reefs. This is because the calcifying coral reef taxa that construct the calcium carbonate frameworks and cement the reef together are highly sensitive to ocean warming and acidification. However, the global-scale effects of ocean warming and acidification on rates of coral reef net carbonate production remain poorly constrained despite a wealth of studies assessing their effects on the calcification of individual organisms. Here, we present global estimates of projected future changes in coral reef net carbonate production under ocean warming and acidification. We apply a meta-analysis of responses of coral reef taxa calcification and bioerosion rates to predicted changes in coral cover driven by climate change to estimate the net carbonate production rates of 183 reefs worldwide by 2050 and 2100. We forecast mean global reef net carbonate production under representative concentration pathways (RCP) 2.6, 4.5, and 8.5 will decline by 76, 149, and 156%, respectively, by 2100. While 63% of reefs are projected to continue to accrete by 2100 under RCP2.6, 94% will be eroding by 2050 under RCP8.5, and no reefs will continue to accrete at rates matching projected sea level rise under RCP4.5 or 8.5 by 2100. Projected reduced coral cover due to bleaching events predominately drives these declines rather than the direct physiological impacts of ocean warming and acidification on calcification or bioerosion. Presently degraded reefs were also more sensitive in our analysis. These findings highlight the low likelihood that the world's coral reefs will maintain their functional roles without near-term stabilization of atmospheric CO2 emissions.

A portfolio of climate-tailored approaches to advance the design of marine protected areas in the Red Sea.

Intensified coastal development is compromising the health and functioning of marine ecosystems. A key example of this is the Red Sea, a biodiversity hotspot subjected to increasing local human pressures. While some marine-protected areas (MPAs) were placed to alleviate these stressors, it is unclear whether these MPAs are managed or enforced, thus providing limited protection. Yet, most importantly, MPAs in the Red Sea were not designed using climate considerations, likely diminishing their effectiveness against global stressors. Here, we propose to tailor the design of MPAs in the Red Sea by integrating approaches to enhance climate change mitigation and adaptation. First, including coral bleaching susceptibility could produce a more resilient network of MPAs by safeguarding reefs from different thermal regions that vary in spatiotemporal bleaching responses, reducing the risk that all protected reefs will bleach simultaneously. Second, preserving the basin-wide genetic connectivity patterns that are assisted by mesoscale eddies could further ensure recovery of sensitive populations and maintain species potential to adapt to environmental changes. Finally, protecting mangrove forests in the northern and southern Red Sea that act as major carbon sinks could help offset greenhouse gas emissions. If implemented with multinational cooperation and concerted effort among stakeholders, our portfolio of climate-tailored approaches may help build a network of MPAs in the Red Sea that protects more effectively its coastal resources against escalating coastal development and climate instability. Beyond the Red Sea, we anticipate this study to serve as an example of how to improve the utility of tropical MPAs as climate-informed conservation tools.

The past century of coral bleaching in the Saudi Arabian central Red Sea.

Accurate knowledge of the spatial and temporal patterns of coral bleaching is essential both for understanding how coral reef ecosystems are changing today and forecasting their future states. Yet, in many regions of the world, the history of bleaching is poorly known, especially prior to the late 20th century. Here, I use the information preserved within skeleton cores of long-lived Porites corals to reconstruct the past century of bleaching events in the Saudi Arabian central Red Sea. In these cores, skeletal "stress bands"-indicative of past bleaching-captured known bleaching events that occurred in 1998 and 2010, but also revealed evidence of previously unknown bleaching events in 1931, 1978, and 1982. However, these earlier events affected a significantly lesser proportion of corals than 1998 and 2010. Therefore, coral bleaching may have occurred in the central Red Sea earlier than previously recognized, but the frequency and severity of bleaching events since 1998 on nearshore reefs is unprecedented over the past century. Conversely, corals living on mid- to outer-shelf reefs have not been equally susceptible to bleaching as their nearshore counterparts, which was evident in that stress bands were five times more prevalent nearshore. Whether this pattern of susceptible nearshore reefs and resistant outer-shelf reefs continues in the future remains a key question in forecasting coral reef futures in this region.

Nutrient-supplying ocean currents modulate coral bleaching susceptibility.

With predictions that mass coral bleaching will occur annually within this century, conservation efforts must focus their limited resources based on an accurate understanding of the drivers of bleaching. Here, we provide spatial and temporal evidence that excess nutrients exacerbate the detrimental effects of heat stress to spark mass coral bleaching in the Red Sea. Exploiting this region's unique oceanographic regime, where nutrients and heat stress vary independently, we demonstrate that the world's third largest coral reef system historically suffered from severe mass bleaching only when exposed to both unusually high temperature and nutrients. Incorporating nutrient-supplying ocean currents and their variability into coral bleaching forecasts will be critical for effectively guiding efforts to safeguard the reefs most likely to persist in the Anthropocene.

Treating coral bleaching as weather: a framework to validate and optimize prediction skill.

Few coral reefs remain unscathed by mass bleaching over the past several decades, and much of the coral reef science conducted today relates in some way to the causes, consequences, or recovery pathways of bleaching events. Most studies portray a simple cause and effect relationship between anomalously high summer temperatures and bleaching, which is understandable given that bleaching rarely occurs outside these unusually warm times. However, the statistical skill with which temperature captures bleaching is hampered by many "false alarms", times when temperatures reached nominal bleaching levels, but bleaching did not occur. While these false alarms are often not included in global bleaching assessments, they offer valuable opportunities to improve predictive skill, and therefore understanding, of coral bleaching events. Here, I show how a statistical framework adopted from weather forecasting can optimize bleaching predictions and validate which environmental factors play a role in bleaching susceptibility. Removing the 1 °C above the maximum monthly mean cutoff in the typical degree heating weeks (DHW) definition, adjusting the DHW window from 12 to 9 weeks, using regional-specific DHW thresholds, and including an El Niño threshold already improves the model skill by 45%. Most importantly, this framework enables hypothesis testing of other factors or metrics that may improve our ability to forecast coral bleaching events.

An enigmatic decoupling between heat stress and coral bleaching on the Great Barrier Reef.

Ocean warming threatens the functioning of coral reef ecosystems by inducing mass coral bleaching and mortality events. The link between temperature and coral bleaching is now well-established based on observations that mass bleaching events usually occur when seawater temperatures are anomalously high. However, times of high heat stress but without coral bleaching are equally important because they can inform an understanding of factors that regulate temperature-induced bleaching. Here, we investigate the absence of mass coral bleaching on the Great Barrier Reef (GBR) during austral summer 2004. Using four gridded sea surface temperature data products, validated with in situ temperature loggers, we demonstrate that the summer of 2004 was among the warmest summers of the satellite era (1982-2017) on the GBR. At least half of the GBR experienced temperatures that were high enough to initiate bleaching in other years, yet mass bleaching was not reported during 2004. The absence of bleaching is not fully explained by wind speed or cloud cover. Rather, 2004 is clearly differentiated from bleaching years by the slow speed of the East Australian Current (EAC) offshore of the GBR. An anomalously slow EAC during summer 2004 may have dampened the upwelling of nutrient-rich waters onto the GBR shelf, potentially mitigating bleaching due to the lower susceptibility of corals to heat stress in low-nutrient conditions. Although other factors such as irradiance or acclimatization may have played a role in the absence of mass bleaching, 2004 remains a key case study for demonstrating the dynamic nature of coral responses to marine heatwaves.

Acclimatization of massive reef-building corals to consecutive heatwaves.

Reef-building corals typically live close to the upper limits of their thermal tolerance and even small increases in summer water temperatures can lead to bleaching and mortality. Projections of coral reef futures based on forecasts of ocean temperatures indicate that by the end of this century, corals will experience their current thermal thresholds annually, which would lead to the widespread devastation of coral reef ecosystems. Here, we use skeletal cores of long-lived Porites corals collected from 14 reefs across the northern Great Barrier Reef, the Coral Sea, and New Caledonia to evaluate changes in their sensitivity to heat stress since 1815. High-density 'stress bands'-indicative of past bleaching-first appear during a strong pre-industrial El Niño event in 1877 but become significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming. However, the proportion of cores with stress bands declines following successive bleaching events in the twenty-first century despite increasing exposure to heat stress. Our findings demonstrate an increase in the thermal tolerance of reef-building corals and offer a glimmer of hope that at least some coral species can acclimatize fast enough to keep pace with global warming.

Investigating marine bio-calcification mechanisms in a changing ocean with in vivo and high-resolution ex vivo Raman spectroscopy.

Ocean acidification poses a serious threat to marine calcifying organisms, yet experimental and field studies have found highly diverse responses among species and environments. Our understanding of the underlying drivers of differential responses to ocean acidification is currently limited by difficulties in directly observing and quantifying the mechanisms of bio-calcification. Here, we present Raman spectroscopy techniques for characterizing the skeletal mineralogy and calcifying fluid chemistry of marine calcifying organisms such as corals, coralline algae, foraminifera, and fish (carbonate otoliths). First, our in vivo Raman technique is the ideal tool for investigating non-classical mineralization pathways. This includes calcification by amorphous particle attachment, which has recently been controversially suggested as a mechanism by which corals resist the negative effects of ocean acidification. Second, high-resolution ex vivo Raman mapping reveals complex banding structures in the mineralogy of marine calcifiers, and provides a tool to quantify calcification responses to environmental variability on various timescales from days to years. We describe the new insights into marine bio-calcification that our techniques have already uncovered, and we consider the wide range of questions regarding calcifier responses to global change that can now be proposed and addressed with these new Raman spectroscopy tools.

Environmental and physiochemical controls on coral calcification along a latitudinal temperature gradient in Western Australia.

The processes that occur at the micro-scale site of calcification are fundamental to understanding the response of coral growth in a changing world. However, our mechanistic understanding of chemical processes driving calcification is still evolving. Here, we report the results of a long-term in situ study of coral calcification rates, photo-physiology, and calcifying fluid (cf) carbonate chemistry (using boron isotopes, elemental systematics, and Raman spectroscopy) for seven species (four genera) of symbiotic corals growing in their natural environments at tropical, subtropical, and temperate locations in Western Australia (latitudinal range of ~11°). We find that changes in net coral calcification rates are primarily driven by pHcf and carbonate ion concentration [ CO 3 2 - ]cf in conjunction with temperature and DICcf . Coral pHcf varies with latitudinal and seasonal changes in temperature and works together with the seasonally varying DICcf to optimize [ CO 3 2 - ]cf at species-dependent levels. Our results indicate that corals shift their pHcf to adapt and/or acclimatize to their localized thermal regimes. This biological response is likely to have critical implications for predicting the future of coral reefs under CO2 -driven warming and acidification.

Repeat bleaching of a central Pacific coral reef over the past six decades (1960-2016).

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world's most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015-16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world.

Similar controls on calcification under ocean acidification across unrelated coral reef taxa.

Ocean acidification (OA) is a major threat to marine ecosystems, particularly coral reefs which are heavily reliant on calcareous species. OA decreases seawater pH and calcium carbonate saturation state (Ω), and increases the concentration of dissolved inorganic carbon (DIC). Intense scientific effort has attempted to determine the mechanisms via which ocean acidification (OA) influences calcification, led by early hypotheses that calcium carbonate saturation state (Ω) is the main driver. We grew corals and coralline algae for 8-21 weeks, under treatments where the seawater parameters Ω, pH, and DIC were manipulated to examine their differential effects on calcification rates and calcifying fluid chemistry (Ωcf , pHcf , and DICcf ). Here, using long duration experiments, we provide geochemical evidence that differing physiological controls on carbonate chemistry at the site of calcification, rather than seawater Ω, are the main determinants of calcification. We found that changes in seawater pH and DIC rather than Ω had the greatest effects on calcification and calcifying fluid chemistry, though the effects of seawater carbonate chemistry were limited. Our results demonstrate the capacity of organisms from taxa with vastly different calcification mechanisms to regulate their internal chemistry under extreme chemical conditions. These findings provide an explanation for the resistance of some species to OA, while also demonstrating how changes in seawater DIC and pH under OA influence calcification of key coral reef taxa.

Mechanisms and seasonal drivers of calcification in the temperate coral Turbinaria reniformis at its latitudinal limits.

High-latitude coral reefs provide natural laboratories for investigating the mechanisms and limits of coral calcification. While the calcification processes of tropical corals have been studied intensively, little is known about how their temperate counterparts grow under much lower temperature and light conditions. Here, we report the results of a long-term (2-year) study of seasonal changes in calcification rates, photo-physiology and calcifying fluid (cf) chemistry (using boron isotope systematics and Raman spectroscopy) for the coral Turbinaria reniformis growing near its latitudinal limits (34.5° S) along the southern coast of Western Australia. In contrast with tropical corals, calcification rates were found to be threefold higher during winter (16 to 17° C) compared with summer (approx. 21° C), and negatively correlated with light, but lacking any correlation with temperature. These unexpected findings are attributed to a combination of higher chlorophyll a, and hence increased heterotrophy during winter compared with summer, together with the corals' ability to seasonally modulate pHcf, with carbonate ion concentration [Formula: see text] being the main controller of calcification rates. Conversely, calcium ion concentration [Ca2+]cf declined with increasing calcification rates, resulting in aragonite saturation states Ωcf that were stable yet elevated fourfold above seawater values. Our results show that corals growing near their latitudinal limits exert strong physiological control over their cf in order to maintain year-round calcification rates that are insensitive to the unfavourable temperature regimes typical of high-latitude reefs.

21st-century rise in anthropogenic nitrogen deposition on a remote coral reef.

With the rapid rise in pollution-associated nitrogen inputs to the western Pacific, it has been suggested that even the open ocean has been affected. In a coral core from Dongsha Atoll, a remote coral reef ecosystem, we observe a decline in the 15N/14N of coral skeleton-bound organic matter, which signals increased deposition of anthropogenic atmospheric N on the open ocean and its incorporation into plankton and, in turn, the atoll corals. The first clear change occurred just before 2000 CE, decades later than predicted by other work. The amplitude of change suggests that, by 2010, anthropogenic atmospheric N deposition represented 20 ± 5% of the annual N input to the surface ocean in this region, which appears to be at the lower end of other estimates.

Mass coral mortality under local amplification of 2 °C ocean warming.

A 2 °C increase in global temperature above pre-industrial levels is considered a reasonable target for avoiding the most devastating impacts of anthropogenic climate change. In June 2015, sea surface temperature (SST) of the South China Sea (SCS) increased by 2 °C in response to the developing Pacific El Niño. On its own, this moderate, short-lived warming was unlikely to cause widespread damage to coral reefs in the region, and the coral reef "Bleaching Alert" alarm was not raised. However, on Dongsha Atoll, in the northern SCS, unusually weak winds created low-flow conditions that amplified the 2 °C basin-scale anomaly. Water temperatures on the reef flat, normally indistinguishable from open-ocean SST, exceeded 6 °C above normal summertime levels. Mass coral bleaching quickly ensued, killing 40% of the resident coral community in an event unprecedented in at least the past 40 years. Our findings highlight the risks of 2 °C ocean warming to coral reef ecosystems when global and local processes align to drive intense heating, with devastating consequences.

Changes in coral reef communities across a natural gradient in seawater pH.

Ocean acidification threatens the survival of coral reef ecosystems worldwide. The negative effects of ocean acidification observed in many laboratory experiments have been seen in studies of naturally low-pH reefs, with little evidence to date for adaptation. Recently, we reported initial data suggesting that low-pH coral communities of the Palau Rock Islands appear healthy despite the extreme conditions in which they live. Here, we build on that observation with a comprehensive statistical analysis of benthic communities across Palau's natural acidification gradient. Our analysis revealed a shift in coral community composition but no impact of acidification on coral richness, coralline algae abundance, macroalgae cover, coral calcification, or skeletal density. However, coral bioerosion increased 11-fold as pH decreased from the barrier reefs to the Rock Island bays. Indeed, a comparison of the naturally low-pH coral reef systems studied so far revealed increased bioerosion to be the only consistent feature among them, as responses varied across other indices of ecosystem health. Our results imply that whereas community responses may vary, escalation of coral reef bioerosion and acceleration of a shift from net accreting to net eroding reef structures will likely be a global signature of ocean acidification.