Including environmental and climatic considerations for sustainable coral reef restoration.

Coral reefs provide ecosystem benefits to millions of people but are threatened by rapid environmental change and ever-increasing human pressures. Restoration is becoming a priority strategy for coral reef conservation, yet implementation remains challenging and it is becoming increasingly apparent that indirect conservation and restoration approaches will not ensure the long-term sustainability of coral reefs. The important role of environmental conditions in restoration practice are currently undervalued, carrying substantial implications for restoration success. Giving paramount importance to environmental conditions, particularly during the pre-restoration planning phase, has the potential to bring about considerable improvements in coral reef restoration and innovation. This Essay argues that restoration risk may be reduced by adopting an environmentally aware perspective that gives historical, contemporary, and future context to restoration decisions. Such an approach will open up new restoration opportunities with improved sustainability that have the capacity to dynamically respond to environmental trajectories.

Divergent recovery trajectories of intertidal and subtidal coral communities highlight habitat-specific recovery dynamics following bleaching in an extreme macrotidal reef environment.

Coral reefs face an uncertain future punctuated by recurring climate-induced disturbances. Understanding how reefs can recover from and reassemble after mass bleaching events is therefore important to predict their responses and persistence in a rapidly changing ocean. On naturally extreme reefs characterized by strong daily temperature variability, coral heat tolerance can vary significantly over small spatial gradients but it remains poorly understood how this impacts bleaching resilience and recovery dynamics, despite their importance as resilience hotspots and potential refugia. In the macrotidal Kimberley region in NW Australia, the 2016 global mass bleaching event had a strong habitat-specific impact on intertidal and subtidal coral communities at our study site: corals in the thermally variable intertidal bleached less severely and recovered within six months, while 68% of corals in the moderately variable subtidal died. We therefore conducted benthic surveys 3.5 years after the bleaching event to determine potential changes in benthic cover and coral community composition. In the subtidal, we documented substantial increases in algal cover and live coral cover had not fully recovered to pre-bleaching levels. Furthermore, the subtidal coral community shifted from being dominated by branching Acropora corals with a competitive life history strategy to opportunistic, weedy Pocillopora corals which likely has implications for the functioning and stress resilience of this novel coral community. In contrast, no shifts in algal and live coral cover or coral community composition occurred in the intertidal. These findings demonstrate that differences in coral heat tolerance across small spatial scales can have large consequences for bleaching resilience and that spatial patchiness in recovery trajectories and community reassembly after bleaching might be a common feature on thermally variable reefs. Our findings further confirm that reefs adapted to high daily temperature variability play a key role as resilience hotspots under current climate conditions, but their ability to do so may be limited under intensifying ocean warming.

Corals at the edge of environmental limits: A new conceptual framework to re-define marginal and extreme coral communities.

The worldwide decline of coral reefs has renewed interest in coral communities at the edge of environmental limits because they have the potential to serve as resilience hotspots and climate change refugia, and can provide insights into how coral reefs might function in future ocean conditions. These coral communities are often referred to as marginal or extreme but few definitions exist and usage of these terms has therefore been inconsistent. This creates significant challenges for categorising these often poorly studied communities and synthesising data across locations. Furthermore, this impedes our understanding of how coral communities can persist at the edge of their environmental limits and the lessons they provide for future coral reef survival. Here, we propose that marginal and extreme coral communities are related but distinct and provide a novel conceptual framework to redefine them. Specifically, we define coral reef extremeness solely based on environmental conditions (i.e., large deviations from optimal conditions in terms of mean and/or variance) and marginality solely based on ecological criteria (i.e., altered community composition and/or ecosystem functioning). This joint but independent assessment of environmental and ecological criteria is critical to avoid common pitfalls where coral communities existing outside the presumed optimal conditions for coral reef development are automatically considered inferior to coral reefs in more traditional settings. We further evaluate the differential potential of marginal and extreme coral communities to serve as natural laboratories, resilience hotspots and climate change refugia, and discuss strategies for their conservation and management as well as priorities for future research. Our new classification framework provides an important tool to improve our understanding of how corals can persist at the edge of their environmental limits and how we can leverage this knowledge to optimise strategies for coral reef conservation, restoration and management in a rapidly changing ocean.

Impacts of ocean warming and acidification on calcifying coral reef taxa: mechanisms responsible and adaptive capacity.

Ocean warming (OW) and acidification (OA) are two of the greatest global threats to the persistence of coral reefs. Calcifying reef taxa such as corals and coralline algae provide the essential substrate and habitat in tropical reefs but are at particular risk due to their susceptibility to both OW and OA. OW poses the greater threat to future reef growth and function, via its capacity to destabilise the productivity of both taxa, and to cause mass bleaching events and mortality of corals. Marine heatwaves are projected to increase in frequency, intensity, and duration over the coming decades, raising the question of whether coral reefs will be able to persist as functioning ecosystems and in what form. OA should not be overlooked, as its negative impacts on the calcification of reef-building corals and coralline algae will have consequences for global reef accretion. Given that OA can have negative impacts on the reproduction and early life stages of both coralline algae and corals, the interdependence of these taxa may result in negative feedbacks for reef replenishment. However, there is little evidence that OA causes coral bleaching or exacerbates the effects of OW on coral bleaching. Instead, there is some evidence that OA alters the photo-physiology of both taxa. Tropical coralline algal possess shorter generation times than corals, which could enable more rapid evolutionary responses. Future reefs will be dominated by taxa with shorter generation times and high plasticity, or those individuals inherently resistant and resilient to both marine heatwaves and OA.

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.

Stress-resistant corals may not acclimatize to ocean warming but maintain heat tolerance under cooler temperatures.

Naturally heat-resistant coral populations hold significant potential for facilitating coral reef survival under rapid climate change. However, it remains poorly understood whether they can acclimatize to ocean warming when superimposed on their already thermally-extreme habitats. Furthermore, it is unknown whether they can maintain their heat tolerance upon larval dispersal or translocation to cooler reefs. We test this in a long-term mesocosm experiment using stress-resistant corals from thermally-extreme reefs in NW Australia. We show that these corals have a remarkable ability to maintain their heat tolerance and health despite acclimation to 3-6 °C cooler, more stable temperatures over 9 months. However, they are unable to increase their bleaching thresholds after 6-months acclimation to + 1 °C warming. This apparent rigidity in the thermal thresholds of even stress-resistant corals highlights the increasing vulnerability of corals to ocean warming, but provides a rationale for human-assisted migration to restore cooler, degraded reefs with corals from thermally-extreme reefs.

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.

How can "Super Corals" facilitate global coral reef survival under rapid environmental and climatic change?

Coral reefs are in a state of rapid global decline via environmental and climate change, and efforts have intensified to identify or engineer coral populations with increased resilience. Concurrent with these efforts has been increasing use of the popularized term "Super Coral" in both popular media and scientific literature without a unifying definition. However, how this subjective term is currently applied has the potential to mislead inference over factors contributing to coral survivorship, and the future trajectory of coral reef form and functioning. Here, we discuss that the information required to support a single definition does not exist, and in fact may never be appropriate, i.e. "How Super is Super"? Instead, we advocate caution of this term, and suggest a workflow that enables contextualization and clarification of superiority to ensure that inferred or asserted survivorship is appropriate into future reef projections. This is crucial to robustly unlock how "Super Corals" can be integrated into the suite of management options required to facilitate coral survival under rapid environmental and climate change.

Coral physiology and microbiome dynamics under combined warming and ocean acidification.

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 µatm) and treatment (29.0°C and pCO2 of 750 µatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

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.

Coral calcification mechanisms facilitate adaptive responses to ocean acidification.

Ocean acidification (OA) is a pressing threat to reef-building corals, but it remains poorly understood how coral calcification is inhibited by OA and whether corals could acclimatize and/or adapt to OA. Using a novel geochemical approach, we reconstructed the carbonate chemistry of the calcifying fluid in two coral species using both a pH and dissolved inorganic carbon (DIC) proxy (δ11B and B/Ca, respectively). To address the potential for adaptive responses, both species were collected from two sites spanning a natural gradient in seawater pH and temperature, and then subjected to three pHT levels (8.04, 7.88, 7.71) crossed by two temperatures (control, +1.5°C) for 14 weeks. Corals from the site with naturally lower seawater pH calcified faster and maintained growth better under simulated OA than corals from the higher-pH site. This ability was consistently linked to higher pH yet lower DIC values in the calcifying fluid, suggesting that these differences are the result of long-term acclimatization and/or local adaptation to naturally lower seawater pH. Nevertheless, all corals elevated both pH and DIC significantly over seawater values, even under OA. This implies that high pH upregulation combined with moderate levels of DIC upregulation promote resistance and adaptive responses of coral calcification to OA.

Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia.

In 2015/16, a marine heatwave associated with a record El Niño led to the third global mass bleaching event documented to date. This event impacted coral reefs around the world, including in Western Australia (WA), although WA reefs had largely escaped bleaching during previous strong El Niño years. Coral health surveys were conducted during the austral summer of 2016 in four bioregions along the WA coast (~17 degrees of latitude), ranging from tropical to temperate locations. Here we report the first El Niño-related regional-scale mass bleaching event in WA. The heatwave primarily affected the macrotidal Kimberley region in northwest WA (~16°S), where 4.5-9.3 degree heating weeks (DHW) resulted in 56.6-80.6% bleaching, demonstrating that even heat-tolerant corals from naturally extreme, thermally variable reef environments are threatened by heatwaves. Some heat stress (2.4 DHW) and bleaching (<30%) also occurred at Rottnest Island (32°01'S), whereas coral communities at Ningaloo Reef (23°9'S) and Bremer Bay (34°25'S) were not impacted. The only other major mass bleaching in WA occurred during a strong La Niña event in 2010/11 and primarily affected reefs along the central-to-southern coast. This suggests that WA reefs are now at risk of severe bleaching during both El Niño and La Niña years.

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.

Microelectrode characterization of coral daytime interior pH and carbonate chemistry.

Reliably predicting how coral calcification may respond to ocean acidification and warming depends on our understanding of coral calcification mechanisms. However, the concentration and speciation of dissolved inorganic carbon (DIC) inside corals remain unclear, as only pH has been measured while a necessary second parameter to constrain carbonate chemistry has been missing. Here we report the first carbonate ion concentration ([CO3(2-)]) measurements together with pH inside corals during the light period. We observe sharp increases in [CO3(2-)] and pH from the gastric cavity to the calcifying fluid, confirming the existence of a proton (H(+)) pumping mechanism. We also show that corals can achieve a high aragonite saturation state (Ωarag) in the calcifying fluid by elevating pH while at the same time keeping [DIC] low. Such a mechanism may require less H(+)-pumping and energy for upregulating pH compared with the high [DIC] scenario and thus may allow corals to be more resistant to climate change related stressors.

Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: Understanding the unique host+symbiont response.

The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.

Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment.

Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.

Annual coral bleaching and the long-term recovery capacity of coral.

Mass bleaching events are predicted to occur annually later this century. Nevertheless, it remains unknown whether corals will be able to recover between annual bleaching events. Using a combined tank and field experiment, we simulated annual bleaching by exposing three Caribbean coral species (Porites divaricata, Porites astreoides and Orbicella faveolata) to elevated temperatures for 2.5 weeks in 2 consecutive years. The impact of annual bleaching stress on chlorophyll a, energy reserves, calcification, and tissue C and N isotopes was assessed immediately after the second bleaching and after both short- and long-term recovery on the reef (1.5 and 11 months, respectively). While P. divaricata and O. faveolata were able to recover from repeat bleaching within 1 year, P. astreoides experienced cumulative damage that prevented full recovery within this time frame, suggesting that repeat bleaching had diminished its recovery capacity. Specifically, P. astreoides was not able to recover protein and carbohydrate concentrations. As energy reserves promote bleaching resistance, failure to recover from annual bleaching within 1 year will likely result in the future demise of heat-sensitive coral species.

Perennial growth of hermatypic corals at Rottnest Island, Western Australia (32°S).

To assess the viability of high latitude environments as coral refugia, we report measurements of seasonal changes in seawater parameters (temperature, light, and carbonate chemistry) together with calcification rates for two coral species, Acropora yongei and Pocillopora damicornis from the southernmost geographical limit of these species at Salmon Bay, Rottnest Island (32°S) in Western Australia. Changes in buoyant weight were normalised to colony surface areas as determined from both X-ray computed tomography and geometric estimation. Extension rates for A. yongei averaged 51 ± 4 mm y(-1) and were comparable to rates reported for Acroporid coral at other tropical and high latitude locations. Mean rates of calcification for both A. yongei and P. damicornis in winter were comparable to both the preceding and following summers despite a mean seasonal temperature range of ∼6 °C (18.2°-24.3 °C) and more than two-fold changes in the intensity of downwelling light. Seasonal calcification rates for A. yongei (1.31-2.02 mg CaCO3 cm(-2) d(-1)) and P. damicornis (0.34-0.90 mg CaCO3 cm(-2) d(-1)) at Salmon Bay, Rottnest Island were comparable to rates from similar taxa in more tropical environments; however, they appeared to decline sharply once summer temperatures exceeded 23 °C. A coral bleaching event observed in December 2013 provided further evidence of how coral at Rottnest Island are still vulnerable to the deleterious effects of episodic warming despite its high latitude location. Thus, while corals at Rottnest Island can sustain robust year-round rates of coral growth, even over cool winter temperatures of 18°-19 °C, there may be limits on the extent that such environments can provide refuge against the longer term impacts of anthropogenic climate change.

Short-term coral bleaching is not recorded by skeletal boron isotopes.

Coral skeletal boron isotopes have been established as a proxy for seawater pH, yet it remains unclear if and how this proxy is affected by seawater temperature. Specifically, it has never been directly tested whether coral bleaching caused by high water temperatures influences coral boron isotopes. Here we report the results from a controlled bleaching experiment conducted on the Caribbean corals Porites divaricata, Porites astreoides, and Orbicella faveolata. Stable boron (δ11B), carbon (δ13C), oxygen (δ18O) isotopes, Sr/Ca, Mg/Ca, U/Ca, and Ba/Ca ratios, as well as chlorophyll a concentrations and calcification rates were measured on coral skeletal material corresponding to the period during and immediately after the elevated temperature treatment and again after 6 weeks of recovery on the reef. We show that under these conditions, coral bleaching did not affect the boron isotopic signature in any coral species tested, despite significant changes in coral physiology. This contradicts published findings from coral cores, where significant decreases in boron isotopes were interpreted as corresponding to times of known mass bleaching events. In contrast, δ13C and δ18O exhibited major enrichment corresponding to decreases in calcification rates associated with bleaching. Sr/Ca of bleached corals did not consistently record the 1.2°C difference in seawater temperature during the bleaching treatment, or alternatively show a consistent increase due to impaired photosynthesis and calcification. Mg/Ca, U/Ca, and Ba/Ca were affected by coral bleaching in some of the coral species, but the observed patterns could not be satisfactorily explained by temperature dependence or changes in coral physiology. This demonstrates that coral boron isotopes do not record short-term bleaching events, and therefore cannot be used as a proxy for past bleaching events. The robustness of coral boron isotopes to changes in coral physiology, however, suggests that reconstruction of seawater pH using boron isotopes should be uncompromised by short-term bleaching events.