pH variability at volcanic CO2 seeps regulates coral calcifying fluid chemistry.

Coral reefs are iconic ecosystems with immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification (OA). Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance in predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO2 seeps in Papua New Guinea to assess their capacity to control their calcifying fluid (CF) chemistry. Several coral species living under conditions of low mean seawater pH, but with either low or high variability in seawater pH, were examined and compared with those living in 'normal' (non-seep) ambient seawater pH. We show that when mean seawater pH is low but highly variable, corals have a greater ability to maintain constant pHcf in their CF, but this characteristic was not linked with changes in abundance. Within less variable low pH seawater, corals with limited reductions in pHcf at the seep sites compared with controls tended to be more abundant at the seep site than at the control site. However, this finding was strongly influenced by a single species (Montipora foliosa), which was able to maintain complete pHcf homeostasis. Overall, although our findings indicate that there might be an association between ecological success and greater pHcf homeostasis, further research with additional species and at more sites with differing seawater pH regimes is required to solidify inferences regarding coral ecological success under future 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.

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.

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.

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.

Active modulation of the calcifying fluid carbonate chemistry (δ11B, B/Ca) and seasonally invariant coral calcification at sub-tropical limits.

Coral calcification is dependent on both the supply of dissolved inorganic carbon (DIC) and the up-regulation of pH in the calcifying fluid (cf). Using geochemical proxies (δ11B, B/Ca, Sr/Ca, Li/Mg), we show seasonal changes in the pHcf and DICcf for Acropora yongei and Pocillopora damicornis growing in-situ at Rottnest Island (32°S) in Western Australia. Changes in pHcf range from 8.38 in summer to 8.60 in winter, while DICcf is 25 to 30% higher during summer compared to winter (×1.5 to ×2 seawater). Thus, both variables are up-regulated well above seawater values and are seasonally out of phase with one another. The net effect of this counter-cyclical behaviour between DICcf and pHcf is that the aragonite saturation state of the calcifying fluid (Ωcf) is elevated ~4 times above seawater values and is ~25 to 40% higher during winter compared to summer. Thus, these corals control the chemical composition of the calcifying fluid to help sustain near-constant year-round calcification rates, despite a seasonal seawater temperature range from just ~19° to 24 °C. The ability of corals to up-regulate Ωcf is a key mechanism to optimise biomineralization, and is thus critical for the future of coral calcification under high CO2 conditions.

Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation.

Coral calcification is dependent on the mutualistic partnership between endosymbiotic zooxanthellae and the coral host. Here, using newly developed geochemical proxies (δ11B and B/Ca), we show that Porites corals from natural reef environments exhibit a close (r2 ∼0.9) antithetic relationship between dissolved inorganic carbon (DIC) and pH of the corals' calcifying fluid (cf). The highest DICcf (∼ × 3.2 seawater) is found during summer, consistent with thermal/light enhancement of metabolically (zooxanthellae) derived carbon, while the highest pHcf (∼8.5) occurs in winter during periods of low DICcf (∼ × 2 seawater). These opposing changes in DICcf and pHcf are shown to maintain oversaturated but stable levels of carbonate saturation (Ωcf ∼ × 5 seawater), the key parameter controlling coral calcification. These findings are in marked contrast to artificial experiments and show that pHcf upregulation occurs largely independent of changes in seawater carbonate chemistry, and hence ocean acidification, but is highly vulnerable to thermally induced stress from global warming.

Coralline algae elevate pH at the site of calcification under ocean acidification.

Coralline algae provide important ecosystem services but are susceptible to the impacts of ocean acidification. However, the mechanisms are uncertain, and the magnitude is species specific. Here, we assess whether species-specific responses to ocean acidification of coralline algae are related to differences in pH at the site of calcification within the calcifying fluid/medium (pHcf ) using δ11 B as a proxy. Declines in δ11 B for all three species are consistent with shifts in δ11 B expected if B(OH)4- was incorporated during precipitation. In particular, the δ11 B ratio in Amphiroa anceps was too low to allow for reasonable pHcf values if B(OH)3 rather than B(OH)4- was directly incorporated from the calcifying fluid. This points towards δ11 B being a reliable proxy for pHcf for coralline algal calcite and that if B(OH)3 is present in detectable proportions, it can be attributed to secondary postincorporation transformation of B(OH)4- . We thus show that pHcf is elevated during calcification and that the extent is species specific. The net calcification of two species of coralline algae (Sporolithon durum, and Amphiroa anceps) declined under elevated CO2 , as did their pHcf . Neogoniolithon sp. had the highest pHcf , and most constant calcification rates, with the decrease in pHcf being » that of seawater pH in the treatments, demonstrating a control of coralline algae on carbonate chemistry at their site of calcification. The discovery that coralline algae upregulate pHcf under ocean acidification is physiologically important and should be included in future models involving calcification.

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.

Ocean acidification causes structural deformities in juvenile coral skeletons.

Rising atmospheric CO2 is causing the oceans to both warm and acidify, which could reduce the calcification rates of corals globally. Successful coral recruitment and high rates of juvenile calcification are critical to the replenishment and ultimate viability of coral reef ecosystems. Although elevated Pco2 (partial pressure of CO2) has been shown to reduce the skeletal weight of coral recruits, the structural changes caused by acidification during initial skeletal deposition are unknown. We show, using high-resolution three-dimensional x-ray microscopy, that ocean acidification (Pco2 ~900 µatm, pH ~7.7) not only causes reduced overall mineral deposition but also a deformed and porous skeletal structure in newly settled coral recruits. In contrast, elevated temperature (+3°C) had little effect on skeletal formation except to partially mitigate the effects of elevated Pco2. The striking structural deformities we observed show that new recruits are at significant risk, being unable to effectively build their skeletons in the Pco2 conditions predicted to occur for open ocean surface waters under a "business-as-usual" emissions scenario [RCP (representative concentration pathway) 8.5] by the year 2100.

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.

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.

Rapid, high-precision measurements of boron isotopic compositions in marine carbonates.

RATIONALE: The isotopic composition and elemental abundance of boron (B) in marine carbonates provide a powerful tool for tracking changes in seawater pH and carbonate chemistry. Progress in this field has, however, been hampered by the volatile nature of B, its persistent memory, and other uncertainties associated with conventional chemical extraction and mass spectrometric measurements. Here we show that for marine carbonates, these limitations can be overcome by using a simplified, low-blank, chemical extraction technique combined with robust multi-collector inductively couple plasma mass spectrometry (MC-ICPMS) methods. METHODS: Samples are dissolved in dilute HNO3 and loaded first onto on a cation-exchange column with the major cations (Ca, Mg, Sr, Na) being quantitatively retained while the B fraction is carried in the eluent. The eluent is then passed directly through an anion column ensuring that any residual anions, such as SO4(2-), are removed. Isotopic measurements of (11)B/(10)B ratios are undertaken by matching both the B concentration and the isotopic compositions of the samples with the bracketing standard, thereby minimising corrections for cross-contamination. RESULTS: The veracity of the MC-ICPMS procedure is demonstrated using a gravimetrically prepared laboratory standard, UWA24.7, relative to the international reference standard NIST SRM 951 (δ(11)B = 0‰). This gives values consistent with gravimetry (δ(11)B = 24.7 ± 0.3‰ 2sd) for solutions ranging in concentration from 50 to 500 ppb, equivalent to ~2-10 mg size coral samples. The overall integrity of the method for carbonate analysis is demonstrated by measurements of the international carbonate standard JCp-1 (δ(11)B = 24.3 ± 0.34‰ 2sd). CONCLUSIONS: A streamlined, integrated approach is described here that enables rapid, accurate, high-precision measurements of boron isotopic compositions and elemental abundances in commonly analysed biogenic carbonates, such as corals, bivalves, and large benthic forams. The overall simplicity of this robust approach should greatly facilitate the wider application of boron isotope geochemistry, especially to marine carbonates.