LETTERS PUBLISHED ONLINE: 1 APRIL 2012 | DOI: 10.1038/NCLIMATE1473 Coral resilience to ocean acidification and global warming through pH up-regulation Malcolm McCulloch 1,2 * , Jim Falter 1,2 , Julie Trotter 1 and Paolo Montagna 3,4,5 Rapidly rising levels of atmospheric CO 2 are not only causing ocean warming, but also lowering seawater pH hence the carbonate saturation state of the oceans, on which many marine organisms depend to calcify their skeletons 1,2 . Using boron isotope systematics 3 , we show how scleractinian corals up-regulate pH at their site of calcification such that internal changes are approximately one-half of those in ambient sea- water. This species-dependent pH-buffering capacity enables aragonitic corals to raise the saturation state of their calcifying medium, thereby increasing calcification rates at little addi- tional energy cost. Using a model of pH regulation combined with abiotic calcification, we show that the enhanced kinetics of calcification owing to higher temperatures has the potential to counter the effects of ocean acidification. Up-regulation of pH, however, is not ubiquitous among calcifying organisms; those lacking this ability are likely to undergo severe declines in calcification as CO 2 levels increase. The capacity to up-regulate pH is thus central to the resilience of calcifiers to ocean acidi- fication, although the fate of zooxanthellate corals ultimately depends on the ability of both the photosymbionts and coral host to adapt to rapidly increasing ocean temperatures 4 . The response of calcifying organisms to the accelerating effects of declining seawater pH and increasing ocean temperatures is still poorly constrained 5 . Some studies 2,6 of warm-water zooxanthellae- bearing corals show a high degree of sensitivity to declining seawater pH. This has led to predictions of major reductions in coral calcification at atmospheric CO 2 levels (p CO2 ) of ∼450 μatm (ref. 7) and, with the additional effects of global warming, the demise of coral reefs at ∼560 μatm (ref. 8). However, other studies 2,9–11 indicate a much lower range of coral sensitivities and thus predict less dramatic changes in calcification rates over the probable range of future p CO2 scenarios. Uncertainties in the response of biogenic calcifiers to the combined effects of climate change and ocean acidification arise, not only from inherent limitations in experiments attempting to simulate the impacts of high p CO2 , but also from the lack of a well-constrained physiologically based understanding of the links between calcification, seawater carbonate chemistry and rapidly changing thermal regimes. Here we present a new approach that effectively quantifies the response of calcification in corals and some other key biogenic calcifiers to ocean acidification and rising ocean temperatures, assuming that they are able to continue to operate within their thermal tolerance 4 . Biogenic calcification occurs within a physiologically controlled environment 12–14 , with scleractinian corals precipitating their cal- cium carbonate (CaCO 3 ) skeleton from an extracellular calcifying 1 The UWA Oceans Institute and School of Earth and Environment, University of Western Australia, Crawley, Western Australia 6009, Australia, 2 ARC Centre of Excellence for Coral Reef Studies, University of Western Australia, Crawley, Western Australia 6009, Australia, 3 Laboratoire des Sciences du Climat et de l’Environnement, Av. de la Terrasse, 91198, Gif-sur-Yvette, France, 4 Institute of Marine Sciences, Bologna 40129, Italy, 5 Lamont Doherty Earth Observatory of Columbia University, 61 Route 9W, Palisades, New York 10964, USA. *e-mail:malcolm.mcculloch@uwa.edu.au. ΔpH = 0 Porites spp. (y = 0.32x + 5.95, r 2 = 0.99) A. nobilis (y = 0.50x + 4.40, r 2 = 0.99) Acropora spp. (y = 0.51x + 4.28) Forams C. caespitosa (y = 0.47x + 4.87, r 2 = 0.89) Seawater pH Calcifying fluid pH P. cylindrica (y = 0.46x + 4.72, r 2 = 0.99) S. pistillata (y = 0.30x + 6.05, r 2 = 0.99) 9.0 8.8 8.6 8.4 8.2 8.0 7.8 7.0 7.2 7.4 7.6 7.8 8.0 8.2 8.4 A V Figure 1 | Plot of pH T relative to pH cf , determined from boron isotope systematics 3 (see Supplementary Information) of aragonitic corals and calcitic foraminifera 17 . At pH T of 8.1, the temperate coral Cladocora caespitosa exhibits the greatest increase in pH cf with pH ∼ 0.5 (pH = pH cf − pH T ), whereas the tropical corals Porites spp., P. cylindrica, Stylophora pistillata, Acropora spp. and A. nobilis have lower pH ∼ 0.3 to ∼0.4 (ref. 3). In contrast, the calcitic foraminifera 17 (shown in blue) lie on or near the abiotic line with pH ∼ 0. Ellipses show pH cf values measured over daily cycles using microelectrodes (A; ref. 12) and pH-sensitive dyes (V; ref. 15), broadly consistent with the longer duration (weeks to month) represented by boron measurements. fluid located in the semi-isolated space 12–14 between the skeleton and the calicoblastic ectoderm. During active calcification, the pH of the calcifying fluid (pH cf ) is often increased 12,15 relative to ambient (that is, external) seawater pH, resulting in the equilibrium composition of dissolved inorganic carbon (DIC) being shifted in favour of CO 3 2− relative to HCO 3 − , thus promoting the reaction Ca 2+ + CO 3 2− ↔ CaCO 3 . Using boron isotope systematics, it has recently been shown 3 (Fig. 1) that corals systematically increase their pH cf over a wide range of seawater pH following highly correlated (r 2 = 0.99) linear arrays, which are approximately sub- parallel for different species. Thus, at a typical seawater pH of ∼8.1 (total scale: pH T ), the pH cf of aragonitic corals shows a species-dependent range from 8.4 to 8.7 (Fig. 1), representing a systematic increase in pH cf relative to ambient sea water (pH) of ∼0.3–0.6 units. NATURE CLIMATE CHANGE | VOL 2 | AUGUST 2012 | www.nature.com/natureclimatechange 623 © 2012 Macmillan Publishers Limited. All rights reserved.