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or collective redistirbution other or collective or means this reposting, of machine, is bySociety, photocopy article only anypermitted of withSociety.Send portion theall approvalOceanographycorrespondence P to: [email protected] The of or Th e This article has been published in Oceanography published been This has article Special Issue Feature

By J oa n A . K l e y pa s

and Kimberly K. Yates , VolumeSociety. 4, a quarterlyOceanography 22, Number The journal of Reefs and Acidification © 2009 by The Oceanography Society.Oceanography A 2009 by The ll rights reserved. P reserved. ll rights ermission is granted to in teaching copy this and research. for use article R

Figure 1. Important calcifying organisms on coral reefs: (A) various -building on a Samoan reef, (B) coralline encrusting rock surfaces on a Samoan reef, (C) alga from Puerto Rico, (D) Penicillus algae, (E) reef composed of benthic from Warraber , Torres (average diameter of foraminifera grains is about 1 mm), and (F) from the US Virgin . Photo credits: A,B,C, Nathan Smiley; D, Matt Miller; E, Deirdre E. Hart; F, Chris DuFore O Box 1931, R O Box epublication, systemmatic reproduction, ockville, MD 20849-1931, U ockville, S A .

108 Oceanography Vol.22, No.4 Abstract. Coral reefs were one of the first to be recognized as future. It explores how ocean acidifica- vulnerable to . To date, most scientific investigations into the tion might affect systems at effects of ocean acidification on coral reefs have been related to the reefs’ unique multiple scales, from organism, to coral ability to produce voluminous amounts of carbonate. It has been estimated communities, to reef structure. Feely that the main reef-building organisms, corals and calcifying macroalgae, will calcify et al. (2009) provide a review of ocean 10–50% less relative to pre-industrial rates by the middle of this century. This acidification . decreased calcification is likely to affect their ability to function within the and will almost certainly affect the workings of the ecosystem itself. However, ocean Effects of Ocean acidification affects not only the organisms, but also the reefs they build. The decline Acidification on Reef in production, coupled with an increase in calcium carbonate Organisms dissolution, will diminish reef building and the benefits that reefs provide, such How do I affect thee? – as high structural complexity that supports on reefs, and Let me count the ways… effects that protect shorelines and create quiet for other ecosystems, such as and beds. The focus on calcification in reefs is warranted, but the Research on the effects of ocean acidifi- responses of many other organisms, such as , noncalcifying algae, and , cation on marine ecosystems continues to name a few, deserve a close look as well. to focus on calcifying organisms, and for good reason. Skeletal formation in Introduction ecosystem functioning does affect reef many organisms that secrete one of the In the 1970s and 1980s, research on coral building. Although reef building may various minerals of calcium carbonate reef ecosystems covered two, often sepa- not be essential to coral communities, (, , and high-magnesium rate, tracks: biological and geological. the reef structure provides services calcite) changes when exposed to

In fact, the Proceedings of the Third to the reef ecosystem by supporting elevated-CO2 conditions. On coral International Coral Reef Symposium1, the biodiversity and creating more surface reefs, the two main calcifying groups— outcome of a meeting held in , area to support the reef community. corals and calcifying macroalgae , in 1977, were cleanly separated These services are important, as is the (Figure 1A, B)—seem particularly sensi- into two volumes: “1. ” and reef function as a breakwater protecting tive to ocean acidification. However, “2. .” Over time, arguments shorelines and creating conditions that noncalcifying organisms on coral reefs about the definition of a coral reef promote other productive systems like will also be affected. It is difficult to (e.g., is reef building a necessary litmus mangroves and seagrass beds. predict the overall impact on coral reefs test for defining a coral reef ecosystem?) Coral reefs are the most widely recog- of some being “winners” and were reconciled in recognition that coral nized ecosystem threatened by ocean others “losers” in a progressively lower- reef ecosystems exist along a continuum, acidification. Changes in chem- pH ocean, but the loss of reef builders from nonreef-building coral ecosystems istry resulting from increased carbon threatens both the biological and geolog- to those that build massive, rapidly dioxide uptake by the ocean impede ical identities of this ecosystem. accumulating structures. Somewhere the basic function of calcium carbonate along that continuum lies a threshold production that is characteristic of many Reef Builders (Corals and between coral communities and coral reef organisms, and that provides the Calcifying Macroalgae) reefs, and across that threshold the coral foundation of coral reef structure. Ocean History communities may or may not func- acidification, therefore, impacts both the The pioneers in reef calcification studies tion similarly. It is not altogether clear biological and geological components have known for some time that calcifica- that the coral community depends on of coral reefs. This article summarizes tion by coral reef communities affects its own reef building. those impacts and provides a glimpse seawater chemistry (Smith and Pesret, What is clear, however, is that into what coral reefs may look like in the 1974; Smith and Key, 1975). Some of

1 The International Coral Reef Symposia have been held every four since 1969.

Oceanography December 2009 109 the early studies of “reef ” Unfortunately, this inference is differs (1) between species, (2) between used the anomaly technique— too simple because corals and other the life stages of species (note that a measure of the drawdown of alka- organisms exert energy to control their the mineralogy of the initial calcium linity over time due to of calcification, and because in most reef carbonate precipitated by larvae is some- calcium and carbonate ions as calcium organisms it is internal and isolated from times a rare, highly soluble form), and carbonate—to quantify calcification seawater. In corals, there is no evidence (3) in some species, between different rates of coral reef communities (Gattuso that carbonate ions are transported stages of calcification. et al., 1993; Kinsey, 1978, 1985; Smith from seawater to the site of calcifica- and Kinsey, 1978). The converse, that tion (McConnaughey et al., 2000), so Calcification seawater chemistry controls coral reef the carbonate ion must Despite our incomplete understanding of calcification rates, was slower to be affect calcification indirectly, or is simply the exact mechanisms that control calcifi- recognized (Smith and Buddemeier, a covariant of some other aspect of cation, decreased skeletal growth in reef- 1992). Some of the first studies to test the carbonate chemistry that controls calcifi- building corals and is one impact of ocean acidification on marine cation rate. Several studies have manipu- of the best-known consequences of ocean organisms were conducted on corals lated seawater chemistry by altering acidification (Figure 2). A wide range 2+ 2– – and coralline algae (Gattuso et al., 1998; of Ca , CO 3 , HCO 3, or of responses has been observed, but on Langdon et al., 2000). The 2 pH while holding the others constant in average, a doubling of pre-industrial studies, in particular, suggested that to tease out which component of atmospheric CO2 concentration results calcification rates of the coral/algal the carbonate system elicits a response in about a 10–50% decrease in the calci- community correlated best with arago- from corals. Those that manipulated fication rate of reef-building corals and nite saturation state (Ωar) (Langdon the calcium ion concentration (Gattuso coralline algae (Kleypas and Langdon, et al., 2000, 2003). This result agrees well et al., 1998; Marshall and Clode, 2002) 2006). The good news is the response is with geochemical studies that show that did cause a calcification response (note reversible (calcification will increase if precipitation rates of inorganic aragonite that marine aquarists are certainly acidification is reversed). The bad news is from seawater can be expressed by the aware that calcium supplements speed it is highly unlikely that ocean acidifica- n empirical equation R = k (Ωar – 1) , coral growth), and thus demonstrated tion can be reversed, and we don’t know where R is the rate of aragonite precipita- the impact of saturation state changes. yet whether corals and coralline algae tion, k is the rate constant, and n is the Ocean acidification, however, does not can adapt to these changes. order of the reaction (Burton and Walter, alter Ca2+ concentration, but rather pH Most studies have been conducted in 2– 1987). Because changes in Ωar correlate and the concentrations of CO2, CO 3 , the lab, under nonvarying conditions. – strongly with changes in carbonate ion and HCO 3. All of these change with This point is important because coral concentration, the natural inference ocean acidification, and each has been reef can naturally exhibit large is that the carbonate ion exerts direct shown to affect calcification either diurnal swings in pH (e.g., 7.9–8.1; Bates control on calcification rates of corals directly or indirectly. Several mecha- et al., 2001; Suzuki and Kawahata, 2003) and coral communities. nisms have been proposed to explain and other carbonate system parameters,

why changes in the CO2 system in and it is unclear whether the added Joan A. Kleypas ([email protected]) is a seawater affect calcification rate in corals. suppression of pH by 0.1–0.3 pH units research at the National Center Cohen and Holcomb (2009) show that projected for this century would have for Atmospheric Research, Climate and corals maintain a high saturation state a significant effect in environments Global Dynamics, , CO, USA. at the site of calcification, but at low where pH is highly variable. A recent Kimberly K. Yates is a research scientist pH this requires extra energy that they ocean acidification study that simulated with the US Geological Survey, Center don’t readily divert from other energy future variations in pH conditions in for Coastal and Watershed Studies, demands. Even within corals, however, accordance with natural variations on St. Petersburg, FL, USA. it is likely that the calcification process the adjacent reef (Jokiel et al., 2008;

110 Oceanography Vol.22, No.4 200 Jokiel et al., 2008). Once settled, however, 280 390 560 atmospheric pCO2 coral larvae reared in elevated-CO2 150 conditions experience depressed growth rates similar to those seen in adults -1

d (Albright et al., 2008; Cohen et al., 2009). -2 100 m 3 Ocean acidification has also been y = 34.1x - 58.7 shown to slow calcification rates in r 2 = 0.8 50 calcifying macroalgae, which have long

mmol CaCO been recognized as important compo- net calci cation nents of coral reef ecosystems. The 0 B2 Community Calci cation Rate net dissolution most common forms are coralline within the Rhodophyta -50 7 6 5 4 3 2 1 0 and calcifying green algae within the Ω arag phylum Chlorophyta. The coralline algae Figure 2. Changes in coral community calcification rate in the coral reef consist of both branching and mesocosm as a function of decreasing aragonite saturation state (Langdon et al., 2003). forms (many of which form unattached Atmospheric pCO2 levels that roughly correspond with the Ωar values are shown: 280 ppm = pre-industrial, 390 = present day, and 560 = 2X pre-industrial. Note that once living nodules called “rhodoliths”) that Ωar reached a value of 1.0–2.0, the coral community shifted from net calcification to net produce large quantities of high-Mg dissolution. Figure drawn from data provided by Chris Langdon calcite (the most soluble form of the common marine carbonate minerals). This group is extremely widespread Kuffner et al., 2008) showed that the 2000). There was no indication that coral in the ocean, existing from equato- calcification responses of corals and calcification rates had decreased, at least rial to polar regions (Nelson, 2009), coralline algae were similar to those in up to the 1987, which was the latest and to the deepest depths recorded for nonvarying conditions. age of the corals at the time of coring. If benthic photosynthetic species (Littler Calcification rates in scleractinian anything, the calcification signal corre- et al., 1985). Such a broad distribution corals (stony, or hard, corals) and calci- lated with more than any suggests that this group as a whole has fying macroalgae are not only affected other variable. Now, data from a new the evolutionary capacity to adapt to a by seawater carbonate chemistry, but by collection of coral cores from the Great wide range of conditions. Unfortunately, other variables such as temperature, light, Barrier Reef, which extends these records individual reef-building species seem and nutrients. Temperature has a particu- through 2005, indicate a 14% decline particularly vulnerable to dissolution larly strong effect, and small increases in calcification rates between 1990 and under increasing CO2 concentrations, in temperature can sometimes override 2005 (De’ath et al., 2009), which the with no demonstrated ability to adapt. the effects of ocean acidification, that authors attribute to excessive temperature Calcification rates of rhodoliths, for is, as long as the temperature increase increases, ocean acidification, or a combi- example, decreased by as much as 250% does not cause bleaching or otherwise nation of the two. (i.e., net dissolution) in mesocosms compromise coral physiology. When the The coral lifecycle includes more than with CO2 levels elevated by 365 ppm potential effects of ocean acidification adults, however, and ocean acidification over present-day conditions, and on coral calcification became apparent, could affect the larval stages of corals and successful recruitment by coralline algae looked through the archives of many other reef species. So far, ocean was diminished (Kuffner et al., 2008). cores taken from massive corals, acidification has not been shown to have Research on other tropical algae indi- mostly from the , to serious effects on coral gamete produc- cates that the calcium carbonate they see if calcification rates had changed over tion and recruitment, albeit the studies produce can dissolve under elevated- the past century (Lough and Barnes, have been few (Albright et al., 2008; CO2 conditions (Anthony et al., 2008).

Oceanography December 2009 111 A common coralline algae from the (Freile et al., 1995), and Halimeda banks et al., 2005; Kump et al., 2009), and Mediterranean , however, did not can be large and may be widespread on calcifying foraminifera went extinct at show a strong calcification response as tropical shelves (Milliman and Droxler, the - boundary (around long as the algae remained alive, and 1996). These structures provide impor- 250 million years ago) although the decreased calcification occurred only tant for many marine organisms. agglutinated forms did not (Knoll et al., when temperature was also elevated Although the effects of ocean acidifica- 2007). Note that these events (Martin and Gattuso, 2009). Nonetheless, tion on Halimeda and Penicillus have not also coincided with elevated tempera- where skeletons were exposed directly to been explicitly studied, multiple studies tures and , so it is difficult to seawater following death, dissolu- indicate that calcification in these genera discern which environmental change tion rates were two to four times faster is somewhat passive, being stimulated was the smoking gun. However, experi- in elevated-CO2 conditions. Dissolution by the photosynthetic removal of CO2 ments that exposed both and of exposed skeletons thus constitutes a from the intercellular spaces (de Beer noncalcareous benthic foraminifera to significant threat for this group, even if and Larkum, 2001; Ries, 2009). Thus, an high CO2 levels confirm that calcareous the algae can continue to calcify under increase in ambient CO2 concentration species are indeed sensitive to high high-CO2 conditions. At a field site near is likely to reduce the ability of these CO2 perturbations while noncalcareous a shallow CO2 vent in the species to calcify. species are not (Bernhard et al., 2009). Mediterranean, a suite of crustose coral- Mollusks are also important reef line algae species was absent near the Other Calcifying Organisms organisms, particularly the shelled forms vent (where average pH < 7.7), which on Reefs such as gastropods and giant clams. supports the findings of the laboratory Many calcifying taxa in addition to Ocean acidification research has focused experiments (Hall-Spencer et al., 2008; corals and calcifying macroalgae on pteropods, squid, and a variety of Martin et al., 2008). produce calcium carbonate skeletons, bivalves and gastropods; surprisingly, Coralline algae are known to be often in large quantities. Although the none of the studied species has been a favored substrate for settlement of effects of ocean acidification on some of from coral reefs. Based on existing coral larvae and their subsequent meta- these taxa have been investigated, rarely studies on nonreef-dwelling mollusks morphosis and growth (Heyward and have the studies focused on coral reef (Gazeau et al., 2007; Green et al., 2004; Negri, 1999). Thus, the reduction in the species. A brief summary of what we Miller et al., 2009; Talmage and Gobler, surface cover of crustose coralline algae know about ocean acidification on these 2009), it might be expected that some, may affect recruitment of other species. calcifying groups follows. but not all, species will produce thinner Similarly, the branching coralline alga Calcareous benthic foraminifera shells and/or suffer reduced recruitment

Amphiroa is known to induce settlement are important contributors to reef sedi- rates under elevated-CO2 conditions. of bivalve larvae (Williams et al., 2008); ments, sometimes producing the bulk of Many , including star- this is also considered sensitive to carbonate in shallower environ- fish (Figure 1F), brittle stars, sea urchins, ocean acidification as evidenced in the ments (Hohenegger, 2006; Figure 1E). sand dollars, , and holothurians, overall community response to ocean Data from previous ocean acidification have important functions in the reef. acidification in the Biosphere 2 coral reef events identified in the geologic record For example, the corallivorous crown- experiments (Langdon et al., 2000). (e.g., deep-sea cores) indicate of-thorns can strip a reef of The calcifying green algae in that calcifying benthic foraminifera most of its live coral tissue; the the genera Halimeda and Penicillus are vulnerable to ocean acidification. of many sea urchins keeps algal growth (Figure 1C, D) produce large volumes of Approximately 40% of benthic fora- in check; and echinoderms, in general, sand- and mud-sized , respec- minifera species went extinct at the are responsible for a large portion of tively, in reef environments. Measured Paleocene-Eocene Thermal Maximum global calcium carbonate (Lebrato

CaCO3 production rates of Halimeda (55 million years ago), which included a et al., in press). All echinoderms secrete meadows can exceed those of coral reefs strong ocean acidification event (Zachos high-Mg calcite skeletons (in the case

112 Oceanography Vol.22, No.4 of holothurians, the skeleton has been contribution of these taxa to carbonate from a state of reef building to one of reduced to small ossicles embedded production is small, their functioning reef destruction. in their tissues). Examination under a in the reef system could be impacted if Most reef fish have not been consid- polarizing microscope shows that each their ability to produce their shells or ered vulnerable to ocean acidification, skeletal component is composed of a skeletons is impaired. but one study looked at the effects of pH single crystal. The greater of changes on the chemosensory ability of the high-Mg calcite skeletons of echi- Noncalcifying Organisms larval clownfish to locate suitable habitat noderms, and their limited control on Many organisms on reefs are not calci- (Munday et al., 2009). Surprisingly, internal acid-base chemistry (Kurihara, fiers, yet their responses to ocean larvae subjected to lowered pH levels 2008; Miles et al., 2007), suggests that acidification can be quite important. appeared to lose their ability to distin- this group is highly vulnerable to ocean Seagrasses, for example, are widely guish between favorable (e.g., their acidification. This vulnerability appears recognized as potential winners with host anemones) and unfavorable to be the case in some species, but ocean acidification. Several studies (e.g., ) habitats. some echinoderms live on or within show that in nutrient-replete condi- sediments, and thus may be adapted tions, the growth of seagrasses increases Species Interactions and to lower-saturation-state conditions. significantly in elevated-CO2 condi- Ecosystem Shifts A temperate brittle star, for example, tions (Palacios and Zimmerman, 2007). A main concern about the effects of calcified more under elevated-CO2 Although seagrasses could potentially ocean acidification on coral reefs is that conditions although at the expense of expand on reef flats and displace corals it appears to affect many groups of reef other tissues (Wood et al., 2008), and a and other calcifiers, recent studies organisms, particularly corals and coral- temperate starfish fed more and grew indicate they could benefit calcifiers, line algae, the “ecosystem engineers” of faster (Gooding et al., 2009). as some coralline algae calcify faster reefs. The loss of these keystone species Within the phylum echinodermata, in the proximity of seagrasses, due to affects many other species associated ocean acidification studies have focused the drawdown of CO2 from the with them. When corals die in bleaching more extensively on larvae than on column (Semesi et al., 2009). Elevated events, the species that depend on them adults. Larval echinoderms produce CO2 may also stimulate growth in other are also impacted, and the effects trickle an amorphous phase of CaCO3 that noncalcifying macroalgae, such as was through the reef ecosystem. These is highly soluble (Politi et al., 2004). found in Porphyra yezoensis and two changes can degrade the reef’s resilience Larval development in most species Gracilaria species (Gao et al., 1991, (i.e., its ability to withstand disturbance) reared in elevated-CO2 conditions 1993), and particularly in algae that use even while it appears visibly healthy, until has been stunted, delayed, or even CO2 rather than bicarbonate for photo- at some point it can no longer sustain malformed (Clark et al., 2009; Kurihara synthesis, such as Lomentaria articulata even minor disturbances, and becomes and Shirayama, 2004). Genomic studies (Kübler et al., 1999). vulnerable to an ecological “,” on larvae of the purple One of the most interesting effects of that is, a rapid transition to a different revealed that gene expression in this ocean acidification concerns “euendo- ecosystem state (Figure 3). The classic species demonstrated a response not lithic” algae, that is, algae that bore into example of such a regime shift occurred only in biomineralization but also in reef skeletal material. At double CO2 on a Jamaican coral reef; it was driven by cellular stress response, metabolism, levels, these algae bore more deeply into the loss of both fish and sea and self-destruction of cells (Todgham skeletal material, dissolving nearly 50% urchin herbivores (through and Hofmann, 2009). more carbonate in the process (Tribollet and disease, respectively), which allowed Many other important taxa on reefs et al., 2009). If this response is universal the ungrazed macroalgae to overgrow produce CaCO3, such as some crusta- on reefs, then increased dissolution by the reef (Hughes, 1994). Other regime ceans, some worms, octoc- these little known but pervasive micro- shifts have been observed on coral reefs orals, and even soft corals. Although the scopic algae could alone push many reefs in (Hatcher, 1984) and in the

Oceanography December 2009 113 A

(e.g., reef building, grazing, filter feeding, Slime f sediment turnover) will collapse, leading to a regime shift. It is difficult to predict Heterotrophic e how future regime shifts will proceed, particularly because ocean acidification Macro algae c is occurring alongside other stressors like temperature increases and over- ‘Stressed’ b . Previous regime shifts on reefs were usually to ecosystems dominated Extra nutrients Sea urchin by macroalgae, but shifts to soft corals ‘Healthy’ or barren f and skeletonless relatives of reef-building reef a turf d Rock corals called corallimorpharians have also occurred (Norström et al., 2009). Fishing Reef Building B Reef building—the accumulation of Overfishing of herbivores calcium carbonate framework and sediments—is almost certain to change Extra nutrients in the future, because both carbonate production (almost entirely biogenic) is ‘Healthy’ likely to decrease, and its removal (via Overfishing of echinoid state mechanical transport of material off the predators reef and chemical dissolution) is likely Macro algae to increase. The severity of the impact state of ocean acidification on coral reefs will Sea urchin depend, in part, upon a delicate balance barren state among calcification, carbonate sediment Rock dissolution, and transport of sediment Figure 3. Regime shifts in coral reefs. (A) Conceptual model showing the effects of away from the reef. An important ques- overfishing and excess nutrients on reef state. With increasing fishing pressure and/or tion is whether reef growth will be able to nutrient , the coral community enters a stressed state with a loss of resilience sustain the reef structure, or rather shift and increased vulnerability to a rapid shift to a different state, such as an algal-domi- nated, sea-urchin-dominated system. (B) Diagram of how environmental changes enable to a state of . However, like inept transitions to new ecosystem states. The dotted lines illustrate the loss of resilience that accountants, most scientists concentrate increases the likelihood of shifting to a different state (redrawn with permission from on what goes into the reef and not on Macmillan Publishers Ltd: [Bellwood et al., 2004], © 2004). The exact effects of ocean acidification will be different than those imposed by pollution or overfishing, what is removed! Observed dissolution but the process of how diminishing resilience increases the likelihood of a regime rates on many reefs can be quite high shift is the same. (Yates and Halley, 2006), particularly in areas where high-Mg calcite is common,

and particularly at night, when CO2 eastern Pacific (Hunter and Evans, 1995) some will be winners (e.g., seagrasses), accumulates in the because and Indian (Graham et al., 2006). but the higher the proportion of species has ceased while respira- As ocean acidification proceeds, more that are affected (including winners and tion continues. In some areas where and more species will be affected. Some losers), the higher the probability that water mass residence time is relatively species will be losers (e.g., corals) and some major function of the ecosystem long (on the order of days as opposed to

114 Oceanography Vol.22, No.4 hours), sediment dissolution may buffer such as metabolic performance due dissolution rates. Reefs at higher lati- decreasing seawater pH and provide to community composition, seasonal tudes tend to be less well developed than some “relief” to calcifying organisms. variation in calcification and dissolution those in warmer, more tropical regions, However, most reefs are well flushed rates, variation in sediment composition, but even reefs in the warm tropics may with open ocean seawater and will degree of biologic control on calcifica- accumulate only slowly if, for example, not be afforded this type of protection tion and dissolution mechanisms, and they grow in turbid waters or if (Andersson et al., 2007). Furthermore, mixing rates of water masses overlying transport much of the excess carbonate loss of reef sediment may be exacer- substrate areas. As ocean acidifica- off the reef. bated for eroding reefs as lagoonal and tion proceeds, slow-growing reefs that Only a few studies have focused on other back-reef areas that are naturally already have a balanced carbonate determining pCO2 thresholds for coral protected by reef structure become budget will be the first to shift from reef communities that mark the critical exposed to higher wave energy, currents, a reef-building to a reef-erosion state point when rates of carbonate sediment and sediment transport. (Figure 4). In general, reefs at higher dissolution are equivalent to rates of The threshold where coral reefs shift latitudes have lower net growth rates calcification, and above which dissolu- from net production/accretion to net because the waters are colder, more tion exceeds calcification. Average pCO2 dissolution/erosion will vary greatly acidic, and perhaps because of shallower thresholds for reef communities in these from reef to reef. These variations light penetration in the winter (Kleypas studies ranged from approximately depend on a complex interplay of factors et al., 1999). They may also have higher 560–654 ppm (Yates and Halley, 2006;

Figure 4. Calculated changes in reef building for coral reefs worldwide at four different atmosphericp CO2 stabilization levels, based on the combined effects of predicted changes in saturation state and temperature on coral community calcification. The values are expressed as a T percentage of pre-industrial calcification rates (when atmospheric CO2 levels were 280 ppm); PIR = pre-industrial rate; Ggross = temperature- dependent gross calcification. Note that this calculation assumes constant coral cover = 50% (but see Silverman et al. [2009] for projections that include changes in coral cover). Reprinted from Silverman et al., 2009, with permission from the American Geophysical Union

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