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ICES Journal of Marine Science ICES Journal of Marine Science (2016), 73(3), 550– 557. doi:10.1093/icesjms/fsv091 Contribution to Special Issue: ‘Towards a Broader Perspective on Ocean Acidification Research’ Food for Thought Predicting the impact of ocean acidification on coral reefs: evaluating the assumptions involved Paul L. Jokiel* Hawaii Institute of Marine Biology, PO Box 1346, Kaneohe, HI 96744, USA *Corresponding author: e-mail: [email protected] Jokiel, P. L. Predicting the impact of ocean acidification on coral reefs: evaluating the assumptions involved. – ICES Journal of Marine Science, 73: 550 – 557. Received 7 March 2015; revised 21 April 2015; accepted 22 April 2015; advance access publication 21 May 2015. Predictions of future impact of climate change on coral reefs indicate that bleaching mortality due to higher temperature will be the major factor in the decline of coral reefs. Ocean acidification (OA) is increasingly considered to be an important contributing factor, but estimates of its importance vary widely in the literature. Models of future reef decline due to OA generally involve four simplifying assumptions that can lead to contradictions. The assumptions are: (i) Oceanic conditions of Varag control or are at least highly correlated with net calcification rate (Gnet) on coral reefs. (ii) Calcification rate is driven by bulk water carbonate ion concentration [CO3 2− ] expressed as Varag. (iii) Changes in coral calcification rate can be used to estimate future changes in coral reef calcification rate. (iv) The impact of OA is additive and not synergistic with other environmental factors such as increased temperature. The assumption that aragonite saturation state (Varag) of seawater drives calcification is the most widely used and needs to be further evaluated. An alternate hypothesis is that calcification is limited by the ability of the system to rid itself of the protons generated by calcification. Recent studies allow further testing of the assumptions and point the way to resolving shortcomings in our understanding of how OA impacts coral reefs. Keywords: climate change, corals, coral reefs, mathematical models, ocean acidification, proton flux. Introduction During 1999, three important publications established the potential seriousness of future anthropogenic global climate change and laid the basis for predictive modelling efforts. Kleypas et al. (1999) proposed that coral reef calcification rate depends on the aragonite saturation state (Varag) of oceanic surface waters based on the correlation between current coral reef distribution and Varag of the surrounding ocean waters. Gattuso et al. (1999) reviewed the potential effect of global climatic changes (pCO2 and temperature) on the rate of calcification in marine organisms and showed that the rate of calcification in various calcifying photosynthetic organisms decreases as a function of increasing pCO2 and decreasing Varag. Their calculated decrease in CaCO3 production due to ocean acidification (OA), estimated using the scenarios considered by the International Panel on Climate Change (IPCC), was 10% between 1880 and 1990, and 9 –30% from 1990 to 2100. Hoegh-Guldberg (1999) presented a model of future coral reef demise based largely on modelled climate change temperature projections and coral mortality due to the higher temperature regimes, with additional decline resulting from projected changes in seawater Varag. The saturation state concept is widely used by physical chemists in describing seawater carbonate chemistry. The concept is especially attractive in relation to biological calcification on coral reefs because aragonite is the mineral form of CaCO3 precipitated by reef corals. Aragonite saturation state (Varag) is defined by the equation: Varag = [Ca2+ ][CO3 2− ] , Ksp where Ksp is the solubility product of aragonite. The [Ca2+] in presentday oceanic seawater is essentially constant at 10.3 mmol kg21 SW, normalized to salinity. Likewise, Ksp is a constant (at a given temperature, pressure, and salinity), so Varag is directly proportional to [CO3 2− ] in shallow oceanic waters. Therefore Varag is essentially a function of the change in [CO3 2− ] on coral reefs. A correlation between Varag and calcification rate does not establish cause and # International Council for the Exploration of the Sea 2015. All rights reserved. For Permissions, please email: [email protected] 551 Predicting the impact of ocean acidification on coral reefs effect because Varag also correlates with various other components of the seawater carbonate system. Nevertheless, nearly all the literature on effects of past, present, and future impact of OA on coral growth present Varag or [CO3 2− ] as the independent variable and coral calcification rate as the dependent variable, leading to the widely held paradigm that [CO3 2− ] drives calcification (Erez et al., 2011). Therefore, the idea that [CO3 2− ] drives coral and coral reef calcification is a central feature of most mathematical model projections of future climate change on coral reefs and calcification is frequently presented as a function of Varag. Mathematical modelling is the process of applying mathematics to a real world problem as a means of gaining understanding of a process such as increasing global OA. The modelling process can shed light on the questions under investigation and thereby stimulate further inquiry, but assumptions used in developing models need to be evaluated whenever conflicting results arise. Models describing impact of OA on corals and coral reefs Two major types of modelling have been conducted on the question of global impact of OA on corals and coral reefs. The first is essentially a metadata analysis of published data showing response of calcification to changes in Varag. The second category includes various numerical models based on coral or coral reef response to changes in Varag as well as increased temperature. about the future of coral reefs as well as the basic assumptions and data manipulations involved in the analysis. Pandolfi et al. (2011) further expanded the analysis of Langdon and Atkinson (2005) using similar techniques. This synthesis included results of seven CO2 experiments at ambient temperature, three CO2 experiments at elevated temperature, seven experiments using different combinations of acid and base to manipulate Varag, along with two studies using field data. The response of calcification to decreasing Varag was consistently negative among individual coral species, coral mesocosms, and in situ reef communities. Results were found to be highly variable and often non-linear. Calcification was strongly sensitive to Varag in some experiments. In other experiments, calcification did not change significantly even where corals were exposed to CO2 levels between two and three times greater than preindustrial concentrations. In some cases, calcification did not decline when held at below the aragonite saturation threshold (Varag ¼ 1). In a few instances, calcification even increased under moderately reduced Varag. This series of three progressively larger metadata analyses based on the relationship between Varag and calcification rate reinforced the idea that a linear equation can be used to describe the relationship between Varag and calcification on a global basis. However, the resulting linear model parameters thus derived are of little predictive value on any given coral reef and are of dubious value in predicting global changes in corals and coral reefs in general. Nevertheless, this analysis does make the point that increasing OA is generally detrimental to coral and coral reef calcification rate. Metadata models Gattuso et al. (1999) was the first paper to model impact of OA on coral reefs. They compiled calcification vs. Varag data on four datasets on temperate and tropical coralline algae, two datasets on scleractinian corals and one on a coral reef community. Six of 7 datasets clearly showed a linear or curvilinear decrease in the rate of calcification as a function of decreasing Varag over the range 0 –6.2. Using scenarios developed by the IPCC, the equations were used to describe historical and possible future changes in calcification due to climate change. Decreases in CaCO3 production were calculated as 10% between 1880 and 1990, and 9 –30% (mid-estimate: 22%) from 1990 to 2100. This model used the assumption that calcification is a function of Varag. Also, changes in reef pCO2 were assumed to be directly related to atmospheric pCO2 as estimated by IPCC scenarios. The model addressed changes in calcification for organisms and did not consider net calcification rates for reefs, which is a more complex question. Langdon and Atkinson (2005) expanded the work of Gattuso et al. (1999) to include results of 13 investigations on corals and coral reef systems. They proposed that calcification rate is controlled by a rate law with calcification being proportional to (Varag 21)n. The experimental data from the various sources were too scattered to fit the model directly so they normalized the data. Rates of calcification were calculated from each experiment were calculated as a percentage of an extrapolated Varag of 4.6, which is their estimated saturation state of the tropical ocean in 1880 when atmospheric pCO2 was 280 ppm based on the report of Kleypas et al. (1999). The resulting plot still showed considerable scatter. The points fell between a line predicted by the linear first-order rate (n ¼ 1) the second curvilinear second-order rate (n ¼ 2). These points are said to predict a decrease of 60% in coral and coral reef calcification by the year 2065. Another set of points that show an insensitivity to Varag fell outside of this region and was said to predict a decline of only 1 –18% by 2065. These findings leave a great deal of uncertainty Numerical models Buddemeier et al. (2008) developed a spreadsheet-based numerical model that calculates the effects of climate change on coral reefs at local-to-regional scales using equations developed from data on coral growth and mortality rates. The model calculates the impacts to coral cover from changes in average sea surface temperature (SST) and Varag, and from high-temperature mortality (bleaching) events. The model uses a probabilistic assessment of the frequency of high-temperature events under future climate scenarios to address scientific uncertainties about potential adverse effects. Further, the model demonstrates the relative importance of high-temperature events, increased average temperature, and increased CO2 concentration on the future status of coral reefs. The Buddemeier et al. (2008) model allows comparisons of past environmental history with predictions. Coral growth in this model was controlled by Varag and the focus was on coral coverage rather than net ecosystem calcification. Silverman et al. (2009) made projections of global changes on coral reefs using a model parameterized by field studies of calcification’s response to medium-term (2-year) fluctuations in calcification and Varag and concluded that most of the world’s reefs will be compromised once atmospheric CO2 reaches 560 ppm. This is based on an empirical rate law developed from field observations for gross community calcification as a function of (Varag), SST, and live coral cover. Calcification rates were calculated for .9000 reef locations using model values of Varag and SST at different concentrations of atmospheric CO2. The model predicted that when the atmospheric partial pressure of CO2 reaches 560 ppm all coral reefs will cease to grow and start to dissolve. Evenhuis et al. (2015) developed a unified model that linked increased temperature and OA to coral reef condition. Changes were modelled by linking the rates of growth, recovery, and calcification to the rates of bleaching and temperature induced mortality 552 for corals. The model has novel aspects including use of is the Arrhenius equation, thermal specialization, resource allocation trade-offs, and adaption to local environments. The model was constructed using a range of experimental and observational data, but assumes that response of corals to Varag can give a reasonable estimate for future impact of OA. Major assumptions of the models The models described above have employed simplifying assumptions. Recent findings have shown that in some cases OA model results do not agree with field and laboratory observations (e.g. Jury et al., 2010; Pandolfi et al., 2011; Shamberger et al., 2011, 2014; Comeau et al., 2012; Roleda et al., 2012). Such contradictions give us new insight into the processes controlling response of coral reefs to OA and allow us to review some of the basic concepts. This is precisely the purpose of modelling, so it is appropriate to revisit and re-evaluate basic assumptions involved. Four major assumptions are listed and evaluated as follows: Assumption 1: Oceanic conditions of Varag control or are at least highly correlated with net calcification rate (Gnet) on coral reefs. The concept that open-ocean Varag controls Gnet and thus coral reef development was carried forward by many investigators as described above. More recently however, Duarte et al. (2013) pointed out that metabolism in inshore waters such as coral reefs results in strong diel to seasonal fluctuations in pH with characteristic ranges of 0.3 pH units or more over a diurnal cycle. Ohde and van Woesik (1999) in their Table 3 showed that pH varied 0.7 pH trough a diurnal cycle (1 d from 8.6 to 7.9; on another day from 8.4 to 7.8). Such extreme variability and presence of multiple, complex metabolic controls on coral reefs suggest that changes in the open-ocean Varag cannot be transposed to coastal ecosystems directly. Hence, Duarte et al. (2013) contend that OA from anthropogenic CO2 is largely an open-ocean syndrome. This concept has been further supported by the work of Cyronak et al. (2014) who showed biogeochemical processes can influence the pCO2 and pH of coastal ecosystems on diel and seasonal time scales, potentially modifying the long-term predicted effects of increasing atmospheric CO2. By compiling data from the literature and removing the effects of short-term variability, they showed that the average pCO2 of coral reefs throughout the globe has increased 3.5-fold faster than in the open ocean over the past 20 years. This rapid increase in coastal and reef pCO2 has the potential to negate the results of models that calculate the predicted effects of OA on coral reef ecosystems based on oceanic Varag. They constructed a model to demonstrate that potential drivers of elevated pCO2 include additional anthropogenic disturbances such as enhanced nutrient and organic matter inputs. P. L. Jokiel from reef to reef depending on differences in the primary factors controlling both calcification and Varag. The calcification rate of reefs is driven largely by photosynthetic rate of the calcifying component and limited by proton efflux from the corals (Jokiel et al., 2014). Photosynthetic rate of a reef community changes with available irradiance and other factors such as community composition, nutrient, water motion, herbivore grazing, etc. If Gnet is measured using the alkalinity depletion method (Kinsey 1978; Smith and Kinsey 1978) the result is greatly modified by dissolution rate of carbonates and changes in pH due to photosynthesis and other factors (Jokiel et al., 2014; Murillo et al., 2014). Thus, we find no consistent relationship between Gnet and Varag on different reefs. Figure 1 presents the results of four field investigations on coral reefs from different parts of the world. There is a lack of consistency in the relationship between Varag and Gnet for different reefs. The reef with lowest Varag shows the highest Gnet. Regression line slopes between Varag and Gnet are generally positive, but the positive slope observed that had been observed during summer at Ningaloo Reef did not occur in winter at the same location. Chan and Connolly (2013) pointed out that the number of experimental studies seeking to estimate the sensitivity of Gnet to Varag has increased dramatically in recent years, but the magnitude of the calcification response estimated in these studies has varied enormously, ranging from an increase in 25% to a decrease in 66%, per unit decrease in Varag. Rodolfo-Metalpa et al. (2015) provide laboratory evidence that Gnet of three common cold-water corals is not affected by pCO2 levels expected for 2100 (pCO2 1058 matm, Varag 1.29). A field transplant experiment with one of the species to 350 m depth (pHT 8.02; pCO2 448 matm, Varag 2.58) and to a 3 m depth CO2 seep in oligotrophic waters (pHT 7.35; pCO2 2879 matm, Varag 0.76) showed that the transplants calcified at the same rates. The data suggest that OA will not disrupt cold-water coral calcification, although falling Varag may affect other organismal physiological and/or reef community processes. Assumption 2: Calcification rate is driven by bulk water carbonate ion concentration [CO3 2− ] expressed as Varag. This assumption appears flawed. Carbonate ion concentration (and thus Varag) of bulk water in laboratory incubations and in field flow metabolism experiments increases with increasing calcification rate, so carbonate ion concentration (or Varag) cannot be limiting calcification (Jokiel et al. 2014). Aragonite saturation state lags behind calcification by 2 h over the diurnal cycle (Shamberger et al., 2011; McMahon et al., 2013; Jokiel et al., 2014) and therefore cannot be driving calcification. However, there is a correlation between Varag and Gnet. The slope and intercept of the correlation varies Figure 1. Plot of net calcification rate Gnet vs. Varag from four studies of calcification conducted in the field: Shamberger et al. (2011), Kaneohe Bay, Hawaii (solid squares); Ohde and van Woesik (1999), Rukan-sho, Japan (solid triangles); Silverman et al. (2007), Eilat Israel (open circles); Falter et al. (2012), Nigaloo Reef, Western Australia summer (open diamonds) and winter (solid diamonds). 553 Predicting the impact of ocean acidification on coral reefs Asumption 3: Changes in coral calcification rate can be used to estimate future changes in coral reef calcification rate. This assumption is questionable because corals can continue to grow relatively well at levels of OA that result in net dissolution of a coral reef (Andersson et al., 2009). A related issue is that growth of corals under various conditions of OA is generally measured directly by change in weight or linear extension (Jokiel et al., 1978), whereas reef calcification is generally measured by the alkalinity depletion method (Kinsey, 1978, Smith and Kinsey, 1978). The alkalinity depletion method measures Gnet and can include a substantial contribution of total alkalinity (AT) from dissolving carbonate sediment and rocks (Murillo et al., 2014) as well as contributions from other components such as macroalgae, crustose coralline algae, sediment diagenesis, etc. Important reef calcifiers such as crustose coralline algae (CCA) are far more sensitive to OA condition than corals and can be dissolving on a reef at OA levels that still allow substantial coral growth (Jokiel et al., 2008; Kuffner et al., 2008). There are many reefs in the world that are dominated by CCA, with a very small component of live coral. Secondary calcification, bioerosion, and reef dissolution are integral to the structural complexity and long-term persistence of coral reefs, yet these processes have received less research attention than reef accretion by corals. Silbiger and Donahue (2015) found that secondary reef calcification and dissolution responded differently to possible future conditions of global warming and increasing OA. Calcification showed a non-linear response to the combined effect of increased pCO2 and increased temperature while dissolution increased linearly, leading to the conclusion that dissolution may be more sensitive to climate change than calcification. Comeau et al. (2014) tested impact of OA on coral reef communities with associated sediments and sediments alone maintained in outdoor flumes under ambient pCO2 vs. high pCO2 at various flow rates. Calcification correlated positively with flow and negatively to increased pCO2 with a substantial dissolution component due to the presence of sediment. Assumption 4: The impact of ocean acidification is additive and not synergistic with other environmental factors. Existing models assume that future reduction in reef coral cover due to elevated temperature (lower growth and high mortality) and OA (lower growth) are simply additive (Hoegh-Guldberg et al. (2007), but more recent reports have demonstrated antagonisms and synergisms. Reynaud et al. (2003) grew small colonies of the reef coral Stylophora pistillata in a matrix of two temperature treatments (25 vs. 288C) and two pCO2 treatments (460 vs. 750 matm) and report no statistical difference between pCO2 treatments at 258C, but a large decline in calcification of 50% at 288C under acidified conditions. Anlauf et al. (2011) studied the effects of a 18C increase in temperature and a 0.2 –0.25 unit decrease in pH on the growth of primary polyps in the coral Porites panamensis. The growth of polyps was reduced marginally by acidic seawater but the combined effect of higher temperature and lowered pH caused a significant growth reduction of 30%. A similar 30% decline at higher temperature—elevated pCO2 was shown by Edmunds et al. (2012) for the rapidly growing branched coral Porites rus, but a slower growing massive Porites sp. did not show the effect. The temperature – pCO2 interaction has been observed in other calcifying reef organisms. Martin and Gattuso (2009) observed an interaction effect between temperature and pCO2 on the coralline alga Lithophyllum cabiochae. Algae were maintained in aquaria for 1 year at ambient or elevated temperature (+38C) and at ambient pCO2 (400 matm) or elevated pCO2 (700 matm). During summer the net calcification of the algae decreased by 50% when both temperature and pCO2 were elevated whereas no effect was found under elevated temperature or elevated pCO2 alone. Questioning the assumptions The assumption that Varag (or its surrogate [CO3 2− ]) drives Gnet has been challenged by a series of publications (Jokiel, 2011a, b , 2013, Jokiel et al., 2014; Cyronak et al., 2016). These papers argue that calcification is not limited by [CO3 2− ] but rather by the ability to dissipate excess protons generated by the calcification process. Various contradictions and inconsistencies in the calcification literature are resolved by the proposed proton flux model (Jokiel, 2011a, b). Recent observations have challenged paradigm that Varag controls Gnet. For example the presence of rich coral reefs in Kāne‘ohe Bay, Hawai‘i existing at low Varag (high pCO2 levels) as shown in Figure 1. The elevated pCO2 is due to metabolism of terrigenous organic material transported into the bay by streams. Fagan and Mackenzie (2007) found that pCO2 was averaging 500 matm. Silverman et al. (2009) estimated that “by the time atmospheric partial pressure of CO2 will reach 560 ppm all coral reefs will cease to grow and start to dissolve”, yet these reefs are flourishing. Several reports have shown that Varag lags behind Gnet by 2 h over the diurnal cycle (Shamberger et al., 2011; McMahon et al., 2013; Jokiel et al., 2014) which means that Varag is not driving Gnet. Testing assumptions using exemplary data from the Rock Islands, Palau Shamberger et al. (2014) reported the existence of highly diverse, coral-dominated reef communities under chronically low pH and low Varag in the Rock Islands of Palau, affording an opportunity to test the validity of several of the above assumptions and provide additional explanations. Their comparison was made between sites located in the open ocean at (1 –3 km offshore) with sites located in a shallow flow-restricted lagoon located at a distance of 7 –9 km from open-ocean waters (Figure 2). The Rock Islands are located in the south lagoon of Palau between Koror and Peleliu. This area is an uplifted ancient coral reef that forms a complex carbonate labyrinth of shallow channels and lagoons containing 250– 300 small islands, which are actually carbonate reef outcrops. Some of the islands display a mushroom shape with a narrow base created by rapid dissolution and bioerosion by sponges and bivalves and intense grazing by chitons, urchins, and fish in the intertidal (Lowenstam, 1974; Glynn, 1997). The extreme bioerosion and carbonate dissolution in the area coupled with very low rates of seawater exchange (Golbuu et al., 2012) produces atypical conditions on the reef. Measurements made in the Rock Islands showed extremely low Varag (2.4) and low pH (7.8) in this area of high coral coverage compared with high Varag (3.8) and high pH (8.1) in the offshore area. An analysis of the dynamic benthic processes involved in coral calcification on the Rock Island reefs can be made with the reported data for [AT], [DIC], and [H+]. The analysis requires that we accept the assumptions implicit in the experimental design that horizontal mixing is uniform throughout the area of study and that [AT], [DIC], and [H+] are not greatly modified by pelagic processes in relation to benthic processes. The environmental gradient between the lagoon stations and offshore stations is shown for [AT] (Figure 2a), 554 P. L. Jokiel [DIC] (Figure. 2b), and [H+] (Figure 2c). The strongest gradient (p , 0.001, Figure 2c) is for net flux of protons out of the lagoon. Net flux of AT into the lagoon also shows a strong gradient (p , 0.001, Figure 2a). Net DIC flux into the lagoon did not show a statistically significant correlation (p ¼ 0.089, Figure 2b). This pattern is consistent with detailed observations made by Jokiel et al. (2014) showing the lag in proton flux in a rapidly calcifying system. Dissipation of the protons generated by the process of calcification is a major factor limiting coral growth. Flushing of the Rock Island system with oceanic waters removes H+ and brings in water with higher [AT]. DIC is abundant in seawater and is not limiting. Proton flux is the important parameter as shown by changes in [AT] and [H+] with distance from the open ocean. An explanation for the presence of this rich coral reef growing under low Varag can be developed based on the proton flux hypothesis (Jokiel, 2011a). Dissolution of carbonates increases AT (Wisshak et al., 2013), especially under low pH conditions at night. Such additional AT will be retained in the system due to low water exchange and made available to the calcifying organisms during the day. High rainfall and tidal variation results in submarine groundwater discharge (SGD), which serves as another source of AT to the calcifying organisms. Furthermore, rainfall in this area is high and varies from 200 to 450 mm month21 (Australian Bureau of Meteorology and CSIRO, 2011). Cyronak et al. (2013a, b) measured increased AT flux due to SGD with the daily flux rate of up to 1080 mmol m22 d21. Dissolution of the complex non-living carbonates supplemented with additional AT from SGD in the low-flushing Rock Island reef system over the 24 h period would provide considerable AT buffering of the protons being generated by calcification. Supplementary Figure S4 of the Shamberger et al. (2014) report shows a rich coral community at the Rock Islands lacking in macroalgae and turf algae, probably due to intense herbivore grazing pressure and low inorganic nutrient supply. Presence of a larger macroalgae component would have increased pH during daylight hours without altering AT. The higher pH in such situations shifts the equilibria toward increased [CO3 2− ] and therefore higher Varag. In this system, as in other systems, Varag simply describes the portion of DIC that is being expressed as CO3 2− under prevailing pH conditions (which can be modified to different degrees by algal photosynthesis without changing AT) and thus is not of value as a universal metric driving coral calcification. There is a local correlation between Varag and Gnet, but Varag is a dependent variable on several factors including Pnet and local dissolution rate of carbonates (e.g. Murillo et al., 2014). The relationship of Gnet to Varag relationship holds within a given system, but varies between systems due to differences in Pnet, which drives Gnet. Systems with a higher portion of Pnet being provided by non-calcifying photosynthetic organisms will have a different relationship to Varag than a system dominated by calcifying photosynthetic organisms. Further evaluation of existing models and methodology Figure 2. Change in water chemistry from open ocean to coral lagoon using data from Shamberger et al. (2014) for: (a) total alkalinity, (b) dissolved inorganic carbon, and (c) proton concentration. Jones et al. (2015) evaluated four published models of reef carbonate production in terms of their predictive power at local and global scales. The models are based on functions sensitive to combinations of light availability Varag and temperature and were implemented within a specifically developed global framework, the Global Reef Accretion Model. None of the models reproduced the independent 555 Predicting the impact of ocean acidification on coral reefs rate estimates of whole-reef calcification. The output from the temperature-only based approach was the only model to significantly correlate with coral calcification rates. They pointed out that validation of reef carbonate budgets is severely hampered by limited and inconsistent methodology in reef-scale observations. Pandolfi et al. (2011) detected striking inconsistencies between experimental and field observations of the Varag vs. calcification relationship and suggested that the role of dissolution could account for the differences. Tribollet et al. (2009) found that carbonate dissolution by microbial endoliths measured under elevated pCO2 was 48% higher than under ambient pCO2. Chan and Connolly (2013) tested whether the methodological and biological factors that have been hypothesized to drive variation in magnitude of response explain a significant proportion of the among-study variation. They found that the overall mean response of coral calcification is 15% per unit decrease in Varag over the range 2 , Varag , 4. Among-study variation is large (standard deviation of 8% per unit decrease in Varag). Neither differences in carbonate chemistry manipulation method, study duration, irradiance level nor study species growth rate explained a significant proportion of the amongstudy variation. Duarte et al. (2015) evaluated perceived ocean calamities and concluded that the issue of global decline of ocean calcifiers due to increasing OA is one of the areas with weak scientific support. Improved predictive models are needed, which means that we must sort out the mechanisms and strengthen the models. Correlation between Gnet and the factor [CO3 2− ] which determines Varag does not establish cause and effect (Jokiel, 2013). Experiments that documented correlations between Gnet, Pnet, and seawater chemistry have been conducted repeatedly since the development of the alkalinity depletion method to measure coral calcification. Initial experiments described calcification dynamics in static aquaria incubations (Smith and Kinsey, 1978) and reef field enclosures (Kinsey, 1978). More recently, these experiments have been expanded to include continuous flow measurements of proton flux in coral reef mesocosms (Jokiel et al., 2014). There is a basic physiological explanation for the observed correlation between Gnet and Varag that must be understood. Daytime coral metabolism rapidly removes DIC (primarily in the form of HCO3 − ) from the seawater while photosynthesis provides the energy that drives Gnet (Jokiel et al., 2014). Higher pH resulting from photosynthesis pushes the seawater carbonate system equilibria toward higher [CO3 2− ] (and therefore higher Varag) although DIC is decreasing. This scenario results in a positive correlation between Gnet and Varag. Both Varag and Gnet are dependent variables on Pnet and many other factors. The correlation between Gnet and Varag is modified by changes in pH. Changes in pH can be due to many processes (e.g. photosynthesis by macroalgae, addition of land-derived material, metabolism of organic materials). Changes in AT occur due to bioerosion and dissolution of carbonate sediment and rocks. Other factors such as irradiance, temperature and water motion influence Pnet, Gnet and Varag. Therefore, the slope and intercept of the regression line varies widely (Figure 1). In conclusion, there are large inconsistencies in descriptions coral and coral reef response to OA. Part of this problem can be traced to assumptions used in these studies. Perhaps the major shortcoming of models lies in the belief that [CO3 2− ] and thus Varag controls calcification. The alternate explanation is the rate at which a calcifying system can rid itself of the excess protons produced as a waste product of calcification (Jokiel et al., 2014). Results of Murillo et al. (2014) should also be considered. They found that corals growing in a mixed-community experience an environment that is more favourable to calcification (higher daytime pH and dissolved oxygen due to algae photosynthesis, additional input of AT and inorganic carbon from sediments). They also showed that the widely used alkalinity depletion method yields a lower net calcification rate for a mixedcommunity vs. a coral-only community due to AT recycling, although the corals may be calcifying at a higher rate under these conditions. Increased temperature will play the dominant role in the decline of reefs during future climate change with OA playing a lesser role, so the uncertainties on the effects of OA have less impact on the final estimates of reef decline. On the brighter side, the consequent expansion of OA research will eventually produce a better understanding of the processes that control coral calcification. Acknowledgements This work partially funded by the Pacific Island Climate Change Cooperative and by the United States Geological Survey, Coastal and Marine Geology Program cooperative agreement G13AC00130. N. Silbiger, M Donahue, and three anonymous reviewers provided comments that improved the original manuscript. References Andersson, A. 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