Claire F. Brace,^[1] Faculty of Science, Monash University

Abstract

Anthropogenic carbon emissions have led to warming and acidification of ocean surface waters globally. Ocean acidification results in the formation of carbonic acid and subsequently bicarbonates, causing the calcium carbonate saturation state (Ω) of seawater to decline with potentially serious implications for calcifying organisms such as reef corals. In this review, the impact of ocean acidification on reef corals is assessed. While numerous studies show decreases in adult reef coral calcification rates in response to declining ocean pH, inconsistency in organism responses suggests the extent of this reduction may be somewhat species-specific. However, regardless of this variability, acclimatisation appears unlikely and it is anticipated a pH threshold exists, below which calcification will cease. Heterogeneity was also uncovered among coral life stages; for example, coral larvae show some tolerance to acidified seawater, but metabolic suppression results in later metamorphic and settlement issues. This review concludes with an investigation of the interaction between warming and acidification on coral calcification; contending the significant among-study variability highlights the need for further investigation of ecosystem dynamics. Furthermore, results highlight the need for multi-stressor and whole-ecosystem studies to better understand the variation in the impact of low ocean pH on coral reefs.

Keywords: Coral reef; climate change; pH; calcification; ocean acidification; CO₂.

Introduction

Rising anthropogenic carbon emissions over the last century have had numerous effects on the Earth’s climate, including the warming and acidification of ocean surface waters (IPCC, 2014). Ocean acidification occurs through the dissolution of additional carbon dioxide in ocean surface waters, producing carbonic acid (H₂CO₃), as seen in the following reaction (Orr et al., 2005: 681; Fabry et al., 2008: 415):

According to the latest report of the Intergovernmental Panel on Climate Change (IPCC), between 1750 and 2010 there was a 26% increase in the acidity of the world’s oceans and a lowering of global ocean surface pH by 0.1 (Figure 1) (IPCC, 2014: 4). While this decrease may seem small, the logarithmic nature of the pH scale means a pH decline of 0.1 translates into a 30% increase in global oceanic hydrogen ion (H+) concentration (Abbasi and Abbasi, 2011: 1602). The excess H+ ions increase ocean acidity and bind to carbonate (CO3-2) molecules, to form bicarbonates (HCO3 -) (Fabry et al., 2008: 415). Such a phenomenon represents a serious threat to biodiversity and the health of marine ecosystems globally, in particular relation to marine invertebrates that rely on dissolved carbonate molecules to build calcium carbonate (CaCO3) skeletons (Orr et al., 2005; Wood, Spicer and Widdicombe, 2008). As the calcium carbonate saturation state (Ω) of world’s oceans declines, it is projected key marine organisms – such as reef coral – will have difficulty building and maintaining their calcium carbonate skeletons (Orr et al. 2005).

A wealth of literature now exists, including a host of reviews and meta-analyses exploring the potential impacts of ocean acidification on marine ecosystems (Hoegh-Guldberg et al., 2007; Kroeker et al., 2010; Pandolfi et al., 2011; Kroeker et al., 2013). For example, Hoegh-Guldberg et al. (2007) use global [CO₂]atm and temperature data from the Vostok Ice Core Study (Petit et al. 1999) to compare present-day carbonate-ion concentration to the recent past and review the potential impacts on coral reefs globally, concluding that the rate of change in ocean chemistry is likely to preclude the capacity of organisms to adapt. The work of Pandolfi et al. (2011) reviews the evidence for variability in coral calcification response to acidification, concluding that greater temporal and spatial heterogeneity exists than previously assumed. Such results are emulated in the meta-analysis of Chan and Connolly (2013), who find an overall average decline in coral calcification with acidification, but with large among-study variation. Similarly, the work of Kroeker et al. (2010; 2013; 2017) provides a key perspective in the review of scientific work on ocean acidification, performing meta-analyses of 228 studies examining organism responses declining pH. While ocean acidification was found to have an overall negative impact on the survival, abundance, growth, development and calcification of a broad range of calcifying and non-calcifying taxa, significant heterogeneity was uncovered (Kroeker et al. 2010; 2013).

As such, this review seeks to extend the existing scholarship on the impact of acidification resulting from anthropogenic carbon emissions on calcifying organisms. While previous studies have considered the effects on a broad range of marine species (Fabry et al., 2008; Hendriks et al., 2010; Kroeker et al., 2010; 2013), here the current evidence regarding calcifying reef corals is assessed more specifically, aiming to explore some of the remaining variation of the responses to ocean acidification within taxonomic groups. The effect of declining ocean pH will firstly be discussed in relation to the calcification rates of adult reef corals and the capacity of such corals to acclimatise to lower pH conditions. Next the impact on future populations will be investigated through the survival, growth and development of larval polyps and juvenile coral. Finally, as ocean acidification occurs in conjunction with rising ocean surface water temperatures, the interaction between anthropogenic ocean warming and acidification will be explored.

Figure 1: Increase in atmospheric CO₂ historically (1750–2000), and projected for 2100 (a), decline in ocean pH pre-industrial, 1994 and 2100 (b) and calcium carbonate concentration (as its two forms, aragonite and calcite) pre-industrial, 1994 and 2100 (c). Reprinted by permission from Macmillan Publishers Ltd: Nature Climate Change (Orr et al. 2005: 682), copyright (2005).

Acidification and calcification rates of adult corals

Reef corals build protective calcium carbonate skeletons by calcification, which occurs via the active and passive exchange of ions between seawater and extracellular fluid (Gagnon, Adkins and Erez, 2012: 150). Marine organisms produce such skeletons from two forms of naturally occurring calcium carbonate minerals, aragonite and calcite, with coral species using crystal-form aragonite (Orr et al., 2005: 681). Thus, it is anticipated as the calcium carbonate saturation state (Ω) of seawater decreases with ocean acidification (due to the binding of excess H+ ions with carbonate molecules), calcification in adult coral will be negatively affected (Hoegh-Guldberg et al. 2007; Gagnon, Adkins and Erez, 2012). For example, Hoegh-Guldberg et al. (2007: 1737) note a suite of experimental studies have shown decreases in coral calcification and growth of up to 40% with a doubling of pre-industrial [CO₂]_atm to 560 ppm, concluding that the speed of change to ocean chemistry is likely to exceed the capacity of most organisms to adapt. While many studies across multiple coral species project that reduced ocean pH causes a decline in calcification rates, it is interesting to note that the extent of this reduction may be somewhat species-specific (Orr et al., 2005; Shaw, McNeil and Tilbrook, 2012).

Over the past decade, research has primarily focused on the impact of ocean acidification on tropical reef corals (Gattuso et al., 1998; De’ath, Lough and Fabricius, 2009; Shaw, McNeil and Tilbrook, 2012). For example, Anthony et al. (2008) used experimental CO₂-dosing scenarios representing the present day (control, 380 ppm), intermediate (570–700 ppm) and high (1000–1300 ppm) CO₂ stabilisation scenarios by the IPCC and two temperature treatments (25–26°C and 28–29°C) over eight weeks to observe effects on bleaching, productivity and calcification in three functionally important tropical reef species: staghorn corals (Acropora intermedia), massive corals (Porites lobate) and crustose coralline algae (Porolithon onkodes) (CCA). Calcification rates in crustose coralline algae (CCA) were highly sensitive to CO₂ dosing, showing a 50% reduction with intermediate CO₂-dosing, and 130–190% reduction with high CO₂-dosing relative to control conditions at low and high temperatures (Anthony et al., 2008: 17442–43). Yet, while Acropora and Prorites both showed a decline of approximately 40% in calcification rate at the highest CO₂-dosing, these responses were considerably weaker in comparison to the effects on bleaching and productivity (hourly rates of photosynthesis minus respiration integrated over the day) (Anthony et al., 2008: 17442–43). Such findings suggest that while it is likely the threshold for growth and survival of species such as CCA may be exceeded, tropical corals show more mixed responses.

However, in more recent years, attention has turned towards temperate (or ‘cold-water’) corals, as they are increasingly considered to be more vulnerable to ocean acidification (Form and Riebesell, 2012; Maier et al. 2013). This is because, the deeper layers of the ocean, where cold-water corals are found, are naturally more acidic as the CO₂ dissolved at the surface descends with colder water as part of the thermohaline circulation and remains there (Feely et al. 2004: 365). These relatively more acidic ocean layers are separated from the aragonite-abundant, higher pH surface layers by a boundary layer called the ‘aragonite saturation horizon’ (ASH) (Feely et al. 2004: 363). Although over 95% of cold-water reefs exist above the ASH, they occupy significantly deeper oceans layers compared to tropical reefs (Form and Riebesell, 2012: 843). As ocean acidification progresses, the ASH will rise higher in the water level, leading to under-saturation of cold-water coral habitats and endangering coral calcification (Feely et al. 2004; Form and Riebesell, 2012; Maier et al., 2013).

A recent investigation of the effect of seawater pH on the calcification rate of cold-water coral species Cladocora caepitosa and Oculina patagonica, found that exposure to ocean pH projected for 2100 (7.83 down from current pH of 8.09) resulted in a significant and linear decrease in average calcification rate across both species (32% lower than control in O. patagonica and 35% lower in C. caepitosa) over 92 days (Movilla et al., 2012: 148). Additionally, colonies that exhibited faster growth rates appeared to be more affected by lowered pH conditions, with greater mean growth reduction seen in O. patagonica (Movilla et al., 2012: 148). A similar long-term study conducted by Bramanti et al. (2013: 1901) over 314 days on Mediterranean coral, Corallium rubrum, found an even greater average decrease in calcification rate (59%) between current pH levels (8.09) and future pH projections (7.81).

In contrast to these results, Maier et al. (2012:1720) found no significant difference in the calcification rate of cold-water species, Madrepora oculata, between current pCO₂ of 404 μatm (amount of dissolved carbon dioxide relative to seawater volume, producing a pH of approximately 8.09) and elevated pCO₂ of 867 μatm (producing a pH of approximately 7.6). Other studies have displayed similarly non-significant declines in coral calcification rates in cold-water species such as Oculina arbuscular and Madrepora oculata, and tropical coral Acropora digitifera (Ries, Cohen and McCorkle, 2010; Maier et al., 2013; Takahashi and Kurihara, 2013). Ries, Cohen and McCorkle (2010: 667) found that although calcification rates in cold-water coral, Oculina arbuscular, were reduced from 11.8% to 3.8% at pCO₂ levels well beyond current future predictions (2856ppm), accretion of new skeletal material did continue despite the aragonite under-saturation that occurred due to the increased pCO₂. Similarly, the studies of Maier et al. (2013) and Takahashi and Kurihara (2013) found no change in coral calcification at low seawater pH However, the results of Maier et al. (2012: 1720–21) did indicate a 50% decrease in calcification between pre-industrial (285 μatm) and current pCO₂ (404 μatm), suggesting that ocean acidification may have already reduced calcification rates in reef corals, despite the lack of significant reduction at further elevated pCO₂ levels. Furthermore, while Ries, Cohen and McCorkle (2010: 667) observed continued calcification of O. arbuscular in aragonite under-saturated conditions (at pCO₂ 2856ppm), the steep decline in calcification rates suggest a potential seawater aragonite saturation threshold, beyond which coral calcification rates will be severely impaired.

There is a considerable gap in the scientific understanding of the potential adaptive capacity of adult reef corals, which would occur over longer time periods (and therefore may not be observed in short-term studies) (Hendriks et al., 2010; Kroeker et al., 2013). However, some evidence has been found to suggest that some coral species may exhibit an ability to adapt to lower ocean pH (Kroeker et al., 2013). For example, Form and Riebesell (2012: 847–48) found that exposure of cold-water coral, L. pertusa, to pH of 8.029 (ambient), 7.960, 7.827 and 7.768 (acidic) resulted in an initial decline in calcification over a short-term period of eight days in the two most acidic conditions, followed by an increasing (but not statistically significant) trend in calcification over a longer-term period of 178 days. It was concluded that the coral underwent an initial shock period followed by subsequent acclimatisation to lower pH (Form and Riebesell, 2012: 850–51). Yet in contrast, Maier et al. (2013: 3–4) found no significant difference in calcification rate of the same coral species over either short-term (two-day) or long-term (nine-month) exposure to pH of 8.1, 8.0, 7.85 or 7.73. A meta-analysis of the vulnerability of marine organisms to ocean acidification conducted by Hendriks et al. (2010) revealed that marine organisms do not respond uniformly to ocean acidification and may be more resistant than has been suggested, particularly if subjected to changes in ocean chemistry occurring gradually in nature rather than abruptly during experimentation. However, the data does suggest that calcification rate was the most sensitive process to ocean acidification, with corals showing a reduction on average of 29% in their calcification rates (Hendriks et al., 2010: 160).

Overall, data regarding the adaptive capacity of adult reef corals remains inconsistent, making conclusions about the acclimatisation of corals to future pH projections difficult to draw. Greater uniformity in experimental methodology is needed to elicit more generalisable results. What becomes increasingly clear is the high degree of species specificity involved in calcification responses, likely due to physiological mechanisms that are currently not well understood (Takahashi and Kurihara, 2012). Therefore, while many studies find significant reductions in adult coral calcification rates due to ocean acidification (Movilla et al., 2012; Shaw, McNeil and Tilbrook, 2012; Bramanti et al., 2013), a high level of variability across calcifying taxa suggests that impacts are likely species-specific, and some species may be more resistant to rising acidity than others. However, it was widely acknowledged that pH thresholds below which calcification will cease are likely to exist, and may possibly be reached if ocean acidification trends continue unabated into the next century (Ries, Cohen and McCorkle, 2010; Form and Riebesell, 2012; Maier et al., 2012; Maier et al., 2013).

Acidification and survival, growth and development of reef coral

As larval polyps and recently settled juvenile corals represent future reefs, an understanding of the influence of ocean acidification on developmental processes is increasingly important for future reef health and resilience. A key aspect of coral development is metamorphosis, the growth of free-floating, larval coral into juvenile polyps (Gleason and Hofmann, 2011: 45). Metamorphosis includes the process of settlement, during which juvenile corals become sedentary reef members (Gleason and Hofmann, 2011: 45–46). These phenomena are governed by a complex set of biological cues both from the external and internal environment of coral larvae (Gleason and Hofmann, 2011: 45–46).

Some studies have revealed an apparent tolerance to acidified seawater among free-floating larval polyps (Suwa et al., 2010; Chua et al., 2013a). Chua et al. (2013a: 147–48) found no significant differences in either average survival rates of the larva of two tropical coral species Acropora tenuis and Acropora millepora, or the average number of such larva to complete metamorphosis when exposed to pH ranging from present-day (8.16) to end-of-century predictions (7.86). However, other studies have drawn distinctions between merely surviving and completing metamorphosis, and undergoing these development processes without defects or deficiencies (Albright and Langdon, 2011; Nakamura et al., 2011). Nakamura et al. (2011: 3) similarly found that larval survival did not differ significantly across pH conditions of 8.0, 7.6 and 7.3, but that lower pH resulted in a suppression of larval metabolism, seen in decreased oxygen consumption. While metabolic suppression allows coral larvae to survive lower pH conditions, this can negatively impact long-term settlement processes by disrupting metamorphosis, observed in decreasing metamorphosis rates (Nakamura et al., 2011: 3–5). Consistent with these ideas, Albright and Langdon (2011: 2481–483) found a 63% decrease in the metabolism of tropical coral Porites astreoide larvae with exposure to 800 μatm (pCO₂ producing projected end-of-century pH values), corresponding with a 55–60% reduction in settlement and a 35% decrease in post-settlement growth rate. Thus, while larval polyps may survive changes in ocean pH, the health of such organisms, and therefore the resilience of reef ecosystems, is likely to be negatively affected.

Additionally, studies such as that of Chua et al. (2013a) and many others fail to account for critical symbiotic and larval-algal relationships that occur during development and early settlement. In an investigation of the impact of symbionts on the pH tolerance of recently settled Acropora digitifera polyps in pre-industrial (<300 μatm), current (400 μatm) and future (600 μatm, 800 μatm, 1000 μatm) pCO₂ conditions, Ohki et al. (2013) revealed a hierarchy of environmental tolerance governed by coral-symbiont relationships. The calcification rates of adult A. digitifera corals showed greatest tolerance to lower pH, remaining highest in future pCO₂ conditions relative to polyp samples (Okhi et al., 2013: 6809–10). Recently settled polyps with symbionts showed some level of tolerance to future pCO₂ conditions, and polyps lacking symbionts showed the least tolerance, with significant decreases in calcification rates (Ohki et al., 2013: 6810). Ohki et al. (2013: 6812) suggest that symbiont dinoflagellate species may play a role in facilitating calcification through the production of glycerol and oxygen, used by coral polyps for mitochondrial respiration and ATP (adenosine triphosphate) production, subsequently fuelling ion transport processes that underlie calcification. These results confirm early-settlement corals without symbionts are likely among the most vulnerable to ocean acidification (Ohki et al., 2013).

Furthermore, Doropoulos et al. (2012: 344) found that ocean acidification indirectly impacts coral settlement by reducing the availability of the symbiont CCA, which produce chemical cues that partially regulate the settlement process in some coral species. A reduction in the availability of preferred CCA resulted in reduced and abnormal settlement behaviour in Acropora millepora coral polyps (Doropoulos et al., 2012: 341–42).

Finally, while still focused on polyp settlement, Dufault et al. (2012) investigated the effect of diurnally oscillating pH and the impact of ocean acidification on these natural pH cycles in Seriatopora caliendrum larval polyps. In comparison to static experimental conditions used in majority of previous studies, natural diurnal oscillation in pH (low night-time pH) stimulated growth of newly-settled S. caliendrum polyps, with 6–19% greater average growth than static ambient (8.0) and low pH conditions (7.88) (Dufault et al., 2012: 2954). However, reverse-phased conditions (low day-time pH), as is consistent with ocean acidification, reduced average growth by 26% compared to natural-phase pH levels (Dufault et al., 2012: 2954).

Collectively, these studies suggest that while larval polyps in particular conditions (such as in symbiotic relationships with dinoflagellates or CCA) show an ability to survive lowered pH conditions, such acidity is likely to negatively impact subsequent stages of development, including early calcification, metamorphosis and reef settlement. Such evidence suggests ocean acidification represents a significant threat to the health and resilience of future reef systems.

Acidification and ocean warming

Finally, to make an accurate assessment of the impact of ocean acidification on marine corals, the phenomenon must be considered in the context of other environmental changes that are likely to occur as a result of increasing atmospheric carbon dioxide. While 30% of anthropogenic carbon emissions to date have been absorbed by the ocean, another 40% has become trapped in the atmosphere, raising the concentration of greenhouse gases and trapping heat in the climate system (IPCC, 2014: 4). This causes the warming of ocean surface waters and it is estimated that the upper 75 metres of oceans globally have warmed by approximately 0.09–0.13 degrees per decade between 1971 and 2010 (IPCC, 2014: 4). Thus, investigation of the interaction between both lower ocean pH and higher ocean temperatures is critical when evaluating the potential impact of ocean acidification on marine corals.

It is known that coral species thrive between specific temperature thresholds, beyond which bleaching occurs (Chua et al., 2013b; Castillo et al., 2014). Coral bleaching refers to a stress response in coral species due to extended periods of high ocean temperatures that causes the loss of intracellular symbiotic dinoflagellates containing the photosynthetic pigments that give coral their colour (leaving bleached corals white) (Ainsworth et al. 2016: 338). While the relationship between warmer ocean temperatures and coral bleaching events is well established (Castillo et al., 2014; IPCC, 2014), and research suggests reductions in ocean pH have an overall negative impact on coral calcification (Orr et al., 2005; Chan and Connolly, 2013; Kroeker et al., 2010, 2013), the effects of high seawater temperatures and low ocean pH on calcification are not yet clear. Some such as Chua et al. (2013b) suggest that as high ocean temperatures have been observed to increase coral metabolism, warmer ocean conditions may mitigate the effects of low pH. Alternatively, low pH results in metabolic suppression, thus potentially counteracting this effect (Chua et al., 2013b; Rivest and Hofmann, 2014).

Rodolfo-Metalpa et al. (2011) conducted a transplant study of Mediterranean coral, Cladocora caespitosa and stony coral, Balanophyllia europaea, along natural pCO₂ gradients in volcanic vents in the Tyrrhenian Sea, Italy. A linear decrease in calcification across the five-month experimental period was observed, with complete dissolution of transplanted corals at the lowest tested pH of 7.3 (Figure 2) (Rodolfo-Metalpa et al., 2014: 309). But, crucially, a period of high seawater temperature (28.5°C) caused widespread coral death, with 80% mortality at 7.1 pH compared to 30% at pH 8.0 (Figure 2) (Rodolfo-Metalpa et al., 2014: 311). In this case, the adverse effect of ocean acidification was seen to be largely exacerbated by ocean warming. Similarly, in an investigation of the physiological responses of tropical Pocillopora damicornis larvae to ocean warming and acidification, Rivest and Hofmann (2014) determined that only small proportions of larvae will exhibit tolerance to changing ocean conditions. Larvae were incubated in seawater samples of pCO₂ (450 μatm or 950 μatm) and temperature (28°C or 30°C) for six hours, showing elevated metabolic rates under warmer conditions and depressed metabolic rates under higher pCO₂ conditions (Rivest and Hoffmann, 2014: 5). However, rather than increased metabolic activity due to ocean warming compensating for the effect of increased pCO₂, the physiological costs of maintaining acid-base homeostasis increased, meaning that long-term tolerance of such conditions is unlikely for the majority of coral species (Rivest and Hoffmann, 2014: 7). Further, Anlauf, Croz and Dea (2011: 16) found that while survival and settlement of stony coral, Porites panamensis, were unaffected by high temperature (29.5°C) and low pH (7.83) conditions, post-settlement growth was adversely affected. While low pH and ambient temperature (28.9°C) resulted in a 3% decrease in skeletal mass, exposure to low pH and high temperatures resulted in a significantly greater decrease of 28% (Anlauf, Croz and Dea, 2011: 16). Collectively, such studies suggest that overall the interaction between warming and acidification will be additive and detrimental.

Yet, some propose the highly variable coral responses to ocean acidification may be evidence that the influence of ocean warming will be even greater than that of acidification (Chua et al., 2013b; Couce, Ridgwell and Hendy, 2013; Putnam et al., 2013). However, such inconsistencies may potentially be attributed to differences in experimental methodology, particularly in the choice of temperature and pH levels and length of study. Further, others such as Schoepf et al. (2013: 4) found in three out of four adult coral species exposed to current (382 μatm) and future (607 μatm, 741 μatm) pCO₂ conditions, and temperatures of either 26.5°C or 29°C, calcification rates were not significantly affected. Only Acropora millepora showed a decrease in calcification (53% at 741 μatm), but this was unaffected by temperature (Schoepf et al., 2013: 4). Thus, while there is strong evidence for the detrimental effect of the interaction between ocean acidification and warming on marine corals, inconsistencies suggest the influence of more complex biological factors. Species-dependent differences imply differing degrees of control over physiological processes such as calcification and metamorphosis. Despite a growing number of studies, the interactions between environmental stressors such as ocean warming and acidification are not yet well understood in terms of coral physiology and presents a need for further research to draw more definitive conclusions.

Figure 2: Underwater and scanning electron microscopy images of B. europaea along CO₂ gradient. Live coral after seven months at mean pH 8.1 (a–c) and 7.3 (d–f). Dead coral after three months at mean pH 7.3 (g–i). Details of the outer corallite wall showing normal skeleton when covered in tissue (Co) (b, e) and dissolved skeleton when uncovered (Un) (h). Reprinted by permission from Macmillan Publishers Ltd: Nature Climate Change (Rodolfo-Metalpa et al. 2011: 310), copyright (2011).

Directions for future research

The literature relating to the impact of ocean acidification on reef coral reveals several important observations. Principally, inconsistencies in the literature mean that the impact of ocean acidification on adult reef coral cannot be considered uniformly negative. While studies show an overall average decrease in coral calcification in response to low ocean pH (Movilla et al., 2012; Shaw, McNeil and Tilbrook, 2012; Bramanti et al., 2013; Kroeker et al., 2013), responses have also shown to be non-linear or inconsistent (Ries, Cohen and McCorkle, 2010; Maier et al., 2012) or reveal no effect of low pH on calcification (Maier et al., 2013; Takahasi and Kurihara, 2013). Similar contradictions are observed in investigations of the interaction between ocean acidification and warming on adult, juvenile and larval coral (Putnam et al., 2013; Schoepf et al., 2013). The variation in such studies highlight three main concepts; the possible influence of experimental methodology and length of study, the species-specific nature of the impact of ocean acidification, and a need for a more holistic, ecosystem-wide approach to determining climate effects on marine corals.

The potential influence of differing research methodologies should be taken into account when considering the inconsistent results. Takahashi and Kurihara (2013: 312) propose that the use of different experimental conditions (open or closed flow-through tanks, light/dark oscillation regimes and so on) and methods of data collection (buoyant weight or alkalinity anomaly technique in measuring calcification) can affect study outcomes. Furthermore, when working with biological systems, study duration can largely affect the reliability of results, particularly in relation to climate phenomena where short-term studies may not encompass the long-term organism response or adaptive capacity but only capture a brief and potentially extreme event (Fabricius et al., 2011). For instance, in an investigation of the impact of low pH and high temperatures on tropical Pocillopora damicornis larvae, Cumbo, Fan and Edmunds (2013: 104) note that effects on survival require greater than 5 days to detect. However, in a meta-analysis of the sensitivity of calcification to changes in the saturation state of aragonite (Ω_Arag) caused by ocean acidification, Chan and Connolly (2013) did not find that study duration, or carbonate manipulation method (either acid addition or CO₂ bubbling) had a statistically significant effect on between-study variability. While analysis revealed studies measuring calcification via the total alkalinity (TA) method showed larger decreases in calcification compared to studies using buoyant weighting, it was concluded that such a finding did not significantly alter the overall average decline in calcification observed (approximately 15% per unit decrease in Ω_Arag) (Chan and Connolly 2013: 285). TA measurements can be made over very short intervals (despite study length) and as such are typically made during the day, thus including only the effects of acidification on light calcification (Chan and Connolly, 2013). In contrast, buoyant weighting estimates calcification over relatively long time scales (weeks to years) and consequently implicitly integrates over light and dark calcification (Chan and Connolly, 2013). Chan and Connolly (2013: 288) suggest as there is some evidence the decrease in dark calcification with decreasing Ω_Arag is less pronounced, this may explain the discrepancy between TA and buoyant weighting techniques.

It is likely, however, that due to the high degree of variance between calcifying taxa, biological factors are primarily responsible for variability in coral responses observed in many of the studies. McCulloch et al. (2012) suggest a mechanism of pH up-regulation may explain the tolerance of particular coral species to high ocean temperatures and low seawater pH. As calcification is partially an active process, some scleractinian corals such as Lophelia pertusa increase the pH of their calcifying fluid in order to promote calcification (McCulloch et al., 2012). Yet, the energetic costs and impact on symbionts is not yet well understood (McCulloch et al., 2012). Overall, throughout the literature knowledge about the physiological links between calcification, metamorphosis and seawater chemistry is limited (Kroeker, 2010). Further study into this area will lead to clearer explanations of taxonomic differences in the effect of ocean acidification on calcification.

Finally, taxonomic variation, interactions with symbionts, algae and the effect of a plethora of abiotic factors such as warming, nutrient availability, salinity and irradiance highlight the need for an ecosystem-focused approach. While single-species laboratory studies provide valuable information about the effect of particular environmental factors on reef corals, this cannot give an overall accurate picture of the interconnected influence of multiple factors and species interactions (Kroeker et al., 2010, 2013, 2017). Thus, in order to build a more precise understanding of the impact of ocean acidification on reef corals, both a greater understanding of coral physiology and functional responses to single stressors, and long-term, field experiments incorporating natural variation in other environmental factors and the acclimation or adaptation of organisms over time is required (Kroeker et al. 2013, 2017).

Conclusion

A review of the current evidence regarding the impact of ocean acidification on reef corals reveals significant heterogeneity between study results. A variety of adult coral responses to ocean acidification have been observed experimentally, but an overall decrease in calcification rates, reef health and resilience of coral reefs globally is probable. Additionally, while coral larvae show an ability to survive low pH conditions, metabolic suppression will likely negatively affect later growth and development. Responses to the combined effect of acidification and warming are also variable but without adaptation reef communities are generally expected to degrade. The influence of methodological variance is considered, however it is concluded heterogenous results are more likely the product of biological factors, including physiological differences between species, the interaction of multiple environmental stressors, and ecosystem interactions across taxa on greater temporal scales. As such, this review reveals a need for greater understanding of coral physiology, and whole-ecosystems dynamics, thus multi-stressor studies conducted in marine communities remain a key area of future research to better determine the effect of ocean acidification on reef corals.

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Notes

[1] Claire F. Brace graduated from a Bachelor of Arts (Global)/Bachelor of Science at Monash University in November 2017. Claire is now undertaking a Bachelor of Arts (Honours) in Human Geography at Monash University, investigating the role of local governments in the multi-level governance of climate action in Melbourne, Australia.

Acknowledgements

This review was originally written as part of SCI2015: Scientific Practice and Communication (Advanced). I thank my tutor and mentor, Melissa Honeydew, for her continuous support and guidance in the adaptation and editing process. I also thank Professor Ramesh Rajan (Monash School of Biomedical Sciences) for his helpful discussions, input and advice.

List of figures

Figure 1: Increase in atmospheric CO₂ historically (1750–2000), and projected for 2100 (a), decline in ocean pH pre-industrial, 1994 and 2100 (b) and calcium carbonate saturation (as its two forms, aragonite and calcite) pre-industrial, 1994 and 2100 (c). Reprinted by permission from Macmillan Publishers Ltd: Nature Climate Change (Orr et al. 2005), copyright (2005).

Figure 2: Underwater and scanning electron microscopy images of B. europaea along CO₂ gradient. Live coral after seven months at mean pH 8.1 (a–c) and 7.3 (d–f). Dead coral after three months at mean pH 7.3 (g–i). Details of the outer corallite wall showing normal skeleton when covered in tissue (Co) (b, e) and dissolved skeleton when uncovered (Un). Reprinted by permission from Macmillan Publishers Ltd: Nature Climate Change (Rodolfo-Metalpa et al. 2011: 310), copyright (2011).

References

 

To cite this paper please use the following details: Brace, C.F. (2018), 'Climate Change Below the Surface: The Impact of Ocean Acidification on Reef Corals ', Reinvention: an International Journal of Undergraduate Research, Volume 11, Issue 2, http://www.warwick.ac.uk/reinventionjournal/archive/volume11issue2/brace. Date accessed [insert date]. If you cite this article or use it in any teaching or other related activities please let us know by e-mailing us at Reinventionjournal at warwick dot ac dot uk.