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Ocean Acidification and Coral Bleaching

  • R. Albright
Chapter
Part of the Ecological Studies book series (ECOLSTUD, volume 233)

Abstract

Simultaneous with the increases in global sea surface temperature, increasing atmospheric carbon dioxide (CO2) is driving changes in the chemistry of the oceans—a process known as ocean acidification. Over the last two decades, reef-related ocean acidification research has focused primarily on the consequences of elevated CO2 on calcification. The impacts of ocean acidification on other critical processes such as coral-algal symbioses and bleaching thresholds are less well known. In this chapter, I review the available literature on the impacts of ocean acidification on coral bleaching. I begin by providing context for ocean acidification and its impacts on coral reefs. I focus primarily on primary literature investigating the effects of CO2 on photophysiology, coral–algal symbioses, and bleaching responses while shedding light on information needs and unresolved issues. I also briefly touch on environmental factors other than temperature and ocean acidification that have the potential to influence coral bleaching responses (e.g., nutrients).

12.1 Introduction

Simultaneous with the increases in global sea surface temperature, increasing atmospheric carbon dioxide (CO2) is driving changes in the chemistry of the oceans—a process known as ocean acidification. Over the last two decades, reef-related ocean acidification research has focused primarily on the consequences of elevated CO2 on calcification. The impacts of ocean acidification on other critical processes such as coral-algal symbioses and bleaching thresholds are less well known. In this chapter, I review the available literature on the impacts of ocean acidification on coral bleaching. I begin by providing context for ocean acidification and its impacts on coral reefs. I focus primarily on primary literature investigating the effects of CO2 on photophysiology, coral-algal symbioses, and bleaching responses while shedding light on information needs and unresolved issues. I also briefly touch on environmental factors other than temperature and ocean acidification that have the potential to influence coral bleaching responses (e.g., nutrients).

12.1.1 Ocean Acidification

Simultaneous with the increases in global sea surface temperature (SST), increasing atmospheric carbon dioxide (CO2, the main greenhouse gas) is driving changes in the seawater chemistry of the oceans. At present, the ocean absorbs about one-third of fossil fuel CO2 emissions and will eventually sequester up to 90% of anthropogenic CO2 (Archer et al. 2009; Sabine et al. 2011), causing measurable shifts in seawater carbonate chemistry (Bates et al. 2014; Canadell et al. 2007; Le Quéré et al. 2015). On entry into the ocean, CO2 reacts with seawater via the following net chemical reaction:
$$ {\mathrm{H}}_2\mathrm{O}+\left(\mathrm{C}{\mathrm{O}}_2\right)\mathrm{aq}+{\mathrm{CO}}_3^{2-}\to 2{\mathrm{H}\mathrm{CO}}_3^{-} $$
(12.1)

As a result, concentrations of aqueous carbon dioxide, [CO2]aq, and bicarbonate \( \left[{\mathrm{HCO}}_3^{-}\right] \) increase, while the concentration of carbonate \( \left[{\mathrm{CO}}_3^{2-}\right] \) and the pH of seawater decrease (Broecker et al. 1979; Caldeira and Wickett 2003; Sabine et al. 2004); this process is referred to as ocean acidification (OA). In the last 200 years, the global average pH of ocean surface waters has declined by about 0.1 units, from pH ~8.2 to pH 8.1 (Rhein et al. 2013), which equates to an increase in acidity (i.e., hydrogen ion concentrations) of approximately 30%. Under a business-as-usual scenario, a further decrease of 0.3–0.4 units (to pH 7.7–7.8) is expected by the end of the twenty-first century. Another important outcome of OA for calcifying organisms, such as reef-building corals, is the decrease in the saturation state of calcium carbonate (Ω), defined as Ω = [Ca2+]\( \left[{\mathrm{CO}}_3^{2-}\right] \)/K′sp, where K′sp is the solubility product for a particular mineral phase of CaCO3 (e.g., aragonite, calcite). Aragonite is the dominant biogenic form of CaCO3 secreted by many reef-building organisms, including corals. If Ω > 1, seawater is supersaturated with respect to CaCO3, and conditions are favorable for CaCO3 precipitation; conversely, if Ω < 1, seawater is undersaturated with respect to CaCO3, and the dissolution of CaCO3 is favored. The surface waters of the tropical oceans are currently supersaturated with respect to aragonite; however, the saturation state of aragonite (Ωarag) of tropical Pacific surface waters is estimated to have decreased from values of about 4.5 in preindustrial times (Kleypas et al. 1999; Cao and Caldeira 2008) to about 3.8 by 1995 (Feely et al. 2009) and is expected to continue declining to approximately 3.0 by the middle of this century and 2.3 by the end of the century (Feely et al. 2009).

12.1.2 Variability in Seawater Carbonate Chemistry of Coral Reefs

OA projections are based on trends from data collected in open ocean environments (Doney et al. 2009; Feely et al. 2009; Zeebe 2012), and their implications for shallow, nearshore environments, such as coral reefs, are poorly understood. In coastal regions, OA can interact with other natural and anthropogenic environmental processes to hasten local declines in pH and carbonate mineral saturation states (Duarte et al. 2013; Feely et al. 2010). In the Great Barrier Reef, Australia, for example, inshore reefs are subjected to elevated pCO2 levels compared to offshore reefs, and the rate of increase in inshore pCO2 is fast3er than offshore and atmospheric values (Cyronak et al. 2014; Uthicke et al. 2014). Changes in pH in coastal ecosystems result from a multitude of drivers, including oceanic uptake of anthropogenic CO2 emissions, nutrient inputs, changes in metabolism (the balance between primary production, respiration, and calcification), impacts from watershed processes, organic matter, and hydrodynamics. For example, organic carbon metabolism (photosynthesis and respiration) and inorganic carbon metabolism (calcification and dissolution) can drive strong diel and seasonal fluctuations in seawater chemistry (Ohde and van Woesik 1999; Anthony et al. 2011a; Bates et al. 2010; Kleypas et al. 2011; Shamberger et al. 2011; Gray et al. 2012; Shaw et al. 2012; Albright et al. 2013, 2015; Koweek et al. 2015). Characteristic ranges are on the order of 0.3 pH units (Duarte et al. 2013) but can be as large as 1 pH unit in some environments [e.g., Lady Elliot Island reef flat, southern Great Barrier Reef (Shaw et al. 2012)]. The extent to which reef metabolism alters the carbonate chemistry of the overlying water column is a function of numerous factors, including benthic community composition (Anthony et al. 2013; Koweek et al. 2014), biological activity (which can vary with temperature, light, and nutrient availability), physical forcing (e.g., temperature, salinity), tidal regime, water depth, and residence time (Falter et al. 2008, 2012).

Changes in the adjacent watershed can also influence alkalinity and CO2 fluxes that, together with metabolic processes and oceanic dynamics, can yield decadal changes of up to 0.5 units in coastal pH (Duarte et al. 2013). Within many coastal ecosystems, anthropogenic nutrient inputs enhance microbial respiration, driving concurrent acidification and hypoxia (Altieri et al. 2017). These interactions between OA and local to regional drivers yield complex regulation of pH in coastal waters that have the capacity to strongly impact ecosystem health and performance. Accordingly, many reef environments experience variable ocean chemistry that often differs from open ocean conditions and, over relatively short time scales (days and months), range more widely than the difference in mean conditions between preindustrial to future OA scenarios (Hofmann et al. 2011; Shaw et al. 2012; Albright et al. 2013). Understanding the significance of OA projections in the context of this background variability is central to gauging the susceptibility of reef ecosystems to projected changes in ocean chemistry.

12.1.3 Impacts of Ocean Acidification on Coral Reefs

Major changes in ocean chemistry can have profound effects on marine ecosystems (Doney 2010) and have even been implicated in creating conditions leading to past mass extinction events (Veron 2008; Clarkson et al. 2015). pH plays a key role in many physiological processes such as ion transport, enzyme activity, and protein function, and as such, changes in CO2 can influence a wide range of physiological processes including acid-base regulation, metabolism, energetics, and dependent processes (Pörtner 2005, 2008). While extracellular and intracellular pH is usually tightly regulated, the capacity of regulatory mechanisms can be overwhelmed. OA also has the capacity to alter physiological processes that depend on carbon species as reactants, including calcification and photosynthesis. Coral reefs are widely regarded as one of the most vulnerable marine ecosystems to OA, in part because the very architecture of the ecosystem is reliant on carbonate-secreting organisms. OA will lead to variable but predominantly adverse biological and ecological responses for key species of coral reef organisms (Kroeker et al. 2010, 2013), including slowed reef growth, altered competitive interactions, and impaired population replenishment. Slower calcification results in slower coral growth, more fragile structures (Madin et al. 2008), and potentially a shift from net accretion to net dissolution (Silverman et al. 2009; Andersson and Gledhill 2013; Perry et al. 2013), with implications for greater susceptibility to storm damage, slower recovery rates between disturbances, less habitat-forming structures, and overall reduced reef resilience (Anthony et al. 2011b). Both laboratory and field studies provide evidence that coral reefs have already lost significant calcification capacity due to OA (Dove et al. 2013; Albright et al. 2016).

Model results suggest that if CO2 emissions continue to follow a business-as-usual path, tropical coral reefs are likely to shift toward conditions that are marginal for reef growth (i.e., net dissolution) this century (Hoegh-Guldberg et al. 2007; Silverman et al. 2009). In addition to impacting corals, OA lowers the abundance of crustose coralline algae (Kuffner et al. 2007), a key player in solidifying reef framework and providing settlement cues for numerous reef invertebrate larvae (Harrington et al. 2004). Other impacts include shifts in competitive interactions between corals and macroalgae (Diaz-Pulido et al. 2011), shifts in the competitive hierarchy of corals (Horwitz et al. 2017), synergistic effects of temperature and OA on coral mortality (Prada et al. 2017), and impairment of behavioral responses critical for fish recruitment (Munday et al. 2010, 2014). Coral communities around natural CO2 seeps show shifts in community composition from highly diverse and structurally complex systems to those characterized by much lower diversity and structural complexity (Fabricius et al. 2011, 2014), leading to loss of ecological function and associated services.

A wide range of impacts are likely on coastal human communities including reduced food, income, and well-being, as well as longer-term impacts such as increasing vulnerability as coral reefs become less able to protect coastal areas from storms and waves (Pendleton 1995; Cooley et al. 2009; Pascal et al. 2016). While local adaptation over evolutionary time scales (involving genetic isolation and strong selective pressure) renders certain communities more resistant to low-Ω seawater (e.g., Golbuu et al. 2016; Barkley et al. 2017), there is little evidence that coral reef organisms can adapt or acclimate to future OA scenarios (but see Putnam and Gates 2015). The possibility of OA acting to lower coral bleaching thresholds has been suggested (e.g., Anthony et al. 2008); however acidification effects on coral bleaching are highly uncertain. Whether or not OA influences the bleaching response of corals remains a topic of debate and is the primary focus of this chapter.

12.2 Ocean Acidification and Coral Bleaching

In reef-building corals, Symbiodinium density and physiology are regulated by host- and symbiont-driven mechanisms that vary in response to environmental conditions such as light intensity, temperature, and nutrients (Lesser 2004, 2011). Abrupt changes in environmental conditions can disrupt coral-algal symbioses and cause bleaching (i.e., loss of Symbiodinium and/or photosynthetic pigments) (Lesser 2011). While the effects of elevated temperature on coral bleaching are well known (Fitt et al. 2001; Jokiel 2004; Lesser 2011), the effects of elevated pCO2 on bleaching responses are less clear. Compared to calcification studies, less attention has been placed on other aspects of holobiont physiology, including symbiont photophysiology and primary productivity. Where these effects have been investigated, outcomes are equivocal (Table 12.1). To inform our understanding of potential mechanisms by which changing seawater chemistry could influence coral-algal symbioses, it is helpful to briefly review proposed bleaching mechanisms and relationships to dissolved inorganic carbon (DIC).
Table 12.1

Studies examining effects of OA and/or OA and temperature on coral bleaching or photophysiology

Reference

Species

T (°C)

pH,

pCO2

Response variable

Observed effect(s)

Anlauf et al. (2011)

Porites panamensis

29, 30

7.8, 8.03 (546, 900–1000 ppm)

Growth, algal density, biomass, survival, larval settlement, bleaching

No effect of low pH on larval settlement, survival, or bleaching of primary polyps. Temp reduced algal density. Temp × CO2 increased algal density. Temp exacerbated CO2 effects on growth. Temp × CO2 reduced biomass of primary polyps.

Anthony et al. (2008)

Acropora intermedia, Porites lobata

25–26, 28–29

8.0–8.4, 7.85–7.95, 7.6–7.7

Productivity, calcification

CO2-induced bleaching observed in two species.

Acropora: Pnet unaffected by intermediate CO2, but Pnet increased at CO2 × temp. Large reductions in Pnet at high CO2. Calcification decreased by 60% at high-CO2 × high-temp

Porites: Calcification and net productivity decreased with decreasing pH. Intermediate CO2 and high-temp increased calcification.

Baghdasarian et al. (2017)

Seriatopora caliendrum

27.6, 30.4

466 ppm, ~895 ppm

Algal density, chl cell−1, algal division

Temperature-induced bleaching (decreased algal density), reduced algal division, and altered chl cell−1, but no CO2 effect. Intraspecific variation observed in bleaching responses, unrelated to algal mitotic index or pigment content.

Comeau et al. (2016)

Porites rus, Acropora pulchra, Pocillopora damicornis, Pavona cactus, massive Porites sp., Psammocora profundacell, Porites irregularis,

Pocillopora verrucosa

27

280, 400, 550, 700, 1000, 2000 μatm

Photosynthesis (Pnet, Pgross), respiration (Rdark, LEDR)

Overall, respiration and photosynthesis of eight coral spp. and seven calcified algal spp. was relatively insensitive to increasing pCO2. No effect of OA on Pnet in seven of eight coral spp. and seven of seven calcified algal spp., Pgross in six of eight coral spp. and six of seven calcified algal spp., Rdark in six of eight coral spp. and six of seven calcified algal spp., and LEDR in eight of eight coral spp. and seven of seven calcified algal spp. Minor effects detected for a few traits in some species.

Comeau et al. (2017)

Mixed community

24, 27

~400, ~1300 μatm

Pnet, Gnet

No effect of pCO2 on Pnet-PAR relationship. pCO2 altered Gnet-PAR relationship by suppressing Gnet. OA may alter balance between net community calcification (ncc) and net community production (ncp) by depressing ncc without affecting ncp.

Crawley et al. (2010)

Acropora formosa

23

7.55–7.65, 7.80–7.90, 8.00–8.20 (380, 560, 1100 ppm)

Photorespiration (PGPase activity), symbiont productivity, photosynthetic capacity, photoprotection

Chl a cell−1 increased, while photosynthetic capacity per chlorophyll decreased with increasing CO2. No change in algal density. Dark respiration remained constant, whereas LEDR increased with increasing CO2. Under high CO2, energy dissipation pathways were over-activated (e.g., nonphotochemical quenching through xanthophyll de-epoxidation) or partially closed due to a reduction in enzyme synthesis. Decreased expression of PGPase (phosphoglycolate phosphatase).

Dove et al. (2013)

Mixed community

25, 26, 28, 30

7.7, 7.9, 8.1, 8.2, (301, 405, 611, 1009 μatm)

Gnet, Pnet, Rnet

OA decreased daytime calcification and increased nighttime dissolution (overall reduction in Gnet). No effect on Pnet or Rnet. Bleaching and mortality observed in all scenarios (including controls and preindustrial treatment).

Fine and Tchernov (2007)

Oculina patagonica, Madracis pharencis

17–30

7.3–7.6, 8.0–8.3

Tissue biomass, algal density, gametogenesis

Low pH induced partial loss of symbionts (bleaching) in some, but not all O. patagonia corals. No effect on gametogenesis. Enhanced protein content and polyp biomass for some corals.

Hoadley et al. (2015)

Acropora millepora, Pocillopora damicornis, Montipora monasteriata, Turbinaria reniformis

26.5, 31.5

382, 607, 741 μatm

Algal cellular volume, protein, lipid, carbohydrate content, maximal photochemical efficiency, intracellular carbonic anhydrase

Complex host- and symbiont-specific responses. Overall, temp had greater influence on photophysiology (algal cellular volume, protein, lipid, carbohydrate content, maximal photochemical efficiency, intracellular carbonic anhydrase) than CO2.

Iguchi et al. (2012)

Porites australiensis

27

7.4, 7.6, 8.0

Calcification, algal density, chl a cell−1, fluorescence yield (Fv/Fm)

pCO2 decreased calcification and fluorescence yield, but no effect on algal density or chl a cell−1. Intraspecific differences in response.

Kaniewska et al. (2012)

Acropora millepora

25

7.6–7.7, 7.8–7.9, 8.0–8.2 (260–440, 600–790, 1010–1350 μatm)

Algal density, Pnet, Rnet, gene expression

High CO2 decreased algal densities (>50%), photosynthesis, and respiration. Changes in gene expression were consistent with metabolic suppression, increase in oxidative stress, apoptosis, and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling.

Kavousi et al. (2015)

Acropora digitifera, Montipora digitata, Porites cylindrical

28, 31

400, 1000 μatm

Calcification, protein content, maximum photosynthetic efficiency, algal density, chl content, Symbiodinium type, Fv/Fm

Significant intra- and interspecific differences in responses. Different responses to pCO2, temp, and pCO2 × temp between hosts with different Symbiodinium type and between similar Symbiodinium types in colonies of different species. No effect of pCO2 or pCO2 × temp on protein content; pCO2 decreased algal density in some, but not all combinations. pCO2 × temp reduced Fv/Fm in some, but not all combinations. Mixed effects on chl a cell−1.

Krueger et al. (2017)

Stylophora pistillata

+1–2

7.8

Pigmentation, net O2 production, primary production

No visual signs of bleaching. No change in algal density or protein or carbohydrate content in symbiont or host tissue. Low pH had additive positive effect on net O2 production at elevated temp. Low pH significantly enhanced the efficiency of gross O2 generation per unit chl, independent of temp. pH × temp increased total chl concentration, predominantly driven by temp (+45%), compared to pH (−9%). Synergistic effects of pH x temp on electron flow in PSII. Temp increased catalase activity in host tissue. No effect on symbiont antioxidant enzyme activity.

Krief et al. (2010)

Porites sp., Stylophora pistillata

25

8.09, 7.49, 7.19 ( pCO2 > 2000 ppm)

Algal density, skeletal growth, coral tissue biomass (protein concentration) chl a, isotopic skeletal composition

pCO2 decreased algal density and skeletal growth but increased coral tissue biomass (protein concentration) and chl a. Altered isotopic skeletal composition.

Langdon et al. (2003)

Mixed community

26.5

404, 658 μatm

Calcification, net community production, dark respiration, light respiration

pCO2 negatively impacted calcification. No change in net community production or dark respiration. pCO2 increased light respiration.

Noonan et al. (2013)

Acropora millepora, Pocillopora damicornis, Seriatopora hystrix, Porites cylindrical, massive Porites sp., Galaxea fascicularis

NA

7.8–7.9, 8.0–8.05 (~390, 500–900, >1000 ppm)

Symbiodinium type

Strong differences in Symbiodinium type by coral species, but no differences along CO2 gradients at volcanic CO2 seeps.

Noonan and Fabricius (2016)

Acropora millepora, Seriatopora hystrix

28, 31

7.79 (~780 μatm), 7.95

Bleaching, maximum PSII quantum yields, light-limited electron transport rates, gross photosynthesis, pigment concentrations

No effect of pCO2 on bleaching during transient bleaching event along CO2 gradient near volcanic CO2 seeps. In tank experiments, temp, but not CO2, affected bleaching. pCO2 increased maximum photosystem II quantum yields and light-limited electron transport rates. pCO2 increased gross photosynthesis and pigment concentrations in S. hystrix. Overall, stronger temp effects than CO2 and species-specific responses.

Reynaud et al. (2003)

Stylophora pistillata

25, 28

460, 760 μatm

Chl c2, chl a, protein, photosynthesis, respiration, calcification, algal density

No effects on chl c2 or protein. Chl a increased under temp × pCO2. Algal density increased at high pCO2. Pnet affected by both temp (increased) and pCO2 (decreased), but no impacts on respiration. Temp × pCO2 decreased calcification (no change with pCO2 at normal temp).

Rodolfo-Metalpa et al. (2010)

Cladocora caespitosa

~15–20, ~20–25

400, 700 μatm

Photosynthesis, respiration, photosynthetic efficiency (Fv/Fm), zooxanthellae density

No effect of pCO2 or pCO2 × temp on photosynthesis, photosynthetic efficiency, or calcification.

Schneider and Erez (2006)

Acropora eurystoma

24

7.9–8.5

Calcification, photosynthesis, respiration

Calcification positively correlated to \( {\mathrm{CO}}_3^{2-} \) and Ωarag. Reduction in \( {\mathrm{CO}}_3^{2-} \) by 30% reduced calcification by 50%. Photosynthesis and respiration did not show any significant response to changes in seawater CO2.

Schoepf et al. (2013)

Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis

26.5, 29

382, 607, 741 μatm

Coral energy reserves (lipid, protein, carbohydrate), chl a, algal density

Coral energy reserves (lipid, protein, carbohydrate) showed species-specific responses to elevated pCO2 and temp. Nonlinear, species-specific responses of chl a and algal density to pCO2. Temp modulated pCO2 response, sometimes mitigating and worsening pCO2 effects.

Strahl et al. (2016)

massive Porites sp., Acropora millepora

29.5

7.8, 8.1 (323, 803 μatm)

Tissue biomass, lipid, protein, tissue energy content, fatty acid content, pigment content, oxidative stress parameters

No effect of pCO2 on tissue biomass, lipid, protein and tissue energy content, fatty acid content, pigment content, and oxidative stress parameters. Differences between species and location much greater than effect of pCO2

In Porites sp., only one of the biochemical parameters investigated (ratio of photoprotective to light-harvesting pigments) responded to pCO2.

Takahashi and Kurihara (2013)

Acropora digitifera

29

7.56, 7.97 (744, 2142 μatm)

Calcification, respiration, photosynthesis, algal density, photosynthetic efficiency (Fv/Fm)

No effect of CO2 on calcification, bleaching, or productivity (photosynthesis, respiration, photosynthetic efficiency, algal density).

Wall et al. (2013)

Seriatopora caliendrum

27.7, 30.5

445, 840 ppm

Bleaching, maximum photochemical efficiency

(Fv/Fm), effective photochemical efficiency (ΔF/Fm′)

of PSII, Pnet, photosynthetic

efficiency (α), chl

a, symbiont density

Temp-induced bleaching and negatively impacted photosynthetic performance of symbionts as measured by maximum photochemical efficiency (Fv/Fm) and effective photochemical efficiency (ΔF/Fm′) of PSII, net photosynthesis (Pnet) and photosynthetic efficiency (α), chl a and symbiont density. High pCO2 had no direct or synergistic effect on Symbiodinium photophysiology or productivity and did not cause bleaching.

12.2.1 Bleaching Mechanisms and Dissolved Inorganic Carbon

The mechanism behind warmwater bleaching is generally accepted to involve accumulation of oxidative stress at photosystem II (PSII) in the symbiont, a process known as photoinhibition (Lesser 1996). Photoinhibition occurs when the rate of photodamage to PSII exceeds the rate of repair and can result in reduced photosynthetic rates and elevated reactive oxygen species (ROS), further damaging the symbiont and coral. This stress can change the energetic/metabolic demands of the symbiont, reducing the amount of photosynthate translocated to the host. Physiological changes in the host, such as reduced tissue thickness and apoptosis of gastrodermal cells, can precede changes in symbionts when corals are exposed to stress. Various photoprotective mechanisms exist to provide alternate electron pathways to divert excess excitation energy that may otherwise lead to the formation of ROS and photooxidative damage of proteins, lipids, and pigments. These include pathways such as the water-water cycle and photorespiration.

Zooxanthellae use the Calvin-Benson cycle (dark reaction) to fix CO2. Symbiodinium contain a form II Rubisco (the enzyme ribulose bisphosphate carboxylase/oxygenase), which has a poor ability to discriminate between CO2 and O2 (Rowan et al. 1996). Consequently, maintaining an elevated ratio of CO2:O2 at the site of photosynthesis benefits overall productivity. In theory, physiological processes that depend on carbon species as reactants (e.g., photosynthesis, calcification) may be directly influenced by acidification-induced changes in the inorganic carbon supply. For organisms that are CO2 limited, increasing dissolved CO2 and \( {\mathrm{HCO}}_3^{-} \) associated with OA could potentially alter photosynthetic kinetics and “fertilize” photosynthesis, with some benefits generally expected for plants and algae. Seagrasses, for example, which appear carbon limited, respond positively to increasing seawater CO2 (Beer and Koch 1996; Zimmerman et al. 1997; Jiang et al. 2010; Russell et al. 2013; Ow et al. 2015). For most investigated species, however, photosynthetic responses to OA are relatively small and are highly variable among taxa (Mackey et al. 2015). For zooxanthellae, the source and reliability of CO2 is complicated by their intracellular location. While molecular CO2 can freely diffuse across cell membranes and lipid bilayers, at typical seawater pH (~8.1), molecular CO2 represents only a small fraction (<1%) of the available DIC in seawater, with the majority in the form of \( {\mathrm{HCO}}_3^{-} \) (Zeebe and Wolf-Gladrow 2001), which is largely inhibited from diffusing into the host cells due to its ionic charge. To enhance the delivery of CO2 to the endosymbiont, many coral species implement a range of CO2-concentrating mechanisms (CCMs), which facilitate the dehydration of \( {\mathrm{HCO}}_3^{-} \) into CO2 in the presence of carbonic anhydrase and H+-ATPase (Furla et al. 2000; Al-Horani et al. 2003). At low irradiance, respiratory CO2 is sufficient to meet photosynthetic demand (Muscatine et al. 1989). At high solar irradiance, however, zooxanthellae rely on the host to supplement the DIC supply by converting \( {\mathrm{HCO}}_3^{-} \) from bulk seawater (Goiran et al. 1996; Marubini et al. 2008). Consequently, CO2 delivery to the symbiont is heavily regulated by host CCM activity. In turn, CCM activity relies on energy (ATP) that is, in part, derived from photosynthate transferred from the zooxanthellae (Al-Horani et al. 2003) (though note that many species utilize heterotrophic carbon to mitigate intracellular CO2 limitation during periods of autotrophic stress, enhancing bleaching resistance). Feedbacks between host-regulated DIC delivery to the symbiont and symbiont-regulated energy to the host complicate our ability to predict effects of increased CO2 on photophysiology. Present information suggests that Symbiodinium in hospite are DIC limited (e.g., Goiran et al. 1996). As CO2(aq) increases with OA, symbiont productivity could increase due to a release from carbon limitation; however, the effect of elevated CO2 on photosynthesis is likely to be minimal for endosymbiotic Symbiodinium owing to host regulation of DIC supply and the presence of CCMs (Mackey et al. 2015).

An alternate bleaching mechanism was proposed by Wooldridge (2009a) whereby the expulsion of zooxanthellae is triggered by CO2 limitation around Rubisco resulting from a functional breakdown in CCM function such as carbonic anhydrase and/or Ca2+-ATPase activity (i.e., CO2 demand exceeds available supply). In this scenario, inadequate CCM activity (due to either direct damage to the CCM or insufficient energy to fuel CCM activity) limits the ability of the coral host to maintain a sufficient supply of CO2 for the endosymbiont, particularly during periods of high photosynthetic demand (e.g., high solar irradiance or thermal stress). This leads to photoinhibition, oxidative damage, and eventual expulsion of zooxanthellae. Whether this model explains the breakdown of coral-algae symbiosis in response to other known bleaching triggers, such as low temperature, low salinity, high sedimentation, aerial exposure, etc. is not yet known.

12.2.2 Evidence of Ocean Acidification-Induced Bleaching

To date, there have been no documented cases of acidification-induced bleaching in the natural environment; most of what we know has been determined experimentally and not verified ecologically. Only a few experimental studies have reported coral bleaching in response to acidification stress. For example, a causal link between CO2 exposure and bleaching response was reported in a symbiotic sea anemone (Pecheux 2002), although these results were not published in the peer-reviewed literature. Anthony et al. (2008) compared bleaching, productivity, and calcification responses to acidification (pH 7.6–8.4) and warming (25–29 °C) at ecologically relevant irradiances (~1000 μmol photons m−2 s−1) and showed that elevated CO2 induced bleaching (loss of pigmentation) in two key groups of reef-building organisms—crustose coralline algae (CCA) and branching (Acropora) and massive (Porites) coral species. These results are often scrutinized because bleaching was evaluated using a luminance colorimetric scale rather than quantifying algal (Symbiodinium) densities or pigment content. The mechanism underlying the observed bleaching response was not explicitly investigated; however the authors hypothesize that changes in seawater chemistry influence bleaching thresholds by altering the functioning of the carbon-concentrating mechanism, photoprotective mechanisms (e.g., photorespiration), and/or direct impacts of acidosis. Kaniewska et al. (2012) investigated the phenotypic and transcriptional responses of Acropora millepora colonies exposed to OA and showed that exposure to high CO2 drives major changes in gene expression, respiration, photosynthesis, and symbiosis. Elevated pCO2 (>1000 μatm) resulted in a loss (>50%) of Symbiodinium cells, an associated decrease in photosynthesis and respiration, and an increase in transcripts of genes involved in/responsible for alleviating oxidative stress, suggesting that the photosynthetic apparatus of the zooxanthellae was compromised. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis, and symbiont loss. Based on the transcriptomics results, the authors suggest that similar cellular events occur during acidosis-induced bleaching as those reported for thermally induced bleaching (e.g., Weis 2008). These include increased ROS (and/or reactive nitrogen species, RNS) production, which in turn disrupts calcium homeostasis, a condition that has been linked to coral bleaching (DeSalvo et al. 2008). Additional cellular impacts of acidosis included changes to acid-base regulation and mitochondrial ATPase activity.

In contrast, mounting experimental evidence from laboratory, field, and modeling studies suggests that the influence of elevated CO2 on coral bleaching may be trivial. For example, thermal bleaching (loss of Symbiodinium and/or chlorophyll content) in Seriatopora caliendrum was unaffected by high pCO2 (>800 ppm) in two studies (Wall et al. 2013; Baghdasarian et al. 2017). Hoadley et al. (2015) report various physiological impacts in four coral species (Acropora millepora, Pocillopora damicornis, Montipora monasteriata, Turbinaria reniformis) exposed to increased temperature (31.5 °C) and pCO2 (~740 ppm), including changes in maximal photochemical efficiency and biochemical composition of the symbionts (e.g., algal cellular volume, protein, and lipid content). However, elevated temperature played a greater role in altering physiological responses than pCO2. Interestingly, the photophysiological response and biochemical composition of the symbionts differed among clades and influenced holobiont responses, drawing attention to the need to understand symbiont, host, and symbiont × host (holobiont) responses (Hoadley et al. 2015). In the Gulf of Aqaba, Stylophora pistillata colonies showed no signs of bleaching despite spending 1.5 months at 1–2 °C above long-term summer maximum SST and a seawater pH of 7.8 (Krueger et al. 2017). Symbiotic dinoflagellates did, however, show improved photochemistry with higher pigmentation and a doubling in net oxygen production, leading to a 51% increase in primary productivity. In a Symbiodinium energetics study, Bedwell-Ivers et al. (2016) found no significant differences in zooxanthellae density or Chl a content in two Caribbean coral species (Acropora cervicornis and Porites divaricata) exposed to elevated pCO2 (~1000 μatm). They did, however, report reductions in the maximum rate of net photosynthesis (Pmax) and dark respiration (Rd), a response the authors attribute to metabolic suppression (an adaptive response to conserve energy) as opposed to bleaching. At natural volcanic CO2 seeps in Papua New Guinea, where corals are chronically exposed to elevated CO2 up to 800 μatm, the majority of variation in important biochemical measures such as tissue biomass, energy storage, pigmentation, cell protection, and cell damage was attributed to species (massive Porites vs. Acropora millepora) and location, with little effect of pCO2 (Strahl et al. 2016). At these same CO2 seeps, Noonan and Fabricius (2016) surveyed four common coral families (Acroporidae, Faviidae, Pocilloporidae, or Poritidae) and a thermally sensitive species Seriatopora hystrix along CO2 gradients during a minor regional bleaching event and found little indication that elevated pCO2 influenced bleaching susceptibility of the broader coral community. Concurrent tank experiments also showed no effect of elevated pCO2 (780 μatm) on bleaching sensitivity in Acropora millepora or Seriatopora hystrix (Noonan and Fabricius 2016). Finally, a modeling study assessed the sensitivity of coral bleaching projections under different Ωarag sensitivities and found that Ωarag exhibits limited influence on bleaching sensitivity under RCP 2.6 and 4.5 scenarios. By the year 2050, RCP 4.5 results in >95% of global reefs experiencing annual bleaching regardless of Ωarag sensitivity. Even under the high mitigation scenario RCP 2.6, >90% of global reefs are projected to experience annual bleaching by the mid-twenty-first century regardless of Ωarag sensitivity (Kwiatkowski et al. 2015).

12.2.3 Photoacclimation and Photoprotection

Photoacclimation refers to the physiological acclimation by an organism to a certain light environment. Similar to plants, corals demonstrate photoacclimatory responses such as changes in symbiont density and/or chlorophyll content per cell. To date, the effects of CO2 enrichment on photoacclimation are equivocal. It is well-established that the coral-algal symbiosis is a dynamic reciprocal relationship, in which the symbiotic interaction can change depending on environmental conditions that differentially benefit either partner (Wooldridge 2017). It has been suggested that there is an optimum zooxanthellae density that optimizes autotrophic capacity (P:R) by maximizing light harvesting and minimizing intraspecific competition for resources such as intracellular CO2 (Wooldridge 2017). Environmentally triggered increases in algal density may cause resource limitation and influence photosynthetic capacity while increasing respiratory and maintenance costs. Nutrient enrichment, for example, can inhibit the ability of the coral host to maintain demographic control of its algal symbionts, resulting in increased algal densities that act as net carbon sinks and limit energetic resources of the coral (Wooldridge 2013, 2016). While high Symbiodinium densities have been suggested to buffer corals from thermal stress (Stimson et al. 2002), Cunning and Baker (2012) showed that increases in symbiont density actually lowered coral bleaching thresholds. This may be because more Symbiodinium produce more reactive oxygen species under stressful conditions (Lesser 1996). Elevated pCO2 promotes enlarged zooxanthellae populations in some (e.g., Reynaud et al. 2003; Crawley et al. 2010; Anlauf et al. 2011), but not all (Rodolfo-Metalpa et al. 2010; Bedwell-Ivers et al. 2016) cases (Table 12.1). While increases in CO2 supply may initially release symbionts from DIC limitation and facilitate growth, an enlarged endosymbiont population may increase the risk of CO2 limitation during periods of high irradiance, theoretically making corals more susceptible to bleaching.

Photorespiration is one of several photoprotective mechanisms that provides alternate electron pathways to divert excess excitation energy that could otherwise lead to ROS formation and photooxidative damage of proteins, lipids, and pigments. Compared to photosynthesis, photorespiration is generally viewed as energetically wasteful because of its higher consumption of NADPH and ATP per unit of sugar produced, but it can be an important physiological pathway for mitigating oxidative stress during periods of excess excitation energy. During photorespiration, Rubisco binds with O2 (as opposed to CO2), resulting in the production of phosphoglycolate (PG). Excess PG can inhibit the Calvin cycle, so PGPase breaks down PG to glycolate, allowing the Calvin cycle to continue. Glycolate is either excreted or enzymatically broken down, adding to the fixed carbon supply for photosynthesis. Crawley et al. (2010) investigated the effect of increasing CO2 on photosynthetic capacity, photoacclimation, and photoprotection in Acropora formosa and found that CO2 enrichment increased chlorophyll a per cell but did not affect symbiont cell density. PGPase expression was reduced by 45% at high CO2 (1160–1500 ppm). The authors suggest that OA has the capacity to influence ROS formation and subsequent oxidative stress by compromising enzymatic activity of key photoprotective pathways. Given that many intracellular enzymes are pH-sensitive, more studies are needed on the effects of CO2 enrichment on enzymatic pathways that underpin coral-algal symbioses.

12.2.4 Phylotype-Specific Responses and Symbiont Shuffling

Thermal stress is known to differentially affect phylotypes of Symbiodinium, resulting in host-specific responses. Compared to temperature, little work has been done to assess phylotype-specific responses to CO2. Brading et al. (2011) investigated the effect of pCO2 on the photosynthesis and growth of four coral-associated phylotypes of Symbiodinium (cultured cells) and found the response to be phylotype-specific. Whereas certain phylotypes (A1 and B1) were largely unaffected by a doubling of pCO2, the growth rate (A13) and photosynthetic capacity (A2) of other phylotypes are doubled. This variability may be linked to differences in carbon acquisition as well as preference for dissolved inorganic carbon species (CO2 vs. \( {\mathrm{HCO}}_3^{-} \)) and may partially explain species-specific responses observed in other studies (e.g., Bedwell-Ivers et al. 2016). Symbiont shuffling—i.e., increased abundance of heat-tolerant symbionts following thermal bleaching (Buddemeier et al. 2004)—has been shown to reduce coral susceptibility to recurrent warming (e.g., Cunning et al. 2015). Whether coral-algal associations respond to changes in pCO2 has not been thoroughly explored; however, Noonan et al. (2013) found that coral-symbiont associations remained stable regardless of proximity to volcanic CO2 seeps in Papua New Guinea, indicating that acclimatization through symbiont shuffling may not be an option to cope with ocean acidification.

12.2.5 Photosynthesis-Respiration

Experiments investigating the effect of elevated CO2 on coral photosynthesis and/or carbon production show complex and species-specific responses with variable results (Table 12.1). The vast majority of studies on coral reef organisms (e.g., corals and calcified algae) and communities suggest that photosynthetic rate is relatively unaffected by elevated CO2 (Leclercq et al. 2002; Langdon et al. 2003; Schneider and Erez 2006; Rodolfo-Metalpa et al. 2010; Dove et al. 2013; Takahashi and Kurihara 2013; Comeau et al. 2016). A meta-analysis of 11 studies found that the mean effect size of CO2 on coral photosynthesis was not statistically discernible from zero (Kroeker et al. 2013). Comeau et al. (2016) used a large range of pCO2 values (280–2000 μatm) and 15 species of common reef calcifiers (eight coral species and seven calcifying algae) on the shallow reefs of Moorea, to show that net photosynthesis, dark respiration, light-enhanced dark respiration (LEDR), and gross photosynthesis of corals and calcified algae are largely insensitive to pCO2 during short-term incubations. The general lack of a “CO2 fertilization” effect on photosynthesis may be, in part, because zooxanthellae primarily use external \( {\mathrm{HCO}}_3^{-} \) (Goiran et al. 1996; Gattuso et al. 1999; Schneider and Erez 2006). In contrast, Kaniewska et al. (2012) report net decreases in both photosynthesis and respiration of Acropora millepora colonies exposed to elevated CO2, and Anthony et al. (2008) report that high CO2 levels (1000–1300 μatm) induced productivity loss and bleaching of Acropora intermedia. Iguchi et al. (2012) report reduced photosynthetic efficiency of the massive coral Porites australiensis at high CO2 (1175–1439 and 1801–2193 μatm), although zooxanthella density was not affected. Meanwhile, greater net productivity with elevated CO2 was reported for symbiotic sea anemones in laboratory experiments and near natural CO2 seeps (Suggett et al. 2012; Towanda and Thuesen 2012). Langdon and Atkinson (2005) found a 20–50% increase in carbon production, but not oxygen production, of coral assemblages composed of Porites compressa and Montipora capitata. It is important to note that CO2 enrichment does not automatically result in increased productivity, as other factors such as nitrogen, phosphorus, and iron may limit photosynthesis. Consequently, it is valuable to understand the interplay between the influence of OA on primary productivity under different nutrient regimes.

It has been suggested that aerobic respiration in corals will increase under OA to compensate for increased energetic demands associated with maintaining calcification rates in a thermodynamically challenging environment (e.g., McCulloch et al. 2012). However, empirical evidence shows that the effects of elevated pCO2 on aerobic respiration are ambiguous, with, for example, no effects of high pCO2 reported on dark respiration of Stylophora pistillata (Reynaud et al. 2003), Acropora eurystoma (Schneider and Erez 2006), and A. formosa (Crawley et al. 2010), while a decrease in respiration has been reported for massive Porites spp. (Edmunds 2012), A. millepora (Kaniewska et al. 2012), and larvae of P. astreoides (Albright and Langdon 2011).

12.3 Ocean Acidification and Coral Reef Resilience

While the link between OA and coral bleaching is tenuous, it is increasingly clear that OA has the capacity to influence post-bleaching recovery by acting on a variety of processes that underpin coral reef resilience, namely, population replenishment and growth.

12.3.1 Reproduction and Recruitment

Ocean acidification has been shown to negatively impact multiple, sequential early life history stages which may severely compromise sexual recruitment and the ability of coral reefs to recover from disturbance. For example, laboratory experiments have found negative impacts of OA on three sequential life history phases necessary for successful coral recruitment: (1) larval availability, by compromising fertilization (Albright et al. 2010; Albright and Mason 2013) but see Chua et al. (2013); (2) settlement ecology, by altering the availability of known settlement cues such as crustose coralline algae (Albright 2011; Albright and Langdon 2011; Doropoulos et al. 2012; Doropoulos and Diaz-Pulido 2013); and (3) post-settlement ecology, by impeding post-settlement growth and survival (Albright et al. 2008, 2010; de Putron et al. 2010; Albright 2011; Albright and Langdon 2011; Anlauf et al. 2011; Moya et al. 2012; Foster et al. 2015, 2016). Field observations from volcanic CO2 seeps in Papua New Guinea validate laboratory findings, indicating altered settlement substrata and reduced coral recruitment at high CO2 (Fabricius et al. 2017).

12.3.2 Growth and Calcification

Over the last two decades, OA research has focused primarily on the consequences of shifting ocean chemistry on coral calcification (Kroeker et al. 2010, 2013; Riebesell and Gattuso 2014; Andersson et al. 2015). While some species appear insensitive over the range of conditions investigated (Comeau et al. 2013; Takahashi and Kurihara 2013), the majority of field and laboratory studies show declines in coral calcification with increasing CO2 (e.g., Gattuso et al. 1998; Langdon et al. 2000, 2003; Marubini et al. 2001, 2003; Reynaud et al. 2003; Langdon and Atkinson 2005; Silverman et al. 2009; Kroeker et al. 2010, 2013; Anthony et al. 2011b; Pandolfi et al. 2011; Dove et al. 2013; Albright et al. 2016). According to a meta-analysis of 25 studies, the mean response of coral calcification to a unit change in Ωarag is approximately 15% (Chan and Connolly 2013). In addition to direct impacts on reef builders, OA and warming have been shown to accelerate decalcification of coral communities, with microbial communities (Dove et al. 2013), endolithic algae (Reyes-Nivia et al. 2013), and excavating sponges (Fang et al. 2013) being the primary agents of erosion.

Both laboratory and field studies provide evidence that coral reefs have already lost significant calcification capacity due to OA (Dove et al. 2013; Albright et al. 2016). Model results suggest that if CO2 emissions continue to follow a business-as-usual path, tropical coral reefs are likely to shift toward conditions that are marginal for reef growth (i.e., net dissolution) this century (Hoegh-Guldberg et al. 2007; Silverman et al. 2009). As the reef framework and carbonate balance are compromised, a wide range of impacts are likely on coastal human communities (Fabricius 2005; Fabricius et al. 2013; Kroeker et al. 2013; Hoegh-Guldberg 2014; Wong et al. 2014; Albright et al. 2016; Edmunds et al. 2016). These include reduced food, income, and well-being, as well as longer-term impacts such as increasing vulnerability as coral reefs become less able to protect coastal areas from storms and waves (Pendleton 1995; Hoegh-Guldberg et al. 2007; Cooley et al. 2009; Pascal et al. 2016).

12.4 Other Environmental Factors (Nutrients)

While a combination of thermal stress and high irradiance is the primary trigger for modern mass-bleaching events (e.g., Hoegh-Guldberg 1999), at a local to regional scale, other environmental stressors can cause bleaching independently and act synergistically by effectively lowering the threshold temperature at which coral bleaching occurs (Lesser 2004, 2011). These factors include changes in salinity, seawater chemistry, disease, sedimentation, cyanide fishing, pollution, unusually low temperatures, excess ultraviolet (UV) radiation, aerial exposure, bacterial pathogens and pollutants, nutrients, and solar radiation (reviewed in Brown 1997; Lesser 2011). Most of these have been determined experimentally in the laboratory and not verified ecologically. In contrast to the recent global bleaching events associated with global climate change (Hughes et al. 2017), nonthermal bleaching tends to occur on smaller spatial scales in response to localized and/or pulsed stress. For this reason, the majority of these factors are not dealt with here. However, due to the vulnerability of coastal ecosystems to terrestrial inputs, nutrients have the potential to operate on chronic and regional scales, thereby influencing bleaching thresholds in nearshore waters.

The mechanism by which excess nutrients influence bleaching thresholds is not dissimilar to that proposed for CO2—release from N or C limitation fuel algal densities and lead to excess ROS under stressful conditions. Symbiodinium are typically nitrogen-limited at high irradiance (Fabricius 2005). Symbiodinium densities typically increase in response to elevated DIN, which is preferentially used for zooxanthellae growth, as opposed to heterotrophically derived nutrients which increase both algal and host tissue growth (Hoegh-Guldberg and Smith 1989; Muscatine et al. 1989; Marubini and Davies 1996; Fabricius 2005). Increased algal populations produce more ROS under stressful conditions (Lesser 1996), thereby making corals more susceptible to bleaching when sea surface temperatures rise (Wooldridge 2009b; Cunning and Baker 2012; Wiedenmann et al. 2012). Thus, the temperature threshold for bleaching has the potential to fluctuate as a function of nutrient levels and their influence on symbiont densities and/or growth rates (Wooldridge 2009a; Cunning and Baker 2012; Wiedenmann et al. 2012).

Despite these proposed links between nutrient availability and bleaching thresholds, there is little empirical evidence that nutrients increase bleaching prevalence in the field. Bleaching severity in inshore environments can be exacerbated relative to offshore (e.g., Wooldridge (2009b), a phenomenon that is often attributed to environmental stress associated with nutrient loading (e.g., Wooldridge 2009b; Wagner et al. 2010). Using a large-scale dataset from the Great Barrier Reef, Wooldridge and Done (2009) investigated geographic patterns of coral bleaching in 1998 and 2002 and show a synergism between heat stress and nutrient flux as a causative mechanism for observed bleaching patterns. Wiedenmann et al. (2012) showed that increased DIN, in combination with limited phosphate concentrations, increases the susceptibility of corals to temperature- and light-induced bleaching. Using a manipulative field experiment in the Florida Keys, Vega Thurber et al. (2014) showed that coastal nutrient loading—at levels commonly found on many degraded reefs worldwide—increases both bleaching severity and disease prevalence. Encouragingly, one year after termination of nutrient enrichment, there were no differences in bleaching or disease prevalence, suggesting that improvements to water quality may be an effective lever to mitigate some coral bleaching and disease. It is certain that local processes such as nitrogen pollution and eutrophication exacerbate the effects of OA, both chemically and physiologically. Changing sediment loads from terrestrial sources and using controls on nutrient inputs as a policy lever for mitigating coastal water acidification can also modify the carbonate chemistry of surface waters by altering the balance between autotrophy and heterotrophy, thereby helping to alleviate coastal acidification (Bille et al. 2013).

12.5 Conclusions

Overall, our understanding of the impacts of OA on coral-algal symbioses, and associated bleaching dynamics, is incomplete. While studies yield mixed results, mounting experimental evidence suggests that bleaching will not be accentuated at ecologically meaningful levels by the expected increase in pCO2 over the next century. In theory, changes in CO2 have the capacity to influence a variety of physiological processes that are integral to host-algal dynamics and photophysiology with the most obvious avenues being direct impacts on algal population dynamics (e.g., algal density and chlorophyll concentrations), downstream effects on energy allocation, and/or impacts on enzymatic pathways that underpin photosynthesis, oxidative stress, and/or photoprotection. However, empirical evidence is dominated by mixed responses, suggesting that the influence of OA on bleaching thresholds is equivocal. Generally, temperature seems to have a greater influence on productivity and photophysiology than CO2, and intra- and interspecific variation in both host and symbiont responses outweighs CO2 effects. The lack of a clear signal may, in part, be due to differences in experimental design (e.g., outdoor/indoor, closed versus flow-through systems, duration which affects acclimation potential), levels of other abiotic factors such as light and nutrients, phylotype-specific responses in Symbiodinium, and species-specific responses. Certainly, comparisons among species and determination of functional relationships between pCO2 and photophysiology are complicated by the wide range of experimental conditions that dominate the literature. Studies that couple observations at the phenotypic level with underlying molecular mechanisms (e.g., Crawley et al. 2010) show promise to elucidate relationships between CO2 enrichment and bleaching physiology. Specifically, studies evaluating connections between CO2 and oxidative stress (ROS production), apoptosis, photoinhibition (and associated repair pathways such as D1 proteins), enzymatic activity (e.g., antioxidant enzymes, Rubisco), and associated processes such as PSII function are needed, as are investigations into phylotype-specific responses, host-symbiont interactions, and the influence on holobiont responses.

While thermal stress remains the primary concern regarding acute impacts to coral reefs, it is clear that both temperature and OA act synergistically to erode coral reef health and performance. As discussed, direct links between OA and bleaching responses are, at present, tenuous; however, it is certain that OA impedes post-disturbance recovery by slowing growth and reproduction. Given that warming and OA share a root cause—increasing atmospheric CO2—it is increasingly clear that deep and rapid emissions reductions are critical to secure the future of coral reefs.

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.California Academy of SciencesSan FranciscoUSA

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