Ocean acidification (OA) is a relatively young yet rapidly developing scientific field. Assessing the potential response(s) of marine organisms to projected near-future OA scenarios has been at the forefront of scientific research, with a focus on ecosystems (e.g., coral reefs) and processes (e.g., calcification) that are deemed particularly vulnerable. Recently, a heightened emphasis has been placed on evaluating early life history stages as these stages are generally perceived to be more sensitive to environmental change. The number of acidification-related studies focused on early life stages has risen dramatically over the last several years. While early life history stages of corals have been understudied compared to other marine invertebrate taxa (e.g., echinoderms, mollusks), numerous studies exist to contribute to our status of knowledge regarding the potential impacts of OA on coral recruitment dynamics. To synthesize this information, the present paper reviews the primary literature on the effects of acidification on sexual reproduction and early stages of corals, incorporating lessons learned from more thoroughly studied taxa to both assess our current understanding of the potential impacts of OA on coral recruitment and to inform and guide future research in this area.

1. Introduction

Coral reefs harbor one of the most diverse ecosystems on the planet in terms of species complexity [1] and are sources of vast economic wealth through a variety of ecosystem goods and services [2]. Despite the profound ecological and economic importance of these valuable marine ecosystems, global degradation of coral reefs has resulted in unprecedented loss over the past several decades [38]. Given the current trends in reef degradation, it is critical to understand processes that may allow these valuable marine ecosystems to persist. The recovery and persistence of a population, and of a species, requires that levels of recruitment keep pace with the loss of adult individuals [9, 10]. Successful coral recruitment, that is, the introduction and inclusion of a new individual to a population, is generally determined by three sequential life history stages: (1) larval availability (including gamete production and successful fertilization), (2) settlement ecology (related to larval and substrate condition), and (3) postsettlement ecology (growth and survival of the newly settled individual) [11]. Larval settlement and subsequent survival (recruitment) are processes that can control marine population dynamics [12, 13]. Environmental factors that disrupt these processes can result in compromised recruitment or recruitment failure and profoundly affect marine population dynamics [1215].

Ocean acidification refers to the increase in acidity (decrease in pH) of the ocean’s waters resulting from oceanic uptake of atmospheric CO2. Present-day atmospheric carbon dioxide (pCO2) levels are estimated to be 387 ppm [16], 30% higher than the natural range over the last 650,000 years [17]. pCO2 levels are increasing at a rate of 0.5% per year [16], 200 times faster than any changes that occurred during the last eight glacial cycles [17] and 8–15 times faster than any changes in the past 60 Myr, including the Paleo-Eocene Thermal Maximum (PETM) [18]. pCO2 levels are projected to double present-day values (reaching 750 ppm) by the end of this century (year 2100) [16]. Nearly 50% of all CO2 emitted into the atmosphere over the last two and a half centuries has been absorbed by the oceans [19]. Consequently, seawater carbonate concentrations have been depleted by ~30 μmol kg−1, simultaneously reducing the pH of the ocean’s surface waters by 0.1 units relative to the preindustrial era (a 30% increase in acidity) [16]. Further reductions of 0.3–0.5 pH units are projected to occur by the end of this century as the oceans continue to absorb anthropogenic CO2 [16].

Documenting and predicting the response(s) of coral reefs and other marine ecosystems to changing ocean chemistry has been of recent concern in the scientific community. The number of ocean acidification-related studies has risen dramatically over the past several years leading to valuable insight regarding the future state of our oceans. While many acidification studies originally focused on the sensitivity of adult growth and calcification, mounting experimental evidence now suggests that numerous biological processes and physiological functions independent of calcification may be negatively impacted including sperm motility in urchins [20], corals and sea cucumbers [21], fertilization success in sea urchins [20, 22, 23] but see [24], molluscs [25, 26] but see [27] and corals [28], larval development and/or growth in crustaceans [2932], molluscs [25, 33, 34], corals [28, 3539] and echinoderms [22, 4043], physiology and behavior of molluscs [34], survival of echinoderms [40, 41] and crustaceans [30], stress response in sea urchins [44, 45], and gene expression in sea urchins [43, 45]. Early life history stages are thought to be particularly vulnerable [46], and recently documented declines in the growth of Caribbean coral recruits has given rise to the speculation that climate change and ocean acidification may already be interfering with recruitment dynamics [47].

The study of ocean acidification and its effects on early life history stages of corals is relatively new. Nonetheless, several published studies are available investigating the effects of elevated pCO2 on early developmental stages, including sexual reproduction, larval settlement, metabolism, algal symbiosis, survival, and postsettlement growth and calcification (Table 1). The present paper synthesizes and reviews these studies to formulate a basic understanding of how coral recruitment may respond to ocean acidification. For areas that are deficient in studies and for which a robust assessment is not possible, lessons learned from studies conducted on more thoroughly studied taxa (e.g., mollusks, echinoderms) are used to supplement the coral literature and to provide guidelines for future experiments.

2. Sexual Reproduction

Very little information is available regarding the effects of ocean acidification on sexual reproduction in corals. Evaluating effects of acidification on gamete development is difficult as gametogenesis can extend over 9–11 months for some species [48, 49], and maintaining colonies under experimental conditions for this period of time can prove challenging. Nonetheless, available studies indicate that gamete production may show resistance to acidification, although this question deserves further attention. Montipora capitata colonies grown under acidified conditions (+365 μatm pCO2) for 6 months did not show a decrease in gamete production compared to controls [50]. Similarly, normal gametogenesis was observed in Oculina patagonica and Madracis pharensis following 12 months exposure to acidified conditions (pH 7.3, 7.6, 8.0, 8.3) [51]. While gametogenesis may proceed normally, a recent study found that spawning female corals are significantly more susceptible to the negative effects of ocean acidification than spawning male corals [52], leading the authors to conclude that the energetically costly process of egg production leaves little energy available to the coral to sustain “normal” calcification rates in the face of ocean acidification [53].

Fertilization studies indicate that elevated pCO2 negatively affects fertilization success of at least two species of coral, Acropora palmata [28] and Montastraea faveolata [54], but in these studies the effect of pCO2 was dependent on the sperm concentration (discussed further below). Acidification has been shown to have varying effects on the fertilization rate of other marine invertebrates. Elevated pCO2 negatively affects fertilization success in the oyster Saccostrea glomerata [25, 26], and the urchins, Echinometra mathaei, Hemicentrotus pulcherrimus ([22], although significant effects were only observed when acidification was severe: 5,000–10,000 ppm) and Strongylocentrotus franciscanus [23]. However, fertilization is unaffected by elevated pCO2 in the oyster Crassostrea gigas [27]. Interestingly, multiple studies on a single urchin species, Heliocidaris erythrogramma, yield inconsistent results—Havenhand et al. [20] showed that fertilization is negatively affected by pCO2 while Byrne et al. [24, 55] did not observe an effect.

2.1. Experimental Design

While differences in results among studies may be partially attributable to species-specific sensitivities, it is likely that methodological differences play a role. Multiple factors can interact to influence fertilization success in broadcast-spawning organisms, including, but not limited to, sperm-egg contact time, gamete compatibility (i.e., polyandry versus single male-female crosses), gamete aging, sperm velocity and motility, egg size, and sperm concentration (reviewed in [23, 56]). While most studies do not provide sufficient detail in the methods to evaluate the role that some of these variables play in determining experimental results, details regarding sperm concentrations are consistently reported, and the interaction between treatment effect and sperm concentration deserves further consideration here.

For two studies conducted on corals, the magnitude of the pCO2 effect was dependent on the sperm concentration. For A. palmata, elevated pCO2 had little to no effect on fertilization at sperm concentrations that have previously been identified as “optimal”, that is, achieving high fertilization success in laboratory experiments (approximately 106 sperm mL−1); however, as sperm concentration declined, the effect of pCO2 was exacerbated [28]. Similar results were obtained for Montastraea faveolata [54]. Results of both experiments indicate that acidification does not alter the maximum achievable percent fertilization but rather affects fertilization efficiency. In both studies, elevated pCO2 increased sperm limitation such that higher sperm concentrations were required to achieve comparable fertilization rates to controls.

Sperm concentration-specific effects of pCO2 on fertilization success have also been documented for a sea urchin, Strongylocentrotus franciscanus [23]. Similar to M. faveolata, pCO2 decreased fertilization efficiency (i.e., increased sperm limitation); elevated pCO2 also reduced the ability of urchin eggs to successfully block fertilization by multiple spermatozoa, that is, polyspermy, which inhibits embryo development [23]. Interactions between sperm concentration and treatment effect have also been acknowledged in ecotoxicology studies, where copper toxicity increased with decreasing sperm concentration in both sea urchins [57] and intertidal polychaete worms [56]. Recently, Byrne et al. [24] reported no effect of pCO2 on fertilization success of a sea urchin, Heliocidaris erythrogramma, across a range of sperm concentrations, indicating that fertilization in some species may be resistant to acidified seawater.

These studies underscore the need for caution when designing and interpreting experiments testing the effects of CO2 (and other environmental pollutants) on the fertilization of corals and other broadcast-spawning marine invertebrates. Since the probability of detecting a treatment effect may depend on the sperm concentration and how the fertilization curve changes under elevated pCO2 [23], to accurately assess the effect of elevated pCO2 on fertilization kinetics, it is critical to use a broad range of sperm concentrations which encompasses concentrations that are ecologically relevant for the study species. Employing multiple sperm concentrations also lends insight to the mechanism(s) responsible for observed reductions in fertilization [23, 56], information that is not discernable from a single concentration.

Unfortunately, many recent studies employ a single sperm concentration [20, 22, 25, 26, 55], severely limiting our ability to make useful predictions about the likely impact of acidification on sexual reproduction. In many cases, the chosen sperm concentration has previously been identified as “optimal”, that is, producing maximum fertilization success in the laboratory. However, the ecological relevance of “optimal” sperm concentrations is not well understood, as fertilization conditions in nature are poorly documented and likely highly variable. The few studies that have quantified in situ sperm concentrations for corals indicate that while “optimal” concentrations can be observed under certain circumstances, sperm concentration and fertilization rates are highly variable in both space and time [58]. For example, Omori et al. [59] reported sperm concentrations of 106 sperm mL−1 one hour after spawning on a reef flat with ~30% coral cover during calm weather conditions. However, concentrations rapidly declined and were approximately 0 within 6 h of spawning. Because sperm concentration depends on population density, time after spawning, wind and water turbulence, amongst other factors, identifying a single concentration that is both suitable for laboratory experiments and ecologically relevant is complex. Additional concerns regarding the use of a single sperm concentration in fertilization studies (e.g., inability to detect treatment effects due to underlying levels of polyspermy) are discussed in Hollows et al. [56] and Marshall [60].

2.2. Mechanism behind Acidification-Induced Reductions in Fertilization Success

Acidification-induced changes to the fertilization curve may be due to physiological effects on the sperm, egg, or both. For many marine invertebrates, including corals, sperm flagellar motility is likely initiated when intracellular pH ([pH]i) is elevated and suppressed when [pH]i decreases (absolute values for [pH]i are not available) [61]. A recent study showed that flagellar motility of Acropora digitifera sperm was significantly reduced when seawater pH decreased by 0.3 units (8.0 to 7.7). The authors conclude that an increase in [H+] outside of the cell interferes with [pH]i, inhibiting sperm motility and compromising the ability of sperm to move towards unfertilized eggs [21]. Similar results were obtained for a sea cucumber, Holothuria spp. [21]. Havenhand et al. [20] found that reducing the pH of seawater by 0.4 pH units significantly reduced swimming speeds and percent motility of sea urchin sperm, Heliocidaris erythrogramma. These results are consistent with a previous study demonstrating that reduced seawater pH affects [pH]i in sea urchin sperm, inhibiting mitochondrial respiration and motility [62]. Conversely, elevated pCO2 does not affect sperm motility in the oyster Crassostrea gigas [27], demonstrating that sperm of some species/taxa may be resistant to seawater acidification.

The fertilization potential of eggs may also be influenced by changes to [pH]i and/or increased susceptibility to polyspermy [23]. While the fertilization process in corals is poorly understood, egg-derived sperm attractants have been described in at least one coral species, Montipora digitata [63], and a recent study observed that sperm motility increases in the vicinity of eggs prior to fertilization and decreases following fertilization [61]. Morita et al. [61] hypothesize that coral eggs secrete motility-inducing substances that increase sperm [pH]i prior to fertilization and motility-suppressing substances immediately following fertilization to prevent polyspermy. Unlike many marine invertebrates, fertilization membranes to prevent polyspermy have not been described in coral eggs [61, 64]. While the effect of acidification on susceptibility to polyspermy has not yet been evaluated in corals, acidification-induced susceptibility to polyspermy has long been documented in other marine invertebrate taxa, though effects are typically only observed when acidification is severe. As early as 1924, researchers noted that sea urchin eggs (Arbacia spp.) fertilized in acidic conditions (pH 7.2) showed higher rates of polyspermy compared to pH 7.4–9.8 [65]. In 1932, Tyler and Schultz demonstrated that fertilization in the marine worm Urechis caupo is more susceptible to decreased pH than later stages of development: exposure to acidified seawater, pH 7.2, prevents fertilization; however, if embryos are placed in acidic conditions immediately following fertilization, they undergo normal cleavage and development at pH values as low as 6.4 [66]. These results led to the hypothesis that acidification interferes with the initial stages of the fertilization reaction, namely, the block to polyspermy [66]. Smith and Clowes [65] concluded that this effect may be due to CO2/H+ interference with the formation of a fertilization membrane. Recently, Reuter et al. [23] observed increased susceptibility to polyspermy in sea urchin eggs exposed to 1800 ppm pCO2, but no significant differences were observed at 800 ppm. In sea urchin eggs, [pH]i increases immediately following insemination [67], triggering the initiation of embryonic development [68]; it is also possible that acidification interferes with [pH]i, inhibiting development. Because coral eggs may not have a fertilization membrane, the existence of a pCO2 effect on fertilization potential and the mechanism behind such an effect may differ from other marine invertebrate taxa; nonetheless, the potential for acidification to decrease fertilization potential of coral eggs and/or embryo viability is an area of research that has yet to be investigated and deserves consideration.

3. Metabolism

Significant reductions in metabolism have been reported for larvae of at least one brooding coral species, Porites astreoides, following exposure to acidified conditions [38]. During a 2 h exposure, larval metabolism decreased by 27–63% at pCO2 levels that are projected to occur by the middle (560 μatm) and end (800 μatm) of this century. Using Acropora digitifera planulae, Nakamura et al. [69] observed a trend of decreasing oxygen consumption with increasing pCO2 following both 3 and 7 days of exposure; however these results were not significant. The authors acknowledge the low statistical power (0.30) of their experiment, and results are, therefore, inconclusive [69]. Further studies are needed concerning the effects of elevated pCO2 on larval respiration. Comparisons of brooding (containing zooxanthellae) and spawning (devoid of zooxanthellae) larvae will shed light on whether certain reproductive strategies are more or less susceptible to acidified conditions during the planktonic stage.

Metabolic suppression resulting from exposure to acidified conditions has previously been reported to occur in a variety of adult marine invertebrates, including crabs [70], squid [71], worms [72], bivalves ([73], adult and juveniles), pteropods and amphipods (reviewed in [74]). Culturing sea urchin larvae in acidified conditions resulted in the downregulation of several genes involved in aerobic metabolism [43, 45]. Acidification reduces the heart rate of juvenile snails ([34], Littorina obtusata). Interestingly, acidification increases metabolism in juvenile oysters (Crassostrea virginica, [75]).

Metabolic suppression is considered an adaptive strategy for the survival of short-term hypercapnia and hypoxia (reviewed in [74]); however, slowed metabolism is generally achieved by halting energy-expensive processes, such as protein synthesis [76, 77], and therefore, if sustained, may lead to reductions in growth and reproductive potential [74]. Thus, metabolic suppression is not considered to be advantageous under chronic elevations of CO2, such as ocean acidification [77, 78].

Depressed metabolic rates in invertebrate larvae may hold implications for larval fitness and motility, thereby limiting dispersal and settlement rates. Recent work demonstrated that oxygen consumption and energy use in coral larvae (Acropora intermedia) peaks ~5 days after spawning, when larvae begin actively swimming and exploring [79]. During the planktonic dispersal phase, larvae of many species actively explore and change their position in the water column to locate ideal settlement sites [80, 81] and possibly influence horizontal transport and dispersal [82]. If metabolic suppression during the planktonic stage translates into decreased larval motility, the ability of larvae to regulate their vertical position in the water column may be compromised, thereby impacting dispersal and settlement potential.

4. Settlement and Metamorphosis

Larvae of many coral species actively select a site of permanent attachment using external chemical cues that induce metamorphosis [8386]. Both positive settlement cues from crustose coralline algae (CCA) and/or microbial biofilms and settlement interference by turf algae have been previously documented [83, 8789]. Environmental factors that alter or interfere with these cues have the potential to greatly impact coral recruitment and future population dynamics. Given that larval settlement can be influenced by conditions experienced in the plankton and by positive or negative cues on the benthos or in the overlying water column [11], to accurately assess whether acidification interferes with settlement, we must assess effects on larval condition, substrate condition, and the interaction between the two.

At least three studies have demonstrated that if settlement cues are present, acidified seawater does not directly impair the physiological ability of coral larvae to undergo metamorphosis and attach to the substrate [35, 38, 90]. Contrary to these findings, Nakamura et al. [69] observed a significant reduction in settlement of Acropora digitifera larvae following just 2 h exposure to acidified seawater. It is important to note that settlement substrates were not used in this experiment, and settlement was induced by the use of the coral metamorphosis-inducer peptide Hym-248, rather than using natural settlement inducers (e.g., CCA). Thus, the ecological significance of the results is not known. Kurihara [46] reported no effect of acidification (1000 μatm pCO2) on settlement by Acropora tenuis. However, methods were not provided for this experiment, and it is, therefore, difficult to assess the implications of these results. For other marine invertebrates, acidification has been shown to directly delay metamorphosis in at least 3 species of marine bivalves, including Crassostrea virginica, Argopecten irradians, and Mercenaria mercenaria [91, 92].

Studies that have evaluated the effect of acidification on both larval condition and substrate condition indicate that acidification has the capacity to influence larval settlement, but may primarily do so indirectly, by altering the substrate community composition and the availability of biological and chemical settlement cues [28, 38]. Albright and Langdon [38] showed that elevated CO2 causes changes in the epilithic algal community of settlement substrates; as pH declined, taxa known to facilitate larval settlement of some coral species (e.g., CCA) were replaced by alternate algal species (e.g., consortia dominated by diatoms and other chromophytes), resulting in reduced settlement of Porites astreoides larvae. These shifts in benthic community composition are consistent with previously published work demonstrating that CCA recruitment and growth decreases with decreasing pH [50, 93, 94]. CCA precipitates high-magnesium calcite 13–15% MgCO3 [95], a mineral phase of calcium carbonate that is 1.2–5 times as soluble as aragonite [96, 97], rendering it particularly vulnerable to acidified conditions. The potential for acidification to indirectly affect settlement success by interfering with the availability of settlement cues is an important area of research that deserves further investigation.

While CCA and/or associated biofilms induce metamorphosis of some coral species, presence of CCA is not an obligate trait for settlement by all species. For example, while Acropora palifera larvae only metamorphose in the presence of coralline red algae [98], and Goniastrea retiformis preferentially settle onto substrates covered with CCA [99], Stylophora pistillata larvae are able to metamorphose in unfiltered seawater and onto glass coverslips [98], and Stylaraea punctata larvae prefer biofilmed rubble to CCA [99]. If acidification primarily affects settlement by altering the substrate community composition and the availability of settlement cues, then species that have more stringent settlement requirements (i.e., surface contact with CCA and/or associated biofilms) may be preempted by species that are capable of settling without these cues. In a 10-month experiment, Jokiel et al. [50] found that despite drastic reductions (86%) in percent cover of CCA (acidified to 365 μatm above control values), Pocillopora damicornis larvae were still able to recruit at levels comparable to controls. Additionally, not all species of CCA induce larval settlement. Harrington et al. [100] showed that Acropora tenuis and A. millepora larvae settled at different rates in response to different species of coralline algae. Similarly, Ritson-Williams et al. [101] showed that A. palmata and A. cervicornis larvae demonstrate different behavioral responses to different CCA species. Evaluating species-specific sensitivities of CCA to acidification will facilitate a better understanding of potential shifts in benthic community composition and the implications for coral settlement and recruitment.

5. Postsettlement Growth and Calcification

The majority of available studies evaluating the effects of ocean acidification on early life history stages of corals assess postmetamorphic growth and calcification. General consensus from these studies is that primary polyp growth is hindered by increasing pCO2 and decreasing saturation state (Figure 1), with at least 7 species of coral exhibiting acidification-induced reductions in post-metamorphic calcification and/or growth: Porites astreoides [35, 38, 39], P. panamensis [90], A. digitifera, A. tenuis [37], A. palmata [28], Agaricia agaricites [54], and Favia fragum [36, 39, 54]. Acidification may also delay the onset of calcification and alter crystal morphology and composition [36]. These findings are consistent with the hypothesis that calcification depends strongly on saturation state, as has been documented for adults of several coral species and reef communities [102, 103].

Albright et al. [35] reared Porites astreoides recruits for 1 month in seawater manipulated with acid-addition and observed drastic declines in post-metamorphic growth with decreasing . Skeletal growth, as measured by the increase in cross-sectional area, was reduced by 45–84% as CO2 increased and decreased. The study was repeated using an improved experimental system (CO2 bubbling and natural lighting); again, growth was positively correlated with saturation state (negatively correlated with CO2), although reductions in growth were less severe, 16–35% [38].

Cohen et al. [36] reared primary polyps of Favia fragum in seawater manipulated with acid-addition for 8 days and found a reduction in the size and weight of the primary corallite with decreasing . Interestingly, recruits were capable of calcifying in strongly undersaturated solutions ( ), suggesting that, for some species, biological control may partially abate thermodynamically unfavorable conditions. Despite the ability to calcify in under saturated seawater, several negative effects were observed: the onset and rate of calcification were significantly delayed; crystal morphology was altered as the crystal aspect ratio (i.e., ratio of crystal length to crystal width) decreased with decreasing saturation state [53]; crystal organization became increasingly random (i.e., less densely packed); and shifts in mineralogy occurred as Sr/Ca ratios increased and Mg/Ca ratios decreased. Acidification-induced shifts in crystal morphology and organization were also reported for P. astreoides recruits [54]; similar effects were observed when seawater chemistry was manipulated with HCl and CO2 gas. Altered skeletal structure of new recruits may render them more susceptible to mechanical damage, reducing their ability to grow rapidly enough to ensure survival [36].

De Putron et al. [39] observed a nonlinear effect of on early calcification (corallite weight) of both P. astreoides and F. fragum: calcification was unaffected at saturation states greater than 2.5–2.8; however, drastic reductions in calcification were observed in both species when dropped below this threshold. The same effect was observed when seawater was acidified with HCl and CO2 gas.

Suwa et al. [37] observed that Acropora digitifera polyps reared for 10 days at low pH (pH 7.3 and 7.6) were significantly smaller than those reared at ambient conditions (pH 8.0), although it is unclear whether polyp “size” measured coral tissue and/or skeleton. Kurihara [46] reported “disturbed” and “malformed” Acropora tenuis polyps following settlement; however, methods and quantitative results were not provided for this study, and it is, therefore, difficult to interpret the results. Jokiel et al. [50] observed no difference in the size of Pocillopora damicornis settlers that recruited to acidified and control mesocosms over a 10-month period, indicating that some species may show higher levels of resistance to acidification.

Anlauf et al. [90] reported a temperature-dependent effect of acidification on calcification of Porites panamensis recruits. Acidification (−0.2 to −0.25 pH units) alone decreased calcification by only 3%, but acidification combined with warming (+1°C) resulted in a 30% reduction in calcification rates. Interestingly, a 4°C warming (25–29°C) had no effect on the response of F. fragum recruits to decreased [39]. An interaction between temperature and acidification has previously been shown to influence the growth response of adult corals [104] and is a critical area of research that deserves further attention.

Larval and juvenile calcification in some marine invertebrates may be more sensitive to acidification than adults, as has been shown for at least one bivalve and one echinoderm (reviewed in [46]). Maier et al. [105] showed that calcification in younger polyps of Lophelia pertusa was more sensitive to acidified seawater than older polyps. Waldbusser et al. [106] found a size dependent pH effect on calcification in juvenile hard clams (Mercenaria spp.), where smaller individuals were more heavily impacted than larger ones. For some marine invertebrates, the heightened sensitivity of early life history stages may, in part, be due to the presence of amorphous calcium carbonate (ACC) precursors that can occur at the onset of calcification and later stabilize into less soluble forms of CaCO3. ACC is 30 times more soluble than calcite [107, 108], rendering it particularly vulnerable to acidified conditions. Many marine invertebrates undergo ontological changes in mineral composition, from ACC to aragonite and sometimes calcite. Larval spines of urchins form via an ACC precursor that later stabilizes into calcite [109, 110]; the oyster, Crassostrea virginica secretes aragonite in the larval stages and calcite in the adult stage [111]; similarly, shell formation in molluscan larvae involves an initial, transient ACC phase [112, 113], and it has been suggested that the same may be true for corals [114], but see [115].

Slowed postsettlement growth resulting from exposure to acidification may translate into increased juvenile mortality. Risk of coral mortality has been shown to be inversely proportional to juvenile growth rate and colony size [116118] with up to a 20% increase in survivorship associated with a 0.5 mm increase in diameter of 4-month-old juveniles of certain species [118]. While postsettlement mortality was not reported for any of the above growth experiments, it is important to note that mortality rates observed in laboratory studies typically do no approximate survivorship of juveniles in situ. Under laboratory conditions, factors known to affect early survivorship on the reef (e.g., competition with algae and other benthic organisms, sedimentation effects, predation) are often controlled or eliminated to minimize influences on growth other than the desired treatment effect. Therefore, survivorship in the laboratory may overestimate survivorship on the reef.

In addition to potential increases in juvenile mortality, both the onset of sexual maturity [119, 120] and fecundity [117, 121, 122] of reef-building corals are known to be a function of colony size. Therefore, depressed growth would likely result in longer time spent in juvenile (nonreproductive) life stages, which, in combination with adult loss, would shift population structures toward dominance by smaller size classes, ultimately reducing effective population sizes, population fecundity, and the resilience of reef-building corals [123].

6. Algal Symbiosis

Knowledge of the effects of ocean acidification on the establishment of coral-algal symbioses is based on relatively few studies. Suwa et al. [37] showed that acidification by 0.4 and 0.7 pH units delayed the onset of symbiosis in Acropora digitifera primary polyps. This effect was temporary (2 days maximum), and all polyps contained algae within four days of infection. The ecological significance of such a delay in the onset of symbiosis is unknown. Anlauf et al. [90] found that temperature, but not CO2, significantly reduced the number of zooxanthellae in primary polyps of Porites panamensis following 42 d exposure to pH 7.8. Further studies are needed to assess if ocean acidification influences the establishment and functionality of the symbiotic relationship in newly settled corals.

7. Survivorship

While acidification may impose numerous sublethal effects on early stages of corals, most studies indicate that mortality does not directly result from exposure to acidified seawater [37, 69, 90]. Suwa et al. [37] found that while survival of Acropora tenuis larvae was significantly higher at pH 7.3 than pH 7.6, survival of A. digitifera larvae did not differ significantly among pH treatments. The lack of a consistent pattern led the authors to conclude that survivorship of coral larvae was not affected by acidified seawater. Nakamura et al. [69] found no effect of CO2-induced acidification (pH 7.3, 7.6, 8.0) on survivorship of Acropora digitifera larvae following 3 and 7 days of exposure. Anlauf et al. [90] observed near 100% survival of Porites panamensis recruits reared at both pH 7.8 and pH 8.0 over the course of 42 days.

Acidification-induced mortality has been reported for other species of marine invertebrates. The most striking example was reported by Dupont et al. [40], where a pH reduction of 0.2 units induced 100% mortality of brittlestar (Ophiothrix fragilis) larvae within 8 days. Mortality following exposure to acidified seawater has also been reported for other echinoderms, including four urchin species—one tropical (Tripneustes gratilla), two temperate (Pseudechinus huttoni, Evechinus chloroticus), and one polar (Sterechinus neumayeri) [41]. Shirayama and Thornton [124] reported increased mortality in one of two studies for two species of urchins, Hemicentrotus pulcerrimus and Echinometra mathaei, and one gastropod Strombus luhuanus. Larval survivorship of several shellfish species also decreases with increasing acidity: Saccostrea glomerata [125], Crassostrea virginica, Mercenaria mercenaria, and Argopecten irradians [91, 92]. Mortality was reported for copepod nauplii (Acartia erythraea, [126]) exposed to OA scenarios, though significant differences were noted only when acidification was severe (+5,000 and +10,000 ppm CO2).

8. Considerations for Future Experiments

Because ocean acidification is a young and rapidly developing field of science, it is fitting to reflect on aspects of experimental design and methodology that may help guide future studies. Facets that have already been discussed, such as the use of multiple sperm concentrations in fertilization studies, are not revisited, but there are several other aspects of experimental design that deserve consideration. Interspecies and intertaxa comparisons are often complicated by variations in methodologies (e.g., acid addition versus CO2 gas bubbling to manipulate seawater carbonate chemistry). Some studies discussed here indicate little difference in biological response between acid-manipulated experiments and CO2 gas-manipulated experiments [39]. Nonetheless, efforts should be made to comply with the recently released Guides to Best Practices [127, 128] to allow for standardized methodologies that facilitate more meaningful comparisons between studies. Inclusion of power analyses for studies with no treatment effect would provide confidence that results are indicative of resistance to acidification, as opposed to a limitation in the experimental design.

While the suitability of techniques for manipulating seawater chemistry has received recent consideration [127], little attention has been given to the relevance of experimental conditions to the natural environment. Unlike open ocean waters, coral reefs experience large diurnal and seasonal fluctuations in carbonate chemistry that are primarily driven by biology (e.g., photosynthesis and respiration) [129]. Despite this, many experimental seawater systems employ constant treatment conditions that eliminate inherent variability. These systems generally target pCO2/pH values that are projected to occur in coming centuries. These projections are based on air-sea fluxes in the open ocean and their relevance to shallow-water ecosystems such as coral reefs is not well understood [129]. The scientific community has a poor understanding of the importance of background variability in determining an organism’s response to an environmental stressor. While variability may not be a concern for ephemeral life history stages such as fertilization, attempts should be made to incorporate variability into long-term experiments (e.g., growth, survivorship) to both mimic the natural environment and cater to more realistic organism responses. This can be achieved through the use of experimental designs/systems that superimpose treatment levels on top of natural trends in temperature and CO2.

9. Conclusion

The studies reviewed here demonstrate that ocean acidification has the potential to affect sexual reproduction and multiple early life history stages of corals that are critical to reef persistence and resilience. While further studies are essential, available information indicates that affected processes may include sperm motility and fertilization success, larval metabolism, larval settlement, and postsettlement growth and calcification. These effects may occur via both direct (e.g., depressed sperm motility, fertilization, larval respiration, growth and calcification) and indirect (e.g., changes in substrate conditions that favor settlement) pathways. Implications of these effects include reduced larval supply, a major determinant of recruit density [10, 130], and depressed recruitment, which will likely compromise coral reef resilience, or the ability of reefs to recover from disturbance. Slowed growth may trigger numerous repercussions, including, but not limited to, elevated juvenile mortality and shifts in population size structure.

Sessile, broadcast-spawning organisms face several population bottlenecks during early life, including fertilization, settlement, and early postsettlement survivorship and growth [130]. As a result, natural larval and early juvenile mortality of many marine invertebrates often exceeds 99% [131, 132]. For corals, research using artificial settlement substrates indicates that coral recruit survivorship during the first year is extremely low, generally reported to be as low as 0.2–6.0% survivorship, depending on the species and environment [133, 134]. Stochastic events or chronic stressors that further reduce survivorship during these critical stages have the potential to significantly alter future population sizes [130, 131]. Although ocean acidification is now recognized as a substantial threat to marine calcifiers and their ability to secrete calcium carbonate shells and/or skeletons, the studies reviewed here demonstrate that increasing pCO2 has the potential to impact multiple life history stages of corals, including critical processes independent of calcification.

Negative impacts on successive life history stages may cumulate in such a way that the overall effect on recruitment is severe. For example, results of studies conducted with the threatened Caribbean elkhorn coral, Acropora palmata, indicate that ocean acidification has the potential to reduce fertilization success by 12-13% (averaged across all sperm concentrations) and to decrease settlement success by 45–69% at pCO2 concentrations expected for the middle and end of this century. The compounding effect of ocean acidification on these early life history stages translates into a 52–73% reduction in the number of larval settlers on the reef. The net impact on recruitment will likely be even greater, given that depressed postsettlement growth may translate into elevated rates of postsettlement mortality [28]. Given the long generation time of corals, multigenerational studies are difficult, if not impossible; however, an attempt should be made to conduct studies evaluating multiple life history stages to allow for the evaluation of cumulative and/or carryover effects [135].

Future research should investigate the existence of genotypes and/or species that show resistance to pH/pCO2 changes at multiple life history stages (e.g., fertilization, settlement, growth), as recruitment failure in these species may not be multiplicative. Within species that demonstrate sensitivity to ocean acidification, additional work needs to be done; there is a need to further investigate organisms’ abilities to acclimatize and/or adapt to elevated pCO2 given prolonged exposure. Although early life history stages are posited to be the most sensitive, the most sensitive life history stage may differ amongst species [46], and variation in life history characteristics (e.g., brooders versus spawners) may prove some species more resilient than others [136]. Focusing efforts on the protection and cultivation of more adaptable species or genotypes may improve the effectiveness of coral preservation and restoration efforts.


The authors would like to thank B. Mason and four anonymous reviewers for constructive feedback that greatly improved this paper. Portions of this paper were supported through work conducted at the University of Miami, Rosenstiel School of Atmospheric Science.