How does rising atmospheric CO2 affect marine organisms?

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Ocean Acidification of Corals (Laboratory Studies) -- Summary
Over the years, a number of researchers have postulated that many of Earth's corals are destined to die, with some species even facing extinction, because of the hypothesized connection between the ongoing rise in the air's CO2 content and reduced rates of coral calcification (Buddemeier, 1994; Buddemeier and Fautin, 1996a,b; Gattuso et al., 1998; Buddemeier, 2001). Kleypas et al. (1999), for example, calculated calcification rates of tropical corals should already have declined by 6 to 11% or more since 1880, as a result of the concomitant increase in atmospheric CO2 concentration; and they predict reductions could reach 17 to 35% by 2100, as a result of expected increases in the air's CO2 content over the coming century. Likewise, Langdon et al. (2000) calculated a decrease in coral calcification rate of up to 40% between 1880 and 2065.

The IPCC has extensively opined about the threat of ocean acidification on corals, claiming in its most recent assessment report that:

    Elevated temperature along with ocean acidification reduces the calcification rate of corals (high confidence), and may tip the calcium carbonate balance of reef frameworks towards dissolution (medium evidence and agreement). (p. 67 of the Technical Summary, Working Group II, IPCC Fifth Assessment Report, dated March 28, 2013)

    Ocean acidification will cause a decrease of calcification of corals, which will cause not only a reduction in the coral's ability to grow its skeleton, but also in its contribution to reef building (high confidence). (p. 73 of the Technical Summary, Working Group II, IPCC Fifth Assessment Report, dated March 28, 2013)

    Ocean warming and acidification expected under RCP 8.5 will reduce calcification, elevate coral mortality and enhance sediment dissolution (high confidence; Manzello et al., 2008). Coral reefs may stop growing and start dissolving when atmospheric CO2 reaches 560 ppm due to the combined effects of both drivers (medium evidence). (p. 19 of Chapter 5. Coastal Systems and Low-Lying Areas, Working Group II, IPCC Fifth Assessment Report, dated March 28, 2013)

In contrast to the dire assessment of the IPCC, the material presented in this summary reveals such predictions are tenuous at best, and at worst may be wholly incorrect. As Idso et al. (2000) have noted, coral calcification is more than a physical-chemical process described by a set of well-defined equations. It is a biologically-driven physical-chemical process that may not be amenable to explicit mathematical description. They state, for example, "photosynthetic activity of zooxanthellae is the chief source of energy for the energetically-expensive process of calcification," and much evidence suggests "long-term reef calcification rates generally rise in direct proportion to increases in rates of reef primary production." They also note "the calcium carbonate saturation state of seawater actually rises with an increase in temperature, significantly countering the direct adverse oceanic chemistry consequences of an increase in atmospheric and/or hydrospheric CO2 concentration." These simple facts led them to conclude "the negative predictions of today could well be replaced by positive predictions tomorrow."

And indeed those negative predictions are being replaced (just not quite yet by the IPCC). As revealed in the material below, the results of numerous scientific studies now point toward a much more optimistic view of the future for the planet's corals. This summary examines what researchers have learned about the topic from several laboratory-based studies.

Suwa et al. (2010) employed controlled infusions of pure CO2 to create mean pH values of 8.03, 7.64 and 7.31 in filtered seawater that flowed continuously through three sets of multiple tanks into which they had introduced the gametes of two Acropora coral species (A. digitifera and A. tenuis) they had collected during a natural spawning event, after which (seven days later) they determined their percent survival. Then, after ten more days, they documented the size of the developing polyps; and after 14 days they documented the percentage of polyps that had acquired zooxanthellae that the researchers had collected from the giant clam T. crocea and released into the several treatment tanks.

Results indicated that "A. digitifera larval survival rate did not differ significantly among pH treatments," and the graphs of their data indicate that survivorship in A. tenuis was actually about 18.5% greater in the lowest pH (highest CO2) treatment than in the ambient seawater treatment. At the end of the subsequent ten-day study, however, polyp size was reduced in the lowest pH treatment, but by only about 14%, which is not too bad for an atmospheric CO2 concentration reported by the authors to be in the range of 2115-3585 ppm. And in the A. tenuis coral, this reduction in individual size was more than compensated by the even greater percentage increase in survivorship. In addition, after only four days of being exposed to the zooxanthellae derived from giant clams, all polyps in all treatments had acquired a full complement of the symbiotic zooxanthella.

In discussing their findings, the seven scientists say they indicate that "the survival of coral larvae may not be strongly affected by pH change," or "in other words," as they continue, "coral larvae may be able to tolerate ambient pH decreases of at least 0.7 pH units," which, in fact, is something that will likely never occur, as it implies atmospheric CO2 concentrations in the range of 2115 to 3585 ppm. In addition, if such high concentrations ever were to occur, they would be a long, long time in coming, giving corals far more than sufficient time to acclimate -- and even evolve (Idso and Idso, 2009) -- to adequately cope with the slowly developing situation.

Also studying the effects of ocean acidification on an Acropora species was Takahashi and Kurihara (2013), who set out to measure the rates of calcification, respiration and photosynthesis of the tropical coral Acropora digitifera - along with the coral's zooxanthellae density - under near-natural summertime temperature and sunlight conditions for a period of five weeks. Results of their analysis revealed that these "key physiological parameters" were not affected by either predicted mid-range CO2 concentrations (pCO2 = 744 ppm, pH = 7.97, Ωarag = 2.6) or by high CO2 concentrations (pCO2 = 2,142 ppm, pH = 7.56, Ωarag = 1.1) over the 35-day period of their experiment. In addition, they state that there was "no significant correlation between calcification rate and seawater aragonite saturation (Ωarag)" and "no evidence of CO2 impact on bleaching."

Kreif et al. (2010) collected two colonies of massive Porites corals (which form large multi-century-old colonies and calcify relatively slowly) and four colonies of the branching Stylophora pistillata coral (which is short-lived and deposits its skeleton rather rapidly) from a reef adjacent to the Interuniversity Institute for Marine Science in Eilat (Israel) at the northern tip of the Red Sea; and they grew fragments of these corals in 1000-liter tanks through which they pumped Gulf of Eilat seawater that they adjusted to be in equilibrium with air of three different CO2 concentrations (385, 1904 and 3970 ppm), which led to corresponding pH values of 8.09, 7.49 and 7.19 and corresponding aragonite saturation state (Ωarag) values of 3.99, 1.25 and 0.65. Then, after an incubation period of six months for S. pistillata and seven months for the Porites corals, several fragments were sampled and analyzed for a number of different coral properties; and fourteen months from the start of the experiment, fragments of each coral species from each CO2 treatment were analyzed for zooxanthellae cell density, chlorophyll a concentration, and host protein concentration.

The results of the study revealed that "following 14 months incubation under reduced pH conditions, all coral fragments survived and added new skeletal calcium carbonate, despite Ωarag values as low as 1.25 and 0.65." This was done, however, at a reduced rate of calcification compared to fragments growing in the normal pH treatment with a Ωarag value of 3.99. Yet in spite of this reduction in skeletal growth, they report that "tissue biomass (measured by protein concentration) was found to be higher in both species after 14 months of growth under increased CO2." And they further note that the same phenomenon had been seen by Fine and Tchernov (2007), who, as they describe it, "reported a dramatic increase (orders of magnitude larger than the present study) in protein concentration following incubation of scleractinian Mediterranean corals (Oculina patagonica and Madracis pharencis) under reduced pH," stating that "these findings imply tissue thickening in response to exposure to high CO2." Also, in a somewhat analogous situation, Krief et al. report that "a decrease in zooxanthellae cell density with decreasing pH was recorded in both species," but that "this trend was accompanied by an increase in chlorophyll concentration per cell at the highest CO2 level."

In discussing their intriguing findings, the Israeli, French and UK researchers say "the inverse response of skeleton deposition and tissue biomass to changing CO2 conditions is consistent with the hypothesis that calcification stimulates zooxanthellae photosynthesis by enhancing CO2 concentration within the coelenteron (McConnaughey and Whelan, 1997)," and they write that "since calcification is an energy-consuming process ... a coral polyp that spends less energy on skeletal growth can instead allocate the energy to tissue biomass," citing Anthony et al. (2002) and Houlbreque et al. (2004). Thus, they suggest that "while reduced calcification rates have traditionally been investigated as a proxy of coral response to environmental stresses, tissue thickness and protein concentrations are a more sensitive indicator of the health of a colony," citing Houlbreque et al. (2004) in this regard as well.

In concluding their paper, Krief et al. say "the long acclimation time of this study allowed the coral colonies to reach a steady state in terms of their physiological responses to elevated CO2," and that "the deposition of skeleton in seawater with Ωarag < 1 demonstrates the ability of both species to calcify by modifying internal pH toward more alkaline conditions." As a result, they further state that "the physiological response to higher CO2/lower pH conditions was significant, but less extreme than reported in previous experiments," suggesting that "scleractinian coral species will be able to acclimate to a high CO2 ocean even if changes in seawater pH are faster and more dramatic than predicted."

Working with branches of Lophelia pertusa - which they collected from reefs off the coast of Norway, and which they describe as "the most common reef framework-forming and ecosystem engineering cold-water coral with a cosmopolitan distribution (Zibrowius, 1980; Cairns, 1994; Freiwald et al., 2004) - Form and Riebesell (2012) conducted a short-term (8-day) experiment and a long-term (178-day) experiment, wherein they employed different atmospheric CO2 treatments to create a range of water pH treatments that ranged from 8.029 to 7.768 in the 8-day study and from 7.944 to 7.755 in the 178-day study, and over which time intervals they measured the corals' growth rates. The findings revealed that "short-term (1-week) high CO2 exposure resulted in a decline of calcification by 26-29% for a pH decrease of 0.1 unit and net dissolution of calcium carbonate." In contrast, however, they discovered that "L. pertusa was capable to acclimate to acidified conditions in long-term (6 months) incubations, leading to even slightly enhanced rates of calcification." And they add that in the long-term low-pH treatment, "net growth is sustained even in waters sub-saturated with respect to aragonite."

Nash et al. (2012) write that "coral reef ecosystems develop best in high-flow environments," but that "their fragile frameworks are also vulnerable to high wave energy." And that is likely why they say that the wave-resistant algal rims, which surround many shallow coral reefs and are predominantly made of crustose coralline algae (CCA), are critical structural elements for the survival of such coral reefs. On the other hand, they also indicate that "concerns have been growing about the susceptibility of CCA to ocean acidification, because CCA Mg-calcite skeletons are more susceptible to dissolution under low pH conditions than are coral aragonite skeletons." But they further state, in this regard, that the recent discovery by Nash et al. (2011) of the stable carbonate known as dolomite in the CCA Porolithon onkodes necessitates a reappraisal of the impacts of ocean acidification on it and other CCAs, such as P. pachydermum.

Taking their own advice, the eleven researchers "carried out dissolution experiments on fragments of CCA that were collected fresh, but then dried, from the Heron Island reef front (Great Barrier Reef, Australia), after which they were exposed to ambient sea water as a control and an enriched CO2 treatment, where "pH ranged from 7.85 to 8.55 (control) and 7.69-8.44 (treatment), tracking natural diurnal changes measured in the lagoon water." From this, Nash et al. (2012) were able to determine that "dried dolomite-rich CCA have 6-10 times lower rates of dissolution than predominantly Mg-calcite CCA in both high-CO2 (~700 ppm) and control (~380 ppm) environments." And they say that they found this stabilizing mechanism to be due to "a combination of reduced porosity due to dolomite infilling and selective dissolution of other carbonate minerals." In commenting on the significance of their finding, due to the fact, as they put it, that "the prevailing theories that Mg-calcites with higher Mg content will undergo greatest dissolution, we were surprised to find a trend in the opposite direction." And since dolomite-rich CCA frameworks are common in shallow coral reefs globally, they conclude "it is likely that they will continue to provide protection and stability for coral reef frameworks as CO2 rises."

Ries et al. (2010) "investigated the impact of CO2-induced ocean acidification on the temperate scleractinian coral Oculina arbuscula by rearing colonies for 60 days in experimental seawaters bubbled with air-CO2 gas mixtures of 409, 606, 903 and 2,856 ppm CO2, yielding average aragonite saturation states (ΩA) of 2.6, 2.3, 1.6 and 0.8." In doing so the authors observed that "following the initial acclimation phase, survivorship in each experimental treatment was 100%," while last of all, in regard to the corals' rates of calcification and linear extension, they say that "no significant difference was detected relative to the control treatment (ΩA = 2.6) for corals reared under ΩA of 2.3 and 1.6," which latter values correspond to pH reductions from current conditions of 0.08 and 0.26, respectively. Based on these findings Ries et al. "propose that the apparent insensitivity of calcification and linear extension within O. arbuscula to reductions in ΩA from 2.6 to 1.6 reflects the corals' ability to manipulate the carbonate chemistry at their site of calcification."

Herfort et al. (2008) note that an increase in atmospheric CO2 will cause an increase in the abundance of HCO3- (bicarbonate) ions and dissolved CO2, and they also report that several studies on marine plants have observed "increased photosynthesis with higher than ambient DIC [dissolved inorganic carbon] concentrations," citing the works of Gao et al. (1993), Weis (1993), Beer and Rehnberg (1997), Marubini and Thake (1998), Mercado et al. (2001, 2003), Herfort et al. (2002), and Zou et al. (2003). In further exploration of the subject, and to see what it might imply for coral calcification, the three researchers employed a wide range of bicarbonate concentrations "to monitor the kinetics of bicarbonate use in both photosynthesis and calcification in two reef-building corals, Porites porites and Acropora sp." This work revealed that additions of HCO3- to synthetic seawater continued to increase the calcification rate of Porites porites until the bicarbonate concentration exceeded three times that of seawater, while photosynthetic rates of the coral's symbiotic algae were stimulated by HCO3- addition until they became saturated at twice the normal HCO3- concentration of seawater.

Similar experiments conducted on Indo-Pacific Acropora sp. showed that calcification and photosynthetic rates in these corals were enhanced to an even greater extent, with calcification continuing to increase above a quadrupling of the HCO3- concentration and photosynthesis saturating at triple the concentration of seawater. In addition, they monitored calcification rates of the Acropora sp. in the dark, and, in their words, "although these were lower than in the light for a given HCO3- concentration, they still increased dramatically with HCO3- addition, showing that calcification in this coral is light stimulated but not light dependent."

In discussing the significance of their findings, Herfort et al. suggest that "hermatypic corals incubated in the light achieve high rates of calcification by the synergistic action of photosynthesis," which, as they have shown, is enhanced by elevated concentrations of HCO3- ions that come courtesy of the ongoing rise in the air's CO2 content. As for the real-world implications of their work, the three researchers note that over the next century the predicted increase in atmospheric CO2 concentration "will result in about a 15% increase in oceanic HCO3-," and they say that this development "could stimulate photosynthesis and calcification in a wide variety of hermatypic corals," a conclusion that stands in stark contrast to the contention of the IPCC.

Another paper focusing on the importance of bicarbonate ions was published two years later by Jury et al. (2010), whose work also provides some thinking as to why some corals show positive responses to ocean acidification in laboratory studies while others do not.

Writing as background for their work, Jury et al. say that "physiological data and models of coral calcification indicate that corals utilize a combination of seawater bicarbonate and (mainly) respiratory CO2 for calcification, not seawater carbonate," but that "a number of investigators are attributing observed negative effects of experimental seawater acidification by CO2 or hydrochloric acid additions to a reduction in seawater carbonate ion concentration and thus aragonite saturation state." Thus, they state there is "a discrepancy between the physiological and geochemical views of coral biomineralization." In addition, they report that "not all calcifying organisms respond negatively to decreased pH or saturation state," and they say that "together, these discrepancies suggest that other physiological mechanisms, such as a direct effect of reduced pH on calcium or bicarbonate ion transport and/or variable ability to regulate internal pH, are responsible for the variability in reported experimental effects of acidification on calcification."

In an effort to shed more light on this conundrum, Jury et al. performed incubations with the coral Madracis auretenra (= Madracis mirabilis sensu Wells, 1973) in modified seawater chemistries, where, as they describe it, "carbonate parameters were manipulated to isolate the effects of each parameter more effectively than in previous studies, with a total of six different chemistries." Results indicated that among-treatment differences "were highly significant," and that "the corals responded strongly to variation in bicarbonate concentration, but not consistently to carbonate concentration, aragonite saturation state or pH." They found, for example, that "corals calcified at normal or elevated rates under low pH (7.6-7.8) when the sea water bicarbonate concentrations were above 1800 ÁM," and, conversely, that "corals incubated at normal pH had low calcification rates if the bicarbonate concentration was lowered."

Jury et al. conclude that "coral responses to ocean acidification are more diverse than currently thought," and they question "the reliability of using carbonate concentration or aragonite saturation state as the sole predictor of the effects of ocean acidification on coral calcification," stating that "if we truly wish to decipher the response of coral calcification to ocean acidification, a firmer grasp of the biological component of biomineralization is paramount."

Also focusing on the question of how ocean acidification impacts the physiological mechanisms that drive calcification, was Venn et al. (2013), which knowledge is needed to predict how corals and other marine calcifiers will respond and potentially acclimate to ocean acidification. According to the authors, in corals, the capacity to regulate pH in the fluid at the tissue-skeleton interface [subcalicoblastic medium (SCM)] and in the calcifying cells [calicoblastic epithelium (CE)] "has been widely proposed to be important in shaping calcification responses to ocean acidification," and they therefore decided to analyze the impact of seawater acidification on pHSCM and pHCE in the coral Stylophora pistillata, "using in vivo imaging of pH in corals exposed to reduced seawater pH and elevated pCO2 in the laboratory for [both] long and short durations," which work included "exposures to levels of acidification and elevated pCO2 many times greater than those predicted to occur at the end of this century."

In discussing their findings, Venn et al. say they "observed calcification (measured by growth of skeletal crystals and whole colonies) in all our treatments, including treatment pH 7.2, where aragonite was undersaturated." And they say that "this finding agrees with previous work with S. pistillata conducted elsewhere, where net calcification was also observed over a similar range of pH and pCO2 (Krief et al., 2010)." Such findings suggest, in their words, that "S. pistillata may have a high tolerance to decreases in seawater pH and changes in seawater chemistry," which leads them to conclude that "maintenance of elevated pHSCM relative to the surrounding seawater may explain how several coral species continue to calcify even in low pH seawater, which is undersaturated with respect to aragonite (this study and Rodolfo-Metalpa et al. (2011) and Cohen et al., (2009))." Last of all, Venn et al. report that "reductions in calcification rate, both at the level of crystals and whole colonies, were only observed in our lowest pH treatment [pH 7.2] when pH was significantly depressed in the calcifying cells in addition to the SCM." Nevertheless, and "overall," they say their findings suggest that "reef corals may mitigate the effects of seawater acidification by regulating pH in the SCM," which is something they clearly have the capacity to do.

Gabay et al. (2013) write that octocorals possess "an internal calcium carbonate skeleton comprised of microscopic sclerites embedded in their tissue," citing Fabricius and Alderslade (2001), Jeng et al. (2011) and Tentori and Ofwegen (2011). They also note that they are "the second most important faunistic component in many reefs, often occupying 50% or more of the available substrate." And in light of these facts, they say "it is important to predict their response to a scenario of increased pCO2." Against this backdrop, Gabay et al. studied three species of octocorals from two families found in the Gulf of Aqaba at Eilat, including the zooxanthellate Ovabunda macrospiculata and Heteroxenia fuscens (family Xeniidae) and Sarcophyton sp. (family Alcyoniidae), which they maintained for five months under normal (8.2) and reduced (7.6 and 7.3) pH conditions, while they assessed their pulsation rate, protein concentration, polyp weight, density of zooxanthellae and chlorophyll concentration per cell.

According to the three Israeli scientists, their results indicated "no statistically significant difference between the octocorals exposed to reduced pH values compared to the control." Quoting Gabay et al., "these findings indicate that octocorals may possess certain protective mechanisms against rising levels of pCO2," and in this regard they suggest that "their fleshy tissues act as a barrier, maintaining a stable internal environment and avoiding the adverse effects of the ambient elevated pCO2," in line with the similar thinking of Rodolfo-Metalpa et al. (2011), while noting that "this suggestion is further supported by our finding that the ultrastructural features of O. macroscipulata sclerites are not affected by increased ambient seawater acidity." And so it is that they ultimately conclude that "octocorals might be able to acclimate and withstand rising levels of ocean acidification, even under conditions that are far beyond what is expected to occur by the end of the present century (pH 7.9)."

Mass et al. (2013) write that "despite the broad interest in coral calcification and the potential for climate-driven adverse effects, the molecules and biophysical mechanism responsible for the precipitation of carbonates are poorly understood." Indeed, they say that "to date, we lack both a characterization of molecules involved in calcification and a mechanistic understanding of processes that lead to and control calcification," which "lack of knowledge limits our ability to predict the response of corals to increasing atmospheric CO2." Against this backdrop, the seven scientists "for the first time," identified, cloned, determined the amino acid sequence, and characterized four highly acidic proteins that they derived from the expression of genes obtained from the common stony coral, Stylophora pistillata, each of which proteins can spontaneously catalyze the precipitation of calcium carbonate in vitro.

Results of the analysis demonstrated "that coral acid-rich proteins (CARPs) not only bind Ca2+ stoichiometrically but also precipitate aragonite in vitro in seawater at pH 8.2 and 7.6 via an electrostatic interaction with protons on bicarbonate anions." In light of this observation, as they write in the closing sentence of their paper's abstract, the seven U.S. researchers say that "based purely on thermodynamic grounds, the predicted change in surface ocean pH in the next decades would appear to have minimal effect on the capacity of these acid-rich proteins to precipitate carbonates." And as they write in the final sentence of their paper's conclusion section, they say their findings "strongly suggest that these proteins will continue to catalyze calcification reactions at ocean pH values projected in the coming century."

Given all of the above, it is clear that there is much more than meets the eye when it comes to understanding and projecting the potential effects of ocean acidification on corals. As ever more pertinent evidence accumulates, the IPCC's narrative of mass coral harm in consequence of a slight decline in oceanic pH appears further and further off the mark.

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Last updated 23 April 2014