CO2SCIENCE & SPPI ORIGINAL PAPER ♦ August 11, 2015

EFFECTS OF OCEAN ACIDIFICATION

AND WARMING ON CORALS

(LABORATORY STUDIES)

2

EFFECTS OF OCEAN ACIDIFICATION AND WARMING ON

CORALS (LABORATORY STUDIES)

Citation: Center for the Study of Carbon Dioxide and Global Change. "Effects of Ocean

Acidification and Warming on Corals (Laboratory Studies).” Last modified August 11, 2015.

http://www.co2science.org/subject/o/summaries/acidwarmcoralslab.php.

Most of the ocean acidification research conducted to date has focused solely on the biological

impacts of declining seawater pH. Fewer studies have investigated the interactive effects of

ocean acidification and temperature. This summary examines what has been learned in several of

such studies for coral reefs, as reported in various laboratory-based studies on the topic. Contrary

to what is widely assumed and reported, the studies reviewed here collectively reveal that many

corals will remain unaffected by rising temperatures and atmospheric CO2 concentrations.

Furthermore, in contrast to projections, some will likely experience growth and performance

benefits.

In a paper published in Nature Climate Change, McCulloch et al. (2012)1 describe how biogenic

calcification occurs within an extracellular calcifying fluid located in the semi-isolated space

between a coral’s skeleton and its calicoblastic ectoderm, where during active calcification the

pH of the calcifying fluid (pHcf) is often increased relative to ambient seawater pH. At a typical

seawater pH of ~8.1, for example, they state that the pH of aragonitic corals shows a species-

dependent range of 8.4 to 8.7, representing a systematic increase in pHcf relative to ambient sea

water (ΔpH) of ~0.3-0.6 units. In fact, they report that in situ measurements of pH within the

calcifying medium of live coral polyps using microelectrodes (Al-Horani et al., 2003; Ries,

2011a) and pH-sensitive dyes (Venn et al., 2011) have registered enhanced pHcf values between

0.6 and 1.2 (and sometimes up to 2) pH units above seawater during the day, when both net

production and calcification are highest.

Using a model of pH regulation combined with abiotic calcification, McCulloch et al. (2012)

additionally show that “the enhanced kinetics of calcification owing to higher temperatures has

the potential to counter the effects of ocean acidification,” adding that “the extra energy required

to up-regulate pH is minor, only <1% of that generated by photosynthesis,” which highlights the

importance of maintaining the zooxanthellae-coral symbiosis for sustaining calcification. And

they further note, in this regard, that their model predicts “a ~15% increase in calcification rates

from the Last Glacial Maximum to the late Holocene,” which increase they describe as being

“consistent with the expansion of tropical habitats that occurred during this time despite PCO2

increasing.”

Projecting into the future with their experimentally-verified model, the four researchers assess

the response of coral reefs to both global warming, with mean tropical sea surface temperatures ~

2°C higher, and with PCO2 increasing from present-day levels to ~1,000 ppm by the year 2100.”

And for this scenario, they report that their model predicts “either unchanged or only minimal

effects on calcification rates.” Thus, from a strictly chemical and kinetic perspective, their model

indicates that “ocean acidification combined with rising ocean temperatures should have only

1 http://www.co2science.org/articles/V15/N50/EDIT.php

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minimal effects on coral calcification,” which they describe as “a direct outcome” of corals’

ability to up-regulate pH at the site of calcification.

Rodolfo-Metalpa et al. (2010)2 collected three live colonies of the Mediterranean zooxanthellate

coral Cladocora caespitosa in the Bay of Villefranche (Ligurian Sea, France) at about 25 meters

depth in July 2006 plus three other colonies in February 2007. The colonies were then divided

into fragments and carefully removed single polyps that they attached to PVC plates and

randomly assigned to aquariums that were continuously supplied with unfiltered seawater and

maintained at ambient or elevated water temperature (T or T + 3°C) in equilibrium with air of

ambient or elevated CO2 concentration (400 or 700 ppm), subjecting them to “(1) mid-term

perturbations (1 month) in summer and winter conditions of irradiance and temperature, and (2)

a long-term perturbation (1 year), mimicking

the seasonal changes in temperature and

irradiance.”

Results indicated that “an increase in CO2, in

the range predicted for 2100, does not reduce

[the coral’s] calcification rate,” and that “an

increase in CO2, alone or in combination with

elevated temperature, had no significant effect

on photosynthesis, photosynthetic efficiency

and calcification.” However, they report that a

3°C rise in temperature in winter resulted in a

72% increase in gross photosynthesis, as well

as a significant increase in daytime calcification

rate.

In light of their several significant findings,

Rodolfo-Metalpa et al. conclude that “the

conventional belief that calcification rates will

be affected by ocean acidification may not be

widespread in temperate corals.” In this regard,

for example, they note that Ries et al. (2009)

have reported that the calcification rate of the

temperate coral Oculina arbuscula is also

unaffected by an increase in atmospheric CO2 concentration of up to 840 ppm, and that a large

decrease in calcification was only found at a CO2 concentration in excess of 2200 ppm. In

addition, they write that “some marine invertebrates may be able to calcify in the face of ocean

acidification or, contrary to what is generally expected, may increase their calcification rates as

reported on the ophiourid brittlestar Amphiura filiformis (Wood et al., 2008), the seastar Pisaster

ochraceus (Gooding et al., 2009) exposed to lower pH (7.8-7.3), the Caribbean coral Madracis

mirabilis at pH 7.6 (Jury et al., 2010), and shown for coralline red algae, calcareous green algae,

temperate urchins, limpets, crabs, lobsters and shrimp (Ries et al., 2009).” Likewise, they write

that there are many cases where “rates of photosynthesis are either not affected (e.g. Langdon et

al., 2003; Reynaud et al., 2003; Schneider and Erez, 2006; Marubini et al., 2008) or slightly

increased (e.g. Langdon and Atkinson, 2005) at the level of CO2 expected in 2100.”

2 http://www.co2science.org/articles/V13/N21/C2.php

“An increase in CO2, alone

or in combination with

elevated temperature, had

no significant effect on

photosynthesis,

photosynthetic efficiency

and calcification.”

4

In a study designed to explore what controls calcification in corals, Sandeman (2012)3

suspended, by means of a torsion microbalance (as per Kesling and Crafts, 1962), small pieces of

coral that he carefully removed from the edges of thin plates of Agaricia agaricites corals and

lowered into gently-stirred temperature-controlled seawater, after which he used the

microbalance to measure coral net calcification rates over a range of seawater temperature and

pH. Results of the experiment indicated that calcification rates of live A. agaricites coral

increased by 15-17.7% per °C as seawater temperature rose from 27 to 29.5°C; and in his

experiments in which the pH of the seawater was reduced from an average of 8.2 to 7.6, he

observed that calcification in living corals increased significantly. On the other hand, similar

experiments conducted with small portions of dead coral skeleton revealed that “when the

average pH was reduced from 8.2 to 7.5, calcification rate decreased.” More specifically, he

determined that the difference between calcification rates in going from seawater of pH 8.2 to

seawater of pH 7.8 ranged from +30% for coral with no dead areas to -21.5% for coral with 30%

dead exposed surface area.

Commenting on the analysis, the Trent University researcher from Peterborough, Ontario

(Canada) says his findings suggest that lower seawater pH due to atmospheric CO2 enrichment

and increased temperature (but short of reaching the bleaching level) “will both enhance active

biotic calcification.” And he therefore states that the wide range of results between his and other

scientists’ studies of calcification rate and carbon dioxide “may be explainable in terms of the

ratio of ‘live’ to ‘dead’ areas of coral,” as is also suggested by the work of Rodolfo-Metalpa et

al. (2011) and Ries (2011b), all of which information leads him to conclude that coral species

that typically have smaller areas of exposed dead surface “may have a better chance of survival

as pH levels drop.”

Introducing their work, Schoepf et al. (2013)4 write that "since scleractinian corals are calcifying

organisms that already live close to their upper thermal tolerance limits, both ocean warming and

acidification severely threaten their survival and role as reef ecosystem engineers." Yet they

further state that "no studies to date have measured energy reserve pools (i.e., lipid, protein, and

carbohydrate) together with calcification under ocean acidification conditions under different

temperature scenarios," which omissions inspired them to conduct an experiment that actually

did what was needed to be done in this regard.

Specifically, Schoepf et al. studied the single and interactive effects of pCO2 (382, 607 and 741

ppm) and temperature (26.5 and 29.0°C) on coral calcification, energy reserves (i.e., lipid,

protein, and carbohydrate), chlorophyll a and endosymbiont concentrations in four species of

Pacific coral having different growth morphologies (Acropora millepora, Pocillopora

damicornis, Montipora monasteriata and Turbinaria reniformis). In doing so, the thirteen

researchers discovered that coral energy reserves were largely not metabolized "in order to

sustain calcification under elevated pCO2 and temperature," in harmony with the fact that

"maintenance of energy reserves has been shown to be associated with higher resistance to coral

bleaching and to promote recovery from bleaching (Rodrigues and Grottoli, 2007; Anthony et

al., 2009)." In fact, they report that lipid concentrations actually increased under ocean

acidification conditions in both A. millepora and P. damicornis, and that they "were fully

maintained in M. monasteriata and T. reniformis," while protein, carbohydrate and tissue

biomass were also "overall maintained under ocean acidification conditions in all species." And,

3 http://www.co2science.org/articles/V15/N31/B2.php 4 http://www.co2science.org/articles/V17/N1/B2.php

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therefore, they found that "only one of the four corals species studied [Acropora millepora]

decreased calcification in response to average ocean acidification levels expected by the second

half of this century (741 ppm), even when combined with elevated temperature (+2.5°C)."

As a result of their several findings, Schoepf et

al. concluded that "some corals could be more

resistant to combined ocean acidification and

warming expected by the end of this century

than previously thought," such that "the

immediate effects of rising seawater

temperature and ocean acidification may be

tolerable for some species," possibly because

the increased availability of CO2(aq) under

ocean acidification conditions may enhance

algal productivity, especially in Symbiodinium

phylotypes with less efficient carbon-

concentrating mechanisms that rely to a greater

extent on the passive, diffusive uptake of

CO2(aq) and its fertilization effect, citing in this

regard the work of Herfort et al. (2008) and

Brading et al. (2011).

In a study published in the journal Marine

Ecology Progress Series, Chua et al. (2013)5

purposed to test "whether temperature might

act in combination with OA to produce a

measurable ecological effect on fertilization,

development, larval survivorship or

metamorphosis of two broadcast spawning

species, Acropora millepora and A. tenuis,

from the Great Barrier Reef. More specifically,

the four researchers studied the effects of four

different treatments: control, high temperature

(+2°C), high partial pressure of CO2 (pCO2,

700 µatm), and a combination of both high

temperature and high pCO2, corresponding to

the current levels of these parameters and the

values projected for them by the end of this century in the IPCC's A2 scenario. And what did

they thereby learn?

Chua et al. say they "found no consistent effect of elevated pCO2 on fertilization, development,

survivorship or metamorphosis, neither alone nor in combination with temperature," contrasting

with the results found by Schoepf et al. (2013) for A. millepora discussed earlier. As for

warming, they also say that it "had no consistent effect on fertilization, survivorship or

metamorphosis." However, they observed that the two degrees of warming actually increased

rates of development, providing encouraging news concerning the future of these organisms.

5 http://www.co2science.org/articles/V17/nov/a21.php

"Some corals could be more

resistant to combined

ocean acidification and

warming expected by the

end of this century than

previously thought," such

that "the immediate effects

of rising seawater

temperature and ocean

acidification may be

tolerable for some species."

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Determined to discover "whether elevated pCO2 predicted for the year 2100 (85.1 Pa) affects

bleaching in the coral Seriatopora caliendrum either independently or interactively with high

temperature," Wall et al. (2014)6 collected specimens of the species from Nanwan Bay, Taiwan,

and subjected them to combinations of temperature (27.7 vs. 30.5°C) and pCO2 (45.1 vs. 85.1

Pa) for 14 days," while assessing all pertinent biological responses of the coral. In discussing

their findings, the three researchers report that "high temperature reduced values of all dependent

variables (i.e., bleaching occurred), but high pCO2 did not affect Symbiodinium photophysiology

or productivity, and did not cause bleaching," either "individually, or interactively with high

temperature." Given such findings, Wall et al. concluded that "the present results clearly support

a null effect for high pCO2." Or as they state in the final sentence of their paper's abstract, "short-

term exposure to 81.5 Pa pCO2, alone and in combination with elevated temperature, does not

cause or affect coral bleaching."

Introducing their recent work, Levas et al.

(2015)7 write that "research to date has largely

neglected the individual and combined effects

of OA and seawater temperature on coral-

mediated organic carbon (OC) fluxes," noting

that this void of knowledge "is of particular

concern as dissolved and particulate OC (DOC

and POC, respectively) represent large pools of

fixed OC on coral reefs."

In an attempt to reduce this knowledge void, the

sixteen scientists assessed coral-mediated POC

and DOC, as well as total OC (TOC = DOC +

POC), plus the relative contributions of each of

them to coral metabolic demand for two species

of coral, Acropora millepora and Turbinaria

reniformis, at two different levels of pCO2 (382

and 741 µatm) and seawater temperatures (26.5

and 31.0°C). And what did they thereby learn?

Levas et al. report that "independent of

temperature, DOC fluxes decreased

significantly with increases in pCO2 in both species, resulting in more DOC being retained by the

corals and only representing between 19 and 6% of TOC fluxes for A. millepora and T.

reniformis," while at the same time POC fluxes were unaffected by elevated temperature and/or

pCO2. And, thus, they were able to conclude that "these findings add to a growing body of

evidence that certain species of coral may be less at risk to the impacts of OA and temperature

than previously thought."

In one final study, Towle et al. (2015)8 examined "the ability of coral heterotrophy to mitigate

reductions in growth due to climate change stress in the critically endangered Caribbean coral

Acropora cervicornis via changes in feeding rate." This they did in a laboratory study where the

6 http://www.co2science.org/articles/V17/N19/C3.php 7 http://www.co2science.org/articles/V18/jun/a10.php 8 http://www.co2science.org/articles/V18/aug/a2.php

Such results "show for the

first time that a

threatened coral species

can buffer ocean-

acidification-reduced

calcification by increasing

feeding rates.

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corals in question "were either fed or unfed and exposed to elevated temperature (30°C),

enriched pCO2 (800 ppm) or both (30°C/800 ppm) as compared to a control (26°C/390 ppm) for

8 weeks."

This experiment revealed, as the three researchers describe it, that the "fed corals were able to

maintain ambient growth rates at both elevated temperature and elevated CO2, while unfed corals

experienced significant decreases in growth with respect to fed conspecifics." In light of these

findings, therefore, the three researchers write that their results "show for the first time that a

threatened coral species can buffer ocean-acidification-reduced calcification by increasing

feeding rates." And they thus conclude with the good-to-hear news that "a critically endangered

species with access to food sources other than photosynthate may be able to maintain growth

physiology under climate change stress."

Although, much remains to be learned on this subject, it is clear that many corals will not

succumb to the presumed negative impacts of rising temperatures and ocean acidification. And

when adaptive and evolutionary responses are considered, it may be that few, if any, corals will

actually suffer harm from increases in these two phenomena. In fact, many coral species could

well benefit from the warmer ocean temperatures and higher atmospheric CO2 concentrations

predicted for the years and decades ahead.

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