FFECTS OF OCEAN ACIDIFICATION AND WARMING ON CORALS (LABORATORY...
Transcript of FFECTS OF OCEAN ACIDIFICATION AND WARMING ON CORALS (LABORATORY...
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.”
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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.
References
Al-Horani, F.A., Al-Moghrabi, S.M. and de Beer, D. 2003. The mechanism of calcification and
its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis.
Marine Biology 142: 419-426.
Anthony, K.R.N., Hoogenboom, M.O., Maynard, J.F., Grottoli, A.G. and Middlebrook, R. 2009.
Energetics approach to predicting mortality risk from environmental stress: a case study of coral
bleaching. Functional Ecology 23: 539-550.
Brading, P., Warner, M.E., Davey, P., Smith, D.J., Achterberg, E.P. and Suggett D.J. 2011.
Differential effects of ocean acidification on growth and photosynthesis among phylotypes of
Symbiodinium (Dinophyceae). Limnology and Oceanography 56: 927-938.
Chua, C.M., Leggat, W., Moya, A. and Baird, A.H. 2013. Temperature affects the early life
history stages of corals more than near future ocean acidification. Marine Ecology Progress
Series 475: 85-92.
Gooding, R.A., Harley, C.D.G. and Tang, E. 2009. Elevated water temperature and carbon
dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the
National Academy of Sciences USA 106: 9316-9321.
Herfort, L., Thake, B. and Taubner, I. 2008. Bicarbonate stimulation of calcification and
photosynthesis in two hermatypic corals. Journal of Phycology 44: 91-98.
Jury, C.P., Whitehead, R.F. and Szmant, A.M. 2010. Effects of variations in carbonate chemistry
on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973):
bicarbonate concentrations best predict calcification rates. Global Change Biology:
10.1111/j.1365-2486.2009.02057.x.
8
Kesling, R.V. and Crafts, F.C. 1962. Ontogenetic increase in archimedian weight of the ostracod
Clamidotheca unispinosa (Baird). American Midland Naturalist 68: 149-153.
Langdon, C. and Atkinson, M.J. 2005. Effect of elevated pCO2 on photosynthesis and
calcification of corals and interactions with seasonal change in temperature, irradiance and
nutrient enrichment. Journal of Geophysical Research 110: 1-54.
Langdon, C., Broecker, W.S., Hammond, D.E., Glenn, E., Fitzsimmons, K., Nelson, S.G., Peng,
T.-S., Hajdas, I. and Bonani, G. 2003. Effect of elevated CO2 on the community metabolism of
an experimental coral reef. Global Biogeochemical Cycles 17: 10.1029/2002GB001941.
Levas, S., Grottoli, A.G., Warner, M.E., Cai, W.-J., Bauer, J., Schoepf, V., Baumann, J.H.,
Matsui, Y., Gearing, C., Melman, T.F., Hoadley, K.D., Pettay, D.T., Hu, X., Li, Q, Xu, H. and
Wang, Y. 2015. Organic carbon fluxes mediated by corals at elevated pCO2 and temperature.
Marine Ecology Progress Series 519: 153-164.
Marubini, F., Ferrier-Pages, C., Furla, P. and Allemand, D. 2008. Coral calcification responds to
seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs
27: 491-499.
McCulloch, M., Falter, J., Trotter, J. and Montagna, P. 2012. Coral resilience to ocean
acidification and global warming through pH up-regulation. Nature Climate Change 2: 623-627.
Reynaud, S., Leclercq, N., Romaine-Lioud, S., Ferrier-Pages, C., Jaubert, J. and Gattuso, J.-P.
2003. Interacting effects of CO2 partial pressure and temperature on photosynthesis and
calcification in a scleractinian coral. Global Change Biology 9: 1660-1668.
Ries, J.B. 2011a. A physicochemical framework for interpreting the biological calcification
response to CO2-induced ocean acidification. Geochimica et Cosmochimica Acta 75: 4053-4064.
Ries, J. 2011b. Acid ocean cover up. Nature Climate Change 1: 294-295.
Ries, J., Cohen, A. and McCorkle, D. 2008. Marine biocalcifiers exhibit mixed responses to
CO2-induced ocean acidification. In: 11th International Coral Reef Symposium, Fort Lauderdale,
Florida USA, 7-11 July 2008, p. 229.
Rodolfo-Metalpa, R., Houlbreque, F., Tambutte, E., Boisson, F., Baggini, C., Patti, F.P., Jeffree,
R., Fine, M., Foggo, A., Gattuso, J.P. and Hall-Spencer, J.M. 2011. Coral and mollusk resistance
to ocean acidification adversely affected by warming. Nature Climate Change 1: 308-312.
Rodolfo-Metalpa, R., Martin, S., Ferrier-Pages, C. and Gattuso, J.-P. 2010. Response of the
temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature
levels projected for the year 2100 AD. Biogeosciences 7: 289-300.
Rodrigues, I.J. and Grottoli, A.G. 2007. Energy reserves and metabolism as indicators of coral
recovery from bleaching. Limnology and Oceanography 52: 1874-1882.
9
Sandeman, I.M. 2012. Preliminary results with a torsion microbalance indicate that carbon
dioxide and exposed carbonic anhydrase in the organic matrix are the basis of calcification on
the skeleton surface of living corals. Revista de Biologia Tropical 60 (Supplement 1): 109-126.
Schneider, K. and Erez, J. 2006. The effect of carbonate chemistry on calcification and
photosynthesis in the hermatypic coral Acropora eurystoma. Limnology and Oceanography 51:
1284-1293.
Schoepf, V., Grottoli, A.G., Warner, M.E., Cai, W-J., Melman, T.F., Hoadley, K.D., Pettay,
D.T., Hu, X., Li, Q., Xu, H., Wang, Y., Matsui, Y. and Baumann, J.H. 2013. Coral energy
reserves and calcification in a high-CO2 world at two temperatures. PLOS ONE 8: e75049.
Towle, E.K., Enochs, I.C. and Langdon, C. 2015. Threatened Caribbean coral is able to mitigate
the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE
10: 10.1371/journal.pone.0123394.
Venn, A., Tambutte, E., Holcomb, M., Allemand, D. and Tambutte, S. 2011. Live tissue imaging
shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6:
e20013.
Wall, C.B., Fan, T.-Y. and Edmunds, P.J. 2014. Ocean acidification has no effect on thermal
bleaching in the coral Seriatopora caliendrum. Coral Reefs 33: 119-130.
Wood, H.L., Spicer, J.I. and Widdicombe, S. 2008. Ocean acidification may increase
calcification rates, but at a cost. Proceedings of the Royal Society B 275: 1767-1773.
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