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Scleractinian Coral Species Survive and Recover from Decalcification

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Science  30 Mar 2007:
Vol. 315, Issue 5820, pp. 1811
DOI: 10.1126/science.1137094

Abstract

Anthropogenic-driven accumulation of carbon dioxide in the atmosphere and projected ocean acidification have raised concerns regarding the eventual impact on coral reefs. This study demonstrates that skeleton-producing corals grown in acidified experimental conditions are able to sustain basic life functions, including reproductive ability, in a sea anemone‐like form and will resume skeleton building when reintroduced to normal modern marine conditions. These results support the existence of physiological refugia, allowing corals to alternate between nonfossilizing soft-body ecophenotypes and fossilizing skeletal forms in response to changes in ocean chemistry. This refugia, however, does not undermine the threats to reef ecosystems in a high carbon dioxide world.

Increasing global concentrations of atmospheric carbon dioxide (CO2) enhance hydrolysis of CO2 in seawater, ultimately decreasing seawater pH (1). This has already caused the pH of modern surface waters (8.0 to 8.3) to be about 0.1 pH unit less than in pre-industrial times, and geochemical models have estimated further acidification of up to 1.4 pH units over the next 300 years (1).

Increased atmospheric CO2 also reduces carbonate ion concentrations in seawater, which decreases the saturation of aragonite (Ω-arag), the principal mineral deposit of corals. Ω-arag, together with temperature and light, sets boundaries for coral reef biogeography (2). Reef communities thrive where Ω-arag is 3.1 to 4.1, but under CO2 doubling Ω-arag is projected to drop below 3.0. Experiments have shown that CO2 doubling results in reduced coral calcification (by 44 to 80%) (3). A concern has been raised (4) that low Ω-arag values and increased chemical dissolution might shift the balance from net accumulation at present to net loss under high-CO2 conditions.

The geological record suggests that there have been periods with unfavorable conditions for calcification, characterized by absence of fossilized coral (reef gaps) (5). The phylogeny of recent corals suggests, however, their origin in the pre-Permian extinction (6). These contradicting facts led to the hypothesis that corals have a means of alternating between soft bodies and fossilizing forms (5, 7, 8), but this has never been tested. We therefore examined the ability of scleractinian corals to survive acidic conditions.

Thirty coral fragments from five coral colonies of the scleractinian Mediterranean species Oculina patagonica (encrusting) (Fig. 1A) and Madracis pharencis (bulbous) were subjected to pH values of 7.3 to 7.6 and 8.0 to 8.3 (ambient) for 12 months. The corals were maintained in an indoor flow-through system under ambient Mediterranean seawater temperatures (17° to 30°C) and photoperiod (intensity of 250 υmol photons m–2 s–1). After 1 month in acidic conditions, morphological changes were seen, initially polyp elongation (Fig. 1B), followed by dissociation of the colony form and complete skeleton dissolution. Surprisingly, the polyps remained attached to the undissolved hard rocky substrate (Fig. 1C).

Fig. 1.

Photographs of O. patagonica. Scale bars indicate 2 mm. (A) Control colony. (B) Sea anemone–like coral polyps following skeleton dissolution in low-pH conditions. (C) Solitary polyps reforming a colony and calcifying after being transferred back to normal seawater following 12 months as soft-bodied polyps in low-pH conditions. (D) Time series illustrating percent change (average ± SE) in protein per polyp (biomass) and total buoyant weight over 12 months in experimental (pH = 7.4) and control (pH = 8.2) seawater (N = 20). A two-way analysis of variance (time × pH) revealed significant changes (P < 0.001) between treatments over time.

The biomass of the solitary polyps under acidic conditions was three times as high as the biomass of polyps in the control colonies that continued to calcify and grow. Control and treatment fragments maintained their algal symbionts during the entire experiment, except for six fragments (10%) of O. patagonica that partially lost their symbionts (bleached) during July but recovered within 2 months. Gametogenesis in control and experimental corals developed similarly during spring and summer months.

All skeleton-free coral fragments survived to the end of the experiment. After 12 months, when transferred back to ambient pH conditions, the experimental soft-bodied polyps calcified and reformed colonies (Fig. 1D). Hence, in the absence of conditions supporting skeleton building, both species maintained basic life functions as skeleton-less ecophenotypes. This has far-reaching implications for better understanding the natural history of corals (6, 8) but mainly implies that corals might survive large-scale environmental change, such as that expected for the following century.

Physiological, versus geographical, refugia may provide a broader explanation for the existence of corals during times of stress. It is important to note that although survival as soft bodies allows corals to persist, substantial decalcification of reefs will cause major changes to the structure and function of coral reef ecosystems and the services they provide to human society.

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