The “Naked coral” hypothesis

Today, it is well known that the anthropogenic rise in atmospheric CO2 is changing not only the climate but also the chemistry of the world’s oceans. First, global warming is causing massive coral bleaching. But a rise in coral disease by undermining their ability to build reefs is also produced by the mixing of anthropogenic CO2 in seawater. Indeed, a large amount of the CO2 produced by the human activities is taken up by the oceans. As CO2 dissolves in the sea water, it takes part in chemical reactions leading to a decrease in pH. This has led to changes in the physiology of a wide variety of organisms and the ecology of all oceans. For increasing our understanding of the natural history of stony corals and the effect of climate change, biologists are testing acidic sea water on their growing, palaeontologists are exploring the fossil records and mass extinctions to uncover clues of ancient episodes of ocean acidification, while phylogeneticists are elucidating their evolution with DNA.

Scleractinian corals, commonly named stony corals (or hard corals), developed during Paleozoic but became extinct massively in the Permian. They suddenly reappear in fossil records in the middle of the Triassic, several millions years later. One of the primary hypotheses regarding such a crisis is that a decrease of the sea water pH altered the ability of stony corals to form their calcite skeleton. To explain the sudden reappearance of scleractinians in the Triassic, when ocean conditions came back to normal, it has been proposed that they survived perhaps in a different form, a form lacking a skeleton, the so-called “naked coral” (Stanley and Fautin 2001). That seems far fetched, but we must keep in our mind that coral reefs have survived millions of years to sea level change, to chemical disturbance of sea water as well as to massive extinctions of other living organisms.

Laboratory experiments showed that two species of stony corals (the scleractinian Mediterranean species Oculina patagonica and Madracis pharencis) can survive long periods of low pH (Fine and Tchernov 2007). After 1 month in acidic sea water, first morphological changes resulted in polyp elongation, followed by dissociation of the colony and complete skeleton loss. All polyps maintained their algal symbionts and the biomass of the solitary polyps under acidic conditions was three times as high as the biomass of polyps cultured under normal conditions. After 12 months, when transferred back to normal pH, the solitary polyps calcified and rebuild colonies! This important experimental result supports the “naked coral” hypothesis.

The second set of observations supporting the “naked coral” is based on morphological similarities between scleractinians and corallimorpharians, for instance the presence of paired mesenteries in both groups. Also cnidoms and sperm ultrastructure were identified as features that may be synapomorphies for uniting scleractinians and corallimorpharians in a same clade.

Finally, the phylogenetic analysis of mitochondrial genome from nine scleractinians, six corallimorpharians and six soft corals as outgroups (three octocorallians, two actiniarians and one zoanthidean) clarified our understanding of the stony corals natural history (Medina et al 2006). Indeed, the results unambiguously indicated that the corallimorpharians are true members of scleractininians, so that the later should include the formers to refer to a natural group. Thus, scleractinians are likely ancestral to the nonmineralized corallimorpharian which are able to adapt to higher CO2 levels. The skeleton was likely lost in the ancestry of corallimorpharians which originated between -110 and -132 Ma, coinciding with high levels of oceanic CO2.

The Oceans are currently experiencing an increase in CO2 concentration similar to what occurred in the Cretaceous when multiple calcifying scleractinians went extinct. In such a context, the “naked coral” hypothesis represents an important and promising field of research for understanding the response of the coral reefs to ocean acidification due to human activities.

Stanley GD Jr, Fautin DG. Paleontology and evolution. The origins of modern corals. Science. 2001 Mar 9;291(5510):1913-4

Fine M, Tchernov D. Scleractinian coral species survive and recover from decalcification. Science. 2007 Mar 30;315(5820):1811

Medina M, Collins AG, Takaoka TL, Kuehl JV, Boore JL. Naked corals: skeleton loss in Scleractinia. Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9096-100