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Review
, 26 (1), 31-53

How Corals Made Rocks Through the Ages

Affiliations
Review

How Corals Made Rocks Through the Ages

Jeana L Drake et al. Glob Chang Biol.

Abstract

Hard, or stony, corals make rocks that can, on geological time scales, lead to the formation of massive reefs in shallow tropical and subtropical seas. In both historical and contemporary oceans, reef-building corals retain information about the marine environment in their skeletons, which is an organic-inorganic composite material. The elemental and isotopic composition of their skeletons is frequently used to reconstruct the environmental history of Earth's oceans over time, including temperature, pH, and salinity. Interpretation of this information requires knowledge of how the organisms formed their skeletons. The basic mechanism of formation of calcium carbonate skeleton in stony corals has been studied for decades. While some researchers consider coral skeletons as mainly passive recorders of ocean conditions, it has become increasingly clear that biological processes play key roles in the biomineralization mechanism. Understanding the role of the animal in living stony coral biomineralization and how it evolved has profound implications for interpreting environmental signatures in fossil corals to understand past ocean conditions. Here we review historical hypotheses and discuss the present understanding of how corals evolved and how their skeletons changed over geological time. We specifically explain how biological processes, particularly those occurring at the subcellular level, critically control the formation of calcium carbonate structures. We examine the different models that address the current debate including the tissue-skeleton interface, skeletal organic matrix, and biomineralization pathways. Finally, we consider how understanding the biological control of coral biomineralization is critical to informing future models of coral vulnerability to inevitable global change, particularly increasing ocean acidification.

Keywords: amorphous calcium carbonate; aragonite; biomineralization; calcite; calicoblastic cells; corals; crystal growth; skeletal organic matrix.

Conflict of interest statement

Conflict of Interest

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
The general organization of the scleractinian coral soft tissue and underlying skeleton. (a) Planktonic larva (planula, greenish color due to symbiotic algae) and newly settled polyp (d) with incipient skeletal deposits (i). (b) Main skeletal and soft tissue structures of colonial coral with (c) enlargement showing simplified section of two main tissue layers with symbiotic algae in oral endoderm. Such organization is exemplified by the symbiotic scleractinian Stylophora pistillata (e, with tissue cover, brown-green tiny dots (j, enlarged, arrows) are symbiotic algae; k, l, bare skeleton). (g) Solitary and asymbiotic coral Desmophyllum dianthus (f, bare skeleton, upper view). (h) 3D view of solitary corallum with main soft tissue and skeleton structures. Images (b) and (h) are courtesy of Ewa Roniewicz
Figure 2
Figure 2
Coral reefs viewed underwater and by satellite. (a) Massive Porites building reef structures as observed by SCUBA divers (Photo credit: Hagai Nativ, University of Haifa, Israel). (b) Palau Atoll surrounding Babeldaob, Koror, and Peleliu islands in the Republic of Palau, as seen by NASA SeaWIFS satellite (courtesy of NASA: https://eoimages.gsfc.nasa.gov/images/imagerecords/87000/87423/palau_oli_2014080_wide.jpg)
Figure 3
Figure 3
Overview of Phanerozoic anthozoan diversity. (a–g) Recent scleractinian corals are represented by ca. 1,500 species, of which about half are shallow-water, often colonial taxa living in symbiosis with dinoflagellate algae (Z, zooxanthellate), and half are shallow- and deep-water, often solitary taxa lacking symbiotic algae (AZ, azooxanthellate). Molecular phylogeny suggests the presence of three major clades among modern scleractinians that diverged more than 400 Mya: (1) Basalia (e.g., (a) Gardineria [AZ], (b) Letepsammia [AZ]), (2) Complexa (e.g., (c) Fungiacyathus [AZ], (d) Galaxea [Z], (e) Acropora [Z], and Robusta (e.g., (f) Acanthastrea [Z], (g) Stylophora [Z]). (h) Simplified anthozoan phylogeny: sudden appearance of highly diversified scleractinian corals about 14 Ma after the Permian–Triassic boundary (Middle Triassic) is preceded by the rare occurrence of scleractinian-like forms in Paleozoic (e.g., (o) Kilbuchophyllia). Despite of major shifts in seawater Mg/Ca ratio which dictates calcium carbonate polymorph selection in abiotic conditions (low Mg/Ca favors calcite, whereas high Mg/Ca favors aragonite [Berner, 2013]) scleractinians almost invariably form aragonite skeletons throughout their fossil record (possible exception is calcite “Coelosmilia” (i)): (j) Astrocoenia, (k) Donacosmilia, (l) Columnastrea, (m) Tropiastraea (left), Margarophyllia (right), (n) Haimeicyclus, (p) Pamiroseris. Paleozoic calcifying corals were represented by mostly calcite rugose (solitary and colonial: e.g., (r) Hexagonaria, (s) Hadrophyllum, (t) Tachylasma), and colonial tabulate corals (e.g., (u) Heliolites). There is a pre-Ordovician record of calcifying corals, but their exact taxonomic attribution is uncertain (“Corallomorpha,” e.g., (q) Cothonion). Approximate age of illustrated fossil corals is given in bottom-left corner of the image. Scale bars = 2 mm
Figure 4
Figure 4
Growth forms of the Triassic and Recent corals in direct comparison. Triassic scleractinian corals that emerged en masse after the Permian–Triassic boundary (extinction of Paleozoic rugosan corals) were highly diversified and showed solitary (a), phaceloid (d), cerioid (f), thamnasterioid (i), and meandroid (k) growth forms fully comparable to modern scleractinians (c, e, g, j, l, respectively). Some well-preserved Triassic corals (b) show regular banding of TD's (arrows) which characterize modern corals symbiotic with dinoflagellates (h); coral–dinoflagellate symbiosis was likely a key driver in the evolution and expansion of shallow-water Mesozoic scleractinians. Scale bars: a, c–g, i–l = 5 mm, b, h = 50 µm. Triassic (Carnian) specimens from (a, b, d, f, i, k) Carnian of Italian Dolomites and (b) Norian of Turkey
Figure 5
Figure 5
View on the Sassolungo (Langkofel) mountain in the Dolomites (northern Italy). These steep cliffs are 1,000 m high, rising up to nearly 3,200 m above sea level and represent remnants of middle Triassic (Ladinian) reef atolls that formed over millions of years after the end-Permian extinction with the help of the first scleractinian corals. Despite extensive alpine deformation, these Triassic atolls are still in their original position with respect to the surrounding deep-water clays. The extensive build-ups were the result of sea level rise, basin subsidence, and rapid growth of reef organisms
Figure 6
Figure 6
Coral aragonite crystal growth as a physicochemically dominated process (a) versus biologically controlled process (b). In the often-held view of a physicochemically dominated process, the calicoblastic ectoderm and skeleton provide a wide space (Gagnon, Adkins, & Erez, 2012; see criticism in Brahmi et al., 2016) in which biological processes determine the extracellular calcifying medium (ECM) composition, but from there on, the process is dominated by crystal growth by a classical pathway of ion-by-ion attachment yielding a smooth, faceted surface. This is in contrast to the biologically controlled process, in which Ca2+ and bicarbonate, as well as ACC and biomolecules, are transported, in some cases by vesicles (yellow spheres), to the narrow ECM (width based on microsensor dimensions in Ammann, Bührer, Schefer, Müller, & Simon, 1987; de Beer, Kühl, Stambler, & Vaki, 2000). Structural molecules such as the proteins coadhesin, peroxidasin, and collagen, which form functional triple helices, adhere calicoblastic cells to the skeleton and may have a role in mineral formation. ACC nanoparticles are deposited on both ECM biomolecules and the growing mineral surface, and crystallization proceeds through a nonclassical pathway to crystallization by ACC particle attachment to yield a biogenic aragonite crystal with characteristic nanocomposite appearance
Figure 7
Figure 7
CaCO3 crystal bundle growing from the extracellular calcifying medium (ECM) surrounding Stylophora pistillata cells aggregated into protopolyps. XRD analysis has previously determined that these crystal bundles are made of aragonite (Mass et al., 2012) and that they do not occur on coral cells killed with azide
Figure 8
Figure 8
Hierarchical structure of the coral skeleton. Skeletal structures of calcifying corals consist of two main regions: (1) skeletal tips which are composed of Rapid Accretion Deposits (RADs, called also Centers of Calcification [COCs]) and (2) lateral sides of skeleton composed of thickening deposits (TDs, called also “fibers”); (a) schematic drawing with RADs and TDs in longitudinal and transverse sections, (b–d) RADs are cyclically deposited and show alteration of organic-enriched/depleted layers (b, c, optical microscope image of longitudinally sectioned septum; e, epifluorescence microscope image highlighting organic-enriched regions). Individual skeletal layers are often continuous between RADs and TDs (d) pointing to different growth dynamics between two regions but not different timings of their formation; in transverse sections (f) that intersect layers of different growth stage this aspect is not observable. (g–k) Regular alteration of layers analogous to organic-enriched/depleted layers in modern corals can be found in skeletons of Paleozoic (e.g, (g) rugose calcite corals) and Triassic (h), Jurassic (i), Cretaceous (j, calcite Coelosmilia), and Cenozoic (k) scleractinian corals. Distinct patterns of TD arrangement are shared between phylogenetically related taxa (e.g., (l) tuberculate pattern in pocilloporiids (Seriatopora), and (m, n) shingled (red arrows) pattern in acroporiids (Acropora); l, m SEM; n section in polarized light. (o) RADs are composed of well-differentiated nanograins (ca. 100 nm in diameter); (p) TDs show larger, fibrous units that exhibit nanocomposite structure under AFM (q, amplitude image with arrows pointing to a different (?organic) phase of grain envelope)

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