Abstract
Understanding the evolution of scleractinian corals on geological timescales is key to predict how modern reef ecosystems will react to changing environmental conditions in the future. Important to such efforts has been the development of several skeleton-based criteria to distinguish between the two major ecological groups of scleractinians: zooxanthellates, which live in symbiosis with dinoflagellate algae, and azooxanthellates, which lack endosymbiotic dinoflagellates. Existing criteria are based on overall skeletal morphology and bio/geo-chemical indicators—none of them being particularly robust. Here we explore another skeletal feature, namely fine-scale growth banding, which differs between these two groups of corals. Using various ultra-structural imaging techniques (e.g., TEM, SEM, and NanoSIMS) we have characterized skeletal growth increments, composed of doublets of optically light and dark bands, in a broad selection of extant symbiotic and asymbiotic corals. Skeletons of zooxanthellate corals are characterized by regular growth banding, whereas in skeletons of azooxanthellate corals the growth banding is irregular. Importantly, the regularity of growth bands can be easily quantified with a coefficient of variation obtained by measuring bandwidths on SEM images of polished and etched skeletal surfaces of septa and/or walls. We find that this coefficient of variation (lower values indicate higher regularity) ranges from ~40 to ~90% in azooxanthellate corals and from ~5 to ~15% in symbiotic species. With more than 90% (28 out of 31) of the studied corals conforming to this microstructural criterion, it represents an easy and robust method to discriminate between zooxanthellate and azooxanthellate corals. This microstructural criterion has been applied to the exceptionally preserved skeleton of the Triassic (Norian, ca. 215 Ma) scleractinian Volzeia sp., which contains the first example of regular, fine-scale banding of thickening deposits in a fossil coral of this age. The regularity of its growth banding strongly suggests that the coral was symbiotic with zooxanthellates.
Highlights
The ecological success of modern, shallow water reef-building corals is, for a large part, attributed to their symbiosis with Symbiodinium spp. dinoflagellates
Coral skeletons are structurally characterized by two main components: 1) Rapid Accretion Deposits (RAD, traditionally referred to as Centers of Calcification), which represent about 2–5 volume % of the skeleton and in transverse thin sections are recognizable as optically dark spots or narrow, continuous regions [39,47,48,49]
Our observations confirm that fibers in extant scleractinian corals are aragonitic monocrystals that pass without crystallographic disruption across regions corresponding to fine-scale optical banding [50,51,52,53]
Summary
The ecological success of modern, shallow water reef-building corals is, for a large part, attributed to their symbiosis with Symbiodinium spp. dinoflagellates (zooxanthellae). Relative concentration of some amino acids and sugars differs depending on presence or absence of photosymbionts [31] Both bio- and geochemical features hold great potential to identify symbiosis, their application to fossil skeletons is reasonable only with exceptionally well preserved samples. Cathodoluminescence Microscopy (CL) [a simple method used to determine spatial distribution of primary and secondary calcium carbonate polymorphs (aragonite and calcite respectively) within fossil coralla]: Cathodoluminescence of the skeleton of the Triassic Volzeia sp. Raman Microscopy [allows achieving high-resolution spatial distribution of calcium carbonate polymorphs within coral skeleton; verifies CL observations]: Raman maps of the Triassic Volzeia sp. Analysis of growth band regularity: Thickness of growth increments was measured along individual fibers on SEM photomicrographs of polished and etched surfaces of septa and walls (illustrated in Fig 1) for species of both modern zooxanthellate and azooxanthellate corals, listed in S1 Table. All statistical analyses were conducted using Past 3.07 software [46]
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