Fine-Scale Skeletal Banding Can Distinguish Symbiotic from Asymbiotic Species among Modern and Fossil Scleractinian Corals

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.

Photosymbiosis and the expansion of shallow-water corals

“…1, C to G). Fibers were observed to have doublets of optically light and dark bands representing growth increments ( 12 ), which are also observable in scanning electron microscopy (SEM) as layers with positive and negative etching relief, respectively (figs. S2D and S3, E and F).…”

Physiological integration of coral colonies is correlated with bleaching resistance

“…Coates & Jackson (1987) identified a pattern in corals where multiserial colonial forms with small, highly integrated corallites are almost exclusively symbiotic, whereas species that have solitary or uniserial colonial forms with large, poorly integrated corallites are almost exclusively asymbiotic, suggesting that increased colony integration is one of the indications of an evolutionary origin of Symbiodinium symbiosis. Although the pattern is imperfect (Frankowiak et al 2016) and is not the product of a linear evolutionary progression toward increased colonial integration and symbiosis, but is due to a more complex history of repeated acquisition and loss of coloniality and symbiosis that were not always concurrent (Barbeitos et al 2010), it remains a conspicuous motif among extant species. Symbiodinium photosynthesis is the primary source of fixed carbon for reef-building corals (Muscatine 1990), and dis asso ciation of Symbiodinium and coral hosts through thermal stress (bleaching) can result in decreased growth, regeneration, reproduction, and competitive abilities, and increased incidence of disease, predation, and mortality (Brown 1997, Jokiel 2004, Jones 2008, McClanahan et al 2009).…”

Relating Coral Skeletal Structures at Different Length Scales to Growth, Light Availability to Symbiodinium, and Thermal Bleaching

“…Micro-µ s ′ may result from light scattering by the most recently biomineralized calcium carbonate and organic matrix located above the latest dissepiment (e.g., the >60 nm voids in Goniastrea stelligera skeleton; Frankowiak et al, 2016), while bulk-µ s ′ would result from light scattering by new and old skeleton where older voids could potentially be filled with water or gas due to degradation of organic material. However, how the structural and chemical composition of the top skeletal layer is associated with bleaching susceptibility will require further investigation.…”

“…This process of crystal formation, designated as crystallization by particle attachment (CPA), has been observed to occur in biomineralized materials, such as sea urchin spicules or zebrafish fin bone, and could be due, in part, to diffusion-limited kinetics (De Yoreo et al, 2015). In corals, accretion of aragonite nanograins in the skeleton is a diffusion-limited process, dependent on the secretion of ions (calcium, carbonate, and protons) and organic matrix molecules (involved in crystal nucleation) by specialized cells in the basal ectoderm of the coral tissue (calicoblastic cells), and occurs through a combination of linear extension and thickening (Stolarski, 2003;Cuif and Dauphin, 2005b;Nothdurft and Webb, 2007;Frankowiak et al, 2016). Growth of fractal-like structures can be described by mass-fractal dimension, or D f , which characterizes the overall size distribution of skeletal structural elements at different length scales (Basillais, 1997;Martin-Garin et al, 2007;Przeniosło et al, 2008;Young et al, 2017).…”