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

Abstract

Light scattering of coral skeletons and tissues increases light availability to photosynthetic endosymbionts to form one of the most efficient biological collectors of solar radiation. Rapid increases in light availability during thermally-induced symbiont loss (bleaching) impair photosynthetic performance of the remaining Symbiodinium and precipitate a more severe bleaching response (optical feedback-loop hypothesis). Here we focus on light scattering of the skeleton, which is determined by light interaction with skeletal components assembled in a hierarchical fractal-like structure from tens of nanometers (e.g., calcium carbonate nanograins) to micro-and millimeters (septa, corallites, and coenosteum) to centimeters and higher (colony form). We examined the association between skeletal structures, their role in light scattering, and species-specific bleaching responses for 88 coral species using phylogenetically-corrected analysis. We also explored the effect of growth on light scattering by modeling the fractal-like accretive growth of the skeleton (assuming a diffusion limited process of biomineralization) as a function of skeletal density, size of nanograins, fractal range of biomineralized clusters, and overall mass-fractal dimension, and validated the model with experimental data. Our results show that differences in light scattering from the top ∼200 µm (micro-µ s ′) of the skeleton, and not from the whole skeleton (bulk-µ s ′), are related to bleaching susceptibility. We also demonstrate how differences in micro-µ s ′ of corallites and coenosteum could explain, in part, the heterogeneous light environment between polyp and coenosarc. The average effective light transport distance of coenosteum measured in 14 coral species indicates that coenosteum could transport light to the corallites, which could then function as "light-trapping devices" where photons are scattered multiple times by septa and corallite walls until absorbed by Symbiodinium. Furthermore, our fractal skeletal growth model suggests that corals that grow faster typically have lower mass-fractal dimension, denser skeletons, lower skeletal micro-µ s ′ , and higher bleaching susceptibility. Finally, our results demonstrate that several skeletal structures of varying Swain et al. Coral Skeletal Properties and Bleaching length scales known to modulate the light microenvironment of Symbiodinium in coral tissue are not associated with bleaching susceptibility. This work provides evidence of the relationship between skeletal growth, light scattering, and bleaching, and further supports the optical feedback-loop hypothesis of coral bleaching.

What drives phenotypic divergence among coral clonemates of Acropora palmata?

“…The coral skeleton serves as an efficient light‐capturing device and colony and polyp morphology determine the light levels experienced by the intracellular symbionts (Enríquez, Méndez, & Iglesias‐Prieto, ; Swain et al, ). Symbiodiniaceae can also maximize light absorption and utilization by increasing photosynthetic pigments and photosynthetic efficiency in corals acclimatized to low light (Falkowski & Dubinsky, ).…”

“…The coral skeleton serves as an efficient light-capturing device and colony and polyp morphology determine the light levels experienced by the intracellular symbionts (Enríquez, Méndez, & Iglesias-Prieto, 2005;Swain et al, 2018). Symbiodiniaceae can also maximize light absorption and utilization by increasing photosynthetic pigments and photosynthetic efficiency in corals acclimatized to low light (Falkowski & Dubinsky, 1981 and 2 have been previously reported to display diurnal patterns of transcription in corals, with higher expression found in the light phase than in the dark (Hoadley, Szmant, & Pyott, 2011;Levy et al, 2007Levy et al, , 2011.…”

Beneath the surface: community assembly and functions of the coral skeleton microbiome

“…It has been hypothesised that the endolithic community may protect the corals and help them overcome bleaching periods [9]. During bleaching, the increased light scattering from the skeleton affects any remaining Symbiodiniaceae and can accelerate bleaching—a mechanism known as the optical feedback loop [103, 104]. By absorbing more light, blooming endolithic algae colonising the outer portions of the skeleton may reduce the light scattering from the skeleton, alleviating photic stress for the coral and the remaining Symbiodiniaceae [55, 105].…”

What drives phenotypic divergence among coral clonemates?

“…The coral skeleton serves as an efficient light capturing devise and colony and polyp morphology determines the light levels experienced by the intra-cellular symbionts (Swain et al 2018). Symbiodiniaceae can also maximize light absorption and utilization by increasing photosynthetic pigments and photosynthetic efficiency in low-light acclimated corals (Falkowski & Dubinsky 1981).…”