Monte Carlo Modeling of Photon Propagation Reveals Highly Scattering Coral Tissue

Abstract

Corals are very efficient at using solar radiation, with photosynthetic quantum efficiencies approaching theoretical limits. Here, we investigated potential mechanisms underlying such outstanding photosynthetic performance through extracting inherent optical properties of the living coral tissue and skeleton in a massive faviid coral. Using Monte Carlo simulations developed for medical tissue optics it is shown that for the investigated faviid coral, the coral tissue was a strongly light scattering matrix with a reduced scattering coefficient of μ_s' = 10 cm^-1 (at 636 nm). In contrast, the scattering coefficient of the coral skeleton was μ_s' = 3.4 cm^-1, which facilitated the efficient propagation of light to otherwise shaded coral tissue layers, thus supporting photosynthesis in lower tissues. Our study provides a quantification of coral tissue optical properties in a massive faviid coral and suggests a novel light harvesting strategy, where tissue and skeletal optics act in concert to optimize the illumination of the photosynthesizing algal symbionts embedded within the living coral tissue.

Keywords: Monte Carlo simulation; algae; biophysics; coral optics; coral tissue; microorganisms; photosynthesis; symbiosis.

FIGURE 1

Simplified structural 2-layer model of a faviid coral in x, z dimensions. The model assumes the dimensions of a massive faviid coral with ∼3 mm thick skeletal walls (i.e., the coenosteum), ∼10 mm wide corallites and a ∼2 mm thick living tissue layer. The model extends uniformly along y and shows three layers: water, living tissue, and skeleton. The dashed red line indicates the region modeled by the Monte Carlo simulation. The vertical solid red line indicates the position of light delivery to the top of the skeleton/tissue wall.

FIGURE 2

Monte Carlo simulations to estimate coral skeletal optical properties. Escaping light [ϕ; W/cm^-2 per W delivered] as a function of radial distance (r) from the incident laser beam, as measured along the bare skeleton surface. Monte Carlo simulations were run for the 5 μ_s’ values (colored numbers) and for a constant μ_a = 0.01 cm^-1. The best fit of the experimental data (black) was μ_s’ = 3.4 cm^-1 (n = 15 repetitions).

FIGURE 3

Monte Carlo simulations to estimate coral tissue optical properties. Escaping light (ϕ) as a function of radial distance (r) from the incident laser light beam as measured over the intact coral tissue surface. Monte Carlo simulations were run for 5 μ_a values, assuming μ_s’ = 0.6 (A), 3.2 (B), and 17.8 cm^-1 (C). The experimental data are black squares (mean ± SD, n = 13 repetitions). The match between experiment and simulation was based on both the slope and absolute values of the ϕ(r) curves. The best choice was μ_a = 1.8 cm^-1 and μ_s’ = 10 cm^-1.

FIGURE 4

Monte Carlo simulation of light distribution in a faviid coral for vertically incident collimated illumination. (A) The 2D distribution of relative 636 nm fluence rate ϕ (z,x) in the model coral (as in Figure 1A). (B) The axial profile down the center of the coral coenosteum ϕ (z) at x = 0 mm. Note that the fluence rate within the living tissue is twice the delivered irradiance (1 cm^-2). Between z = 0 to 2 mm, the back-reflected light escaping from the tissue adds to the delivered irradiance to yield a fluence rate in water that exceeds 1 cm^-2.

FIGURE 5

Monte Carlo simulation of light distribution in a faviid coral under oblique incident illumination. The white arrow indicates the direction of incident collimated light (at 45°). (A) The 2D distribution of relative 636 nm fluence rate ϕ (z,x) across the model coral (tissue and skeleton). (B) The ϕ (z,x) image if the skeleton was replaced by living tissue.

FIGURE 6

Schematic diagram illustrating different optical strategies of corals. (A) The diffuse backscattering properties of skeletons from the coral Porites branneri have been measured and it was shown that the skeleton was highly reflective with an almost isotropic distribution of the backscattered light. Such scattering can lead to a diffusely enhanced light field for Symbiodinium (based on Enriquez et al., 2005). (B) Low-coherence enhanced backscattering spectroscopy has been used to identify that the optical properties of coral skeletons show a great variability in the microscopic reduced scattering coefficient μ_s’ (for short photon pathlengths). It is shown that a continuum of skeletal scattering properties exist, which are affected by the fractal dimensions of the skeleton (based on Marcelino et al., 2013). (C) Monte Carlo simulations are used to identify the optical properties of live faviid corals including intact coral tissue. A combination of light transport is identified where the tissue strongly scatters and enhances irradiance locally, while the skeleton homogenizes and distributes light to otherwise shaded areas. These two optical strategies are used to counteract the light gradient present in coral tissues. Symbiodinium cells (yellow dots) in oral tissue layers receive high amounts of light while in aboral tissue layers irradiance is reduced and Symbiodinium (dark orange) uses the remaining low light efficiently (based on this study and Wangpraseurt et al., 2012, 2014a, 2016).