Skeletal light-scattering accelerates bleaching response in reef-building corals

Abstract

Background: At the forefront of ecosystems adversely affected by climate change, coral reefs are sensitive to anomalously high temperatures which disassociate (bleaching) photosynthetic symbionts (Symbiodinium) from coral hosts and cause increasingly frequent and severe mass mortality events. Susceptibility to bleaching and mortality is variable among corals, and is determined by unknown proportions of environmental history and the synergy of Symbiodinium- and coral-specific properties. Symbiodinium live within host tissues overlaying the coral skeleton, which increases light availability through multiple light-scattering, forming one of the most efficient biological collectors of solar radiation. Light-transport in the upper ~200 μm layer of corals skeletons (measured as 'microscopic' reduced-scattering coefficient, μ'(S,m)), has been identified as a determinant of excess light increase during bleaching and is therefore a potential determinant of the differential rate and severity of bleaching response among coral species.

Results: Here we experimentally demonstrate (in ten coral species) that, under thermal stress alone or combined thermal and light stress, low-μ'(S,m) corals bleach at higher rate and severity than high-μ'(S,m) corals and the Symbiodinium associated with low-μ'(S,m) corals experience twice the decrease in photochemical efficiency. We further modelled the light absorbed by Symbiodinium due to skeletal-scattering and show that the estimated skeleton-dependent light absorbed by Symbiodinium (per unit of photosynthetic pigment) and the temporal rate of increase in absorbed light during bleaching are several fold higher in low-μ'(S,m) corals.

Conclusions: While symbionts associated with low-[Formula: see text] corals receive less total light from the skeleton, they experience a higher rate of light increase once bleaching is initiated and absorbing bodies are lost; further precipitating the bleaching response. Because microscopic skeletal light-scattering is a robust predictor of light-dependent bleaching among the corals assessed here, this work establishes μ'(S,m) as one of the key determinants of differential bleaching response.

Keywords: Coral bleaching; Global climate change; Optical scattering; Photosynthesis; Symbiosis.

Fig. 1

Dynamics of bleaching response variables. High- and low-${\mathit{\mu }}_{S,m}^{\prime }$ corals (means in gray and black respectively in b–f) responded differentially to experimental light (broken line in a) and temperature (dotted line in a) conditions (CT-CL: control temperature [26 °C] and light [83 μmol quanta m⁻² s⁻¹], CT-HL: control temperature and high light [328 μmol quanta m⁻² s⁻¹], HT-CL: high temperature [32 °C] and control light, and HT-HL: high temperature and high light; shaded areas are control). Under temperature stress (HT-CL and HT-HL), Symbiodinium in hospite of low-${\mathit{\mu }}_{S,m}^{\prime }$ corals experienced suppressed photosynthetic performance (b, c) and reduced cell density (d), and holobiont reflectance (e) of low-${\mathit{\mu }}_{S,m}^{\prime }$ corals approached the level of bare skeleton (dashed lines in e are post-experiment skeletal reflectance). Low-${\mathit{\mu }}_{S,m}^{\prime }$ corals experienced progressively greater average rates of photochemical efficiency loss (CT-CL p = 0.755, CT-HL p = 0.032, HT-CL p = 0.112, and HT-HL p = 0.042) as heat and light stress were combined (f). Isolating the effect of light from temperature on photochemical efficiency (g), ${\mathit{\mu }}_{S,m}^{\prime }$ is correlated with the temporal rate of F _v /F _m change $\left(\mathit{\Delta }PE\sim {\mathit{\Delta }}^2\left(F_V/F_M\right)/\left(\mathit{\Delta }t\mathit{\Delta }I\right)\right)$ expressed as the difference between CL and HL (Eq. 2) for corals exposed to HT (filled circles; p = 0.007) or CT (open circles; p = 0.07). All error bars are standard error of the mean

Fig. 2

Dynamics of modeled Symbiodinium light absorption in hospite due to skeletal backscattering (${\mathit{\mu }}_{S,m}^{\prime }$). Symbiodinium in hospite of high- (gray line) and low-${\mathit{\mu }}_{S,m}^{\prime }$ (black line) corals are (conservatively) predicted by an empirical model to have differential skeleton-dependent light absorption per unit pigment (I _a2/ρ). Under a CT, the absorption of light in high- and low-${\mathit{\mu }}_{S,m}^{\prime }$ corals is similar when exposed to CL (solid line) and HL (broken line). Under b HT, the absorption of light in low-${\mathit{\mu }}_{S,m}^{\prime }$ corals is several times larger under either light condition, but the increase under HL is dramatic. Additionally, the increase in (conservatively) estimated temporal rates of light absorbed per unit pigment $\left(\mathit{\Delta }\left(I_{a2}/\mathit{\rho }\right)/\mathit{\Delta }t\right)$ in low-${\mathit{\mu }}_{S,m}^{\prime }$ corals (black bars) is progressively greater as heat and light stress were combined (c). All abbreviations follow Fig. 1 and error bars are standard error of the mean

Fig. 3

Effects of skeletal reflectance (R _S) and Symbiodinium thermotolerance (Symb _thermo) on photosynthetic performance dynamics. High- and low- (means in gray and black respectively in b–g) R _S and Symb _thermo corals responded similarly to experimental light (broken line in a) and temperature (dotted line in a) conditions (described in Fig. 1). Photosynthetic performance was similarly suppressed under increased stress in corals grouped by R _S (b, c) and was modestly (but non-significantly) more suppressed for corals hosting high-thermotolerance Symbiodinium (d, e). Both low- and high-R _S corals experienced a progressively greater average rate of photochemical efficiency loss (CLL p = 0.64; CHL p = 0.28; TLL p = 0.55 and THL p = 0.91) as heat and light stress were increased (f), and both low and high-Symb _thermo corals experienced a progressively greater average rate of photochemical efficiency loss (CLL p = 0.47; CHL p = 0.70; TLL p = 0.26 and THL p = 0.68) as heat and light stress were increased (g). All error bars are standard error of the mean