Effects of surface geometry on light exposure, photoacclimation and photosynthetic energy acquisition in zooxanthellate corals

Abstract

Symbiotic corals display a great array of morphologies, each of which has unique effects on light interception and the photosynthetic performance of in hospite zooxanthellae. Changes in light availability elicit photoacclimation responses to optimize the energy balances in primary producers, extensively documented for corals exposed to contrasting light regimes along depth gradients. Yet, response variation driven by coral colony geometry and its energetic implications on colonies with contrasting morphologies remain largely unknown. In this study, we assessed the effect of the inclination angle of coral surface on light availability, short- and long-term photoacclimation responses, and potential photosynthetic usable energy. Increasing surface inclination angle resulted in an order of magnitude reduction of light availability, following a linear relationship explained by the cosine law and relative changes in the direct and diffuse components of irradiance. The light gradient induced by surface geometry triggered photoacclimation responses comparable to those observed along depth gradients: changes in the quantum yield of photosystem II, photosynthetic parameters, and optical properties and pigmentation of the coral tissue. Differences in light availability and photoacclimation driven by surface inclination led to contrasting energetic performance. Horizontally and vertically oriented coral surfaces experienced the largest reductions in photosynthetic usable energy as a result of excessive irradiance and light-limiting conditions, respectively. This pattern is predicted to change with depth or local water optical properties. Our study concludes that colony geometry plays an essential role in shaping the energy balance and determining the light niche of zooxanthellate corals.

Fig 1. Variation in the local light climate with the inclination angle of coral surface.

(A) Box plots of the peak irradiance at local noon with a linear regression describing the relationship between irradiance and surface inclination. The top right insert depicts the predicted pattern of diurnal variation of irradiance for each inclination setting, indicating the relative positions of the compensating irradiance (E_c) and saturating irradiance (E_k). The bottom-left insert shows the PVC structure used in the experiment to adjust the inclination angle of coral samples. (B) Relative variation of the diffuse and direct components of total irradiance. Cosine functions were used to illustrate the relationship between the direct and diffuse components of irradiance with surface inclination.

Fig 2. Variation in chlorophyll a fluorescence parameters with coral surface inclination.

(A) Maximum excitation pressure over PSII (Q_m) recorded before and after exposure to the experimental conditions until a steady state of PSII photochemical activity was detected. The diurnal variation in temperature (daily mean) is depicted using a gray dashed line, while a linear regression of the temperature variation is presented as a solid line.(B) Diurnal oscillation of the maximum (F_v/F_m) and effective (ΔF/F_m’) quantum yield of the PSII. The linear associations of Q_m and F_v/F_m with coral surface inclination are shown in plots (C) and (D) respectively, for the experimental samples at 3 m depth (solid squares and continuous lines) and field measurements on coral colonies in their natural habitat at 5 m depth (empty squares and discontinuous lines). Error bars in all graphs are SE.

Fig 3. Variation in optical properties of the coral tissues and associated photosynthetic descriptors with coral surface inclination.

(A) Boxplots describing the variation in coral absorptance at 675 nm (A₆₇₅), and (B) minimum quantum requirements for oxygen evolution (1/Φ_max) with coral surface inclination. The insert in (B) depict the linear relationship between 1/Φ_max and maximum quantum yield of PSII (F_v/F_m), with error bars as SE.

Fig 4. Variation in photosynthetic parameters with the inclination angle of coral surface.

(A-C) Boxplots describing the variation of three photosynthetic parameters (α, E_c and E_k), along with linear regressions showing the association between each parameter and coral surface inclination. (D) Linear association between P_max and R of all coral samples analyzed in this study.

Fig 5. Local irradiance regimes and light-driven processes according to coral surface inclination.

(A) Description of a diurnal cycle of solar irradiance (E), indicating the relative positions of the compensating irradiance (E_c) and saturating irradiance (E_k), and the daytime periods of light intensities exceeding E_c (H_com) and E_k (H_sat) [modified from [38]]. (B) Estimated daily light integral (DLI) at each inclination setting, indicating the relative proportions corresponding to sub-compensating, compensating, and saturating irradiance. Error bars describe standard deviations. (C) Estimated relative changes in light-induced processes affecting the energy balance of coral holobionts. PUES: photosynthetic usable energy supply; P_g: gross productivity of the zooxanthellae; C_a: metabolic costs of maintenance associated with zooxanthellae photosynthesis. Polynomial regressions were used to depict the relationships of these parameters with surface inclination angle.

Fig 6. Coral colonies of O. faveolata affected by environmental perturbations.

(A) Partial mortality observed in a coral colony in the Varadero Reef, an area experiencing elevated anthropogenic turbidity [57]. (B) Bleached and non-bleached regions within a colony during the widespread bleaching event that occurred in the Caribbean in 2010. It is noteworthy that in both conditions, the most affected areas are the low-productivity colony surfaces with the larger inclination angles.