Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity

Abstract

The potential effects of seasonal acclimatization on coral sensitivity to heat-stress, has received limited attention despite differing bleaching thresholds for summer and winter. In this study, we examined the response of two contrasting phenotypes, termed winter and summer, of four Caribbean reef corals to similar light and heat-stress levels. The four species investigated were categorized into two groups: species with the ability to harbour large number of symbionts, Orbicella annularis and O. faveolata, and species with reduced symbiont density (Montastraea cavernosa and Pseudodiploria strigosa). The first group showed higher capacity to enhance photosynthetic rates per area (P_max), while P_max enhancement in the second group was more dependent on Symbiodinium performance (P_sym). In summer all four species presented higher productivity, but also higher sensitivity to lose coral photosynthesis under heat-stress. In contrast, corals in winter exhibit symbionts with higher capacity to photoacclimate to the increased levels of light-stress elicited by heat-stress. Overall, our study supports the importance of the acclimatory coral condition in addition to the previous thermal history, to determine the severity of the impact of heat-stress on coral physiology, but also the dependence of this response on the particular structural and functional traits of the species.

Figure 1

Description of the natural and experimental variation in light and temperature. (a) Monthly average values (thin lines) ± STD (shaded areas) for the annual variation of diurnal light exposure (mol quanta m⁻² day⁻¹) for the period 2011 to 2014 (in blue), and seawater temperature (°C) for the period 1992 to 2015 (in red). Thick solid lines describe average values during 2011for light exposure (blue line) and temperature (red line). Dashed horizontal red lines indicate annual average seawater temperature (28 °C), and local value for MMM (29.8 ≈ 30 °C), for the reef lagoon of Puerto Morelos. (b) Diurnal variation in light exposure (mol quanta m⁻² day⁻¹) during the experiments, values for March 2011 in grey, and for October 2011 in orange. The solid line represents diurnal light exposure for the medium-control light treatment (ML), whereas the upper and lower dashed lines describe, respectively, high light (HL) and low light (LL) treatment values. The red area from day 10 to day 20 shows the variation in diurnal light exposure during the extended 10 days of heat-stress applied in October 2011. In March, corals were back to control conditions (28 °C) after the application of the heat-stress treatments for 10 days.

Figure 2

Characterization of winter and summer coral phenotypes. Box plots describing the variability of the different descriptors used in this study to characterize both winter (dark color) and summer (light color) phenotypes of Orbicella annularis (grey), Orbicella faveolata (orange), Montastraea cavernosa (blue), and Pseudodiploria strigosa (green). Boxes encompass the 25 and 75% quartiles of all the data. The central line corresponds to the median, and bars extend to the 95% and 5% of the confidence limits. Asterisks indicate significant differences (t-test, p < 0.05) between phenotypes within species.

Figure 3

Principal component analysis (PCA) for the four coral species and two phenotypes investigated:. (a) grouping of the control specimens by species: O. annularis (grey), O. faveolata (orange), M. cavernosa (blue), and P. strigosa (green), based on the variability in their structural (Chla, symbiont, Ci, protein content), optical (a*_Chla, a*_sym, a*_M) and photo-physiological (P_max, P_sym, P_M) coral traits. Red arrows indicate the correlation of the different descriptors with PC1 and PC2; and (b) same analysis splitting each species by phenotype (summer phenotype in a lighter color).

Figure 4

Scaling quotient of temperature (Q₁₀). Mean ± SE (n = 5) of the maximum gross photosynthesis rates (P_max, circles), post-illumination respiration rates (triangles), P/R ratio (squares), and calcification rates (diamonds), for the winter (dark color) and summer (light color) phenotypes of Orbicella annularis (grey), Orbicella faveolata (orange), Montastraea cavernosa (blue), and Pseudodiploria strigosa (green). Negative values for coral calcification (grey area) are considered as indication of coral decalcification activity.

Figure 5

Response of coral structural descriptors to heat-stress. Box plots describing the variability of the structural descriptors for the four coral species investigated: Orbicella annularis, Orbicella faveolata, Montastraea cavernosa, and Pseudodiploria strigosa. Each plot describes coral responses in March (winter phenotype) and October (summer phenotype) after 10 days (white area) and 20 days (red area) of exposure to control (28 °C; grey), and heat-stress conditions of +2 °C (30 °C; orange), and +4 °C (32 °C; red). Boxes encompass the 25 and 75% quartiles of all the data (n = 5). The central line corresponds to the median, and bars extend to the 95% and 5% of confidence limits. Letters mark significant differences (Tukey Post-Hoc test, p < 0.05) between treatments within a season.

Figure 6

Response of coral photosynthesis to heat-stress. (a–d) Daily averages for F _v /F _m recorded at dusk (n > 10) for corals exposed to control (28 °C, black triangles), 30 °C (orange triangles) and 32 °C (red triangles) in March (winter phenotype) and October (summer phenotype). (e–p) Box plots describing the variability of the photosynthetic responses of the four coral species investigated: Orbicella annularis, Orbicella faveolata, Montastraea cavernosa, and Pseudodiploria strigosa. Each plot describes coral responses in March (winter phenotype) and October (summer phenotype), after 10 days (white area) and 20 days (red area) of exposure to control (28 °C; grey), 30 °C (orange), and 32 °C (red). Boxes encompass the 25 and 75% quartiles of all the data (n = 5). The central line corresponds to the median, and bars extend to the 95% and 5% of the confidence limits. Letters mark the significant differences (Tukey Post-Hoc test, p < 0.05) between treatments within a season.

Figure 7

Principal component analysis (PCA) for control and heat-stressed corals. (a) grouping of control (dark grey circles), heat-stressed (grey circles) and bleached (light grey triangles) coral phenotypes, based on optical (a*_Chla, a*_sym, a*_M) and photo-physiological (P_max, P_sym, P_M) coral traits. Red arrows indicate the correlation of the different descriptors with PC1 and PC2. (b) grouping of control, heat-stressed and bleached corals based on the same descriptors per species: O. annularis (blue), O. faveolata (orange), M. cavernosa (green), and P. strigosa (red). Different shading illustrates differences from unstressed (dark) to bleached (lighter) phenotypes.