Redox-sensitive δ65Cu isotopic fractionation in the tissue of the scleractinian coral Stylophora pistillata: a biomarker of holobiont photophysiology following volcanic ash exposure

Abstract

Volcanic ash is a significant source of micronutrients including iron (Fe), copper (Cu), and zinc (Zn) in oligotrophic tropical waters. These bioactive metals enhance primary productivity, influencing local and global biogeochemical cycles. This study explores how volcanic ash exposure affects trace metal uptake and photophysiological response, and how redox-sensitive metal stable isotope measurements in the tissues of the scleractinian coral Stylophora pistillata can provide crucial information on coral health. Controlled coral culture experiments were conducted in which coral nubbins were exposed to varying intensity and duration of volcanic ash. Throughout the experiment, coral symbionts showed enhanced photosynthetic performance irrespective of intensity or duration of ash exposure. Stable isotopes, such as δ65Cu and δ56Fe, in the coral tissue are marked by systematic variations, not associated with intensity or duration of ash exposure. Instead, we suggest biologically modulated redox-sensitive fractionation associated with ash exposure, linked to the coral host's oxidative stress state. This is evidenced by significant correlations between δ65Cu in coral hosts and photophysiology, with lighter Cu isotope ratios associated with higher photosynthetic performances. Hence, we propose that δ65Cu, and more generally redox-sensitive isotopic ratios (i.e. δ56Fe), in coral hosts serves as an indicator of the physiological state of symbiotic corals.

Graphical Abstract

Figure 1.

(A) Experimental setup. The colour gradient in the tanks indicates the intensity of ash exposure. Nubbins of Stylophora pistillata were maintained under constant light intensity and water temperature. Control tank nubbins were sampled simultaneously with the 7.5 g/week condition at the end of the 6-week period. n represents the number of analysed nubbins (n = 6 per condition), with the number in brackets [] showing the total number of nubbins in the tank. The lower part (B) lists the measurements performed on nubbins from the corresponding tanks.

Figure 2.

Effective quantum yield of PSII (Φ_PSII) of Stylophora pistillata maintained under four different exposure conditions: no ash (grey dotted), 3.75 g/week for 3 weeks (light grey), 7.5 g/week for 3 (dark grey) and 6 weeks (black) (n = 6 per condition). Data are presented as mean ± SD.

Figure 3.

Effects of ash intensity on metal isotope ratios in the soft tissue of Stylophora pistillata. (A) δ⁵⁶Fe, δ⁶⁵Cu, and δ⁶⁶Zn in the host tissue maintained under four ash exposure conditions. Data are presented as the mean (◇) of individual measurements in host tissue (□). Effects of (B) ash loading and (C) exposure duration on δ⁵⁶Fe, δ⁶⁵Cu, and δ⁶⁶Zn in symbionts and coral host. Data are presented as the deviation of the means of ash-exposed conditions relative to the non-exposed (∆) ± SD. The white-to-black colour gradient resembles the intensity of ash exposure. Statistically significant differences between treatments are represented by asterisks (*), with an indication of the level of significance in the number of asterisks.

Figure 4.

Relationship between δ⁶⁵Cu_{Coral host} in Stylophora pistillata and various photosynthetic parameters. (A) Effective quantum yield value of PSII (Φ_PSII), with each point representing the mean of Φ_PSII per tank ± SD. (B) Net photosynthesis and respiration rates of non-exposed (□) and 6-week ash-exposed nubbins (■). Change in oxygen concentration per hour is normalized by the number of symbiont cells. Each point represents the mean oxygen production/consumption per tank ± SD (n = 3). (C) RLC-derived photochemical parameters: total effective quantum yield of PSII (F_v/F_m), relative electron transport rate (rETR), and non-photochemical quenching (NPQ) in dark-adapted corals. Each point (Δ for nubbins exposed for 6 weeks to 7.5 g/week, and □ for non-exposed corals) represents the mean value of the respective parameter ± SD (n = 3 per tank).

Figure 5.

Indications of Cu/Zn SOD upregulation in Stylophora pistillata soft tissue. (A) Relationship between Cu and Zn concentration in the host tissue and symbionts with corresponding trendlines. (B) Influence of the Cu/Zn ratio as a biomarker for oxidative stress on δ⁶⁵Cu_{Coral host}. Data are presented as the mean (◇) of individual measurements in the host tissue (□). The white-to-black colour gradient resembles the intensity of ash exposure.