Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals?

Annual coral bleaching events due to increasing sea surface temperatures are predicted to occur globally by the mid-century and as early as 2025 in the Caribbean, and severely impact coral reefs. We hypothesize that heterotrophic carbon (C) in the form of zooplankton and dissolved organic carbon (DOC) is a significant source of C to bleached corals. Thus, the ability to utilize multiple pools of fixed carbon and/or increase the amount of fixed carbon acquired from one or more pools of fixed carbon (defined here as heterotrophic plasticity) could underlie coral acclimatization and persistence under future ocean-warming scenarios. Here, three species of Caribbean coral—Porites divaricata, P. astreoides, and Orbicella faveolata—were experimentally bleached for 2.5 weeks in two successive years and allowed to recover in the field. Zooplankton feeding was assessed after single and repeat bleaching, while DOC fluxes and the contribution of DOC to the total C budget were determined after single bleaching, 11 months on the reef, and repeat bleaching. Zooplankton was a large C source for P. astreoides, but only following single bleaching. DOC was a source of C for single-bleached corals and accounted for 11–36 % of daily metabolic demand (CHARDOC), but represented a net loss of C in repeat-bleached corals. In repeat-bleached corals, DOC loss exacerbated the negative C budgets in all three species. Thus, the capacity for heterotrophic plasticity in corals is compromised under annual bleaching, and heterotrophic uptake of DOC and zooplankton does not mitigate C budget deficits in annually bleached corals. Overall, these findings suggest that some Caribbean corals may be more susceptible to repeat bleaching than to single bleaching due to a lack of heterotrophic plasticity, and coral persistence under increasing bleaching frequency may ultimately depend on other factors such as energy reserves and symbiont shuffling