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

Abstract

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 (CHAR DOC), 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.

Spatial variation in the biochemical and isotopic composition of corals during bleaching and recovery

“…The resistance and recovery of corals from bleaching stress is influenced by associations with thermally tolerant symbionts (Sampayo et al ), tissue biomass abundance (Thornhill et al ) and energetic quality (i.e., lipid content), and the capacity to maintain positive energy budgets through nutritional plasticity (Anthony et al ). Coral nutrition is largely supported by fixed carbon derived from endosymbiont algae; however, particle feeding (Mills et al ), plankton capture (Sebens et al ), and the uptake of dissolved compounds from seawater and sediments (Mills and Sebens ; Grover et al ; collectively, “heterotrophy”) can account for < 15–50% of energy demands (Porter ; Houlbrèque and Ferrier‐Pagès ) and > 100% of respiratory carbon demand in bleached corals (Grottoli et al ; Palardy et al ; Levas et al ). Facultative shifts from autotrophic to heterotrophic nutrition are often linked to reduced symbiont photosynthesis in response to periodic light attenuation (i.e., turbidity) and/or environmental stress (Houlbrèque and Ferrier‐Pagès ).…”

Physiological and Biogeochemical Responses of Super-Corals to Thermal Stress from the Northern Gulf of Aqaba, Red Sea

“…This is consistent with field-based findings showing that F. favus allocates a higher proportion of heterotrophic C to its lipids than does S. pistillata (Alamaru et al, 2009). In addition, some species are able to meet up to 36% of metabolic demand when bleached through the heterotrophic acquisition of dissolved and particulate organic carbon (Levas et al, 2013(Levas et al, , 2016. The lower overall δ 13 C h−e of F. favus suggests that when bleached it was able to take up dissolved and/or particulate organic carbon during the tank experiment to meet at least part of its metabolic demand heterotrophically.…”

“…Corals with elevated levels of energy reserves (i.e., lipids, protein, carbohydrates) either take longer to bleach, bleach less severely, and/or recover more quickly from bleaching than corals with lower energy reserves because they have an energy source to buffer them against losses in photosynthetically derived fixed carbon (e.g., Rodrigues and Grottoli, 2007;Anthony et al, 2009;Grottoli et al, 2014;Schoepf et al, 2015). Corals that increase their intake of heterotrophic carbon (i.e., zooplankton, dissolved and particulate organic carbon) or increase the proportionate contribution of heterotrophic vs. photoautotrophic carbon in their tissues when bleached, are able to partially or fully supplement the deficit in their carbon budgets due to declines in photosynthesis when bleached, and are able to recover more quickly from bleaching Rodrigues and Grottoli, 2006;Palardy et al, 2008;Levas et al, 2013Levas et al, , 2016. Corals that are able to shuffle or switch their dominant endosymbiont type for a thermally tolerant one are less sensitive to repeat exposures to thermal stress (e.g., Rowan et al, 1997;Baker et al, 2004;Berkelmans and van Oppen, 2006;Grottoli et al, 2014).…”

Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress

“…Corals utilize these autotrophic nutrients mainly for their daily metabolic needs but also for lipid synthesis2122, which can represent significant energy reserves that corals rely on during bleaching to support their metabolism2324, although it is not always the case25. Nevertheless, heterotrophic feeding (plankton predation, dissolved and particulate organic matter consumption) is an alternative nutrient source for corals2627 that has been proposed as a mechanism to help corals survive bleaching events28. However, ocean warming is causing a decrease in the nutrient enrichment of surface waters, a decline in zooplankton abundance293031 and direct shifts in zooplankton composition30.…”