Trade-offs in a reef-building coral after six years of thermal acclimation

Abstract

Evidence is growing that reef-building corals have the capacity to acclimate to new and challenging thermal conditions by increasing their thermal resistance. This raises hopes for their future persistence in a warming world. However, potential trade-offs that accompany such resistance gains, have remained largely unexplored. We provide the first report on the physiological trade-offs in a globally abundant and ecologically relevant coral species (Pocillopora acuta), after a long-term exposure to an elevated temperature of 31 {degrees}C in comparison to conspecifics cultivated under a cooler control thermal regime. At both temperatures, corals consistently appeared to be visually healthy throughout a six-year period. At 31 {degrees}C, corals had increased metabolic rates (both respiration and photosynthesis) that resulted in higher biomass accumulation and total energy reserves compared to the corals from the ambient regime. Further, the composition of coral host tissues shifted in favor of lipid build-up, suggesting an altered mechanism of energy storage. The increase in biomass growth came at the cost of declining skeletal growth rates and the formation of higher density skeletons. In the long-term, this trade-off will result in lower extension rates that can entail major ramifications for future reef building processes and reef community composition. Moreover, symbionts at 31 {degrees}C were physiologically more compromised with overall lower energy reserves, possibly indicating a stronger exploitation by the host and potentially a lower stress resilience. Our study provides first insights into a successful thermal acclimation mechanism that involved the prioritization of energy storage over skeletal growth, entailing higher demands on the symbionts. Our observation in this 6-year study does not align with observations of short-term studies, where elevated temperatures caused a depletion of tissue lipids in corals, which highlights the importance of studying acclimation of organisms over their relevant biological scales. Further investigations into trade-offs at biologically relevant scales and how they unfold under an acute heat stress will help to provide a more comprehensive picture of the future coral reef trajectory. Importantly, these insights will also help improve interventions aimed at increasing the thermal resilience of corals which anticipate to use thermal preconditioning treatments for stress-hardening. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=96 SRC="FIGDIR/small/549699v2_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@139b33corg.highwire.dtl.DTLVardef@1264477org.highwire.dtl.DTLVardef@158f7c9org.highwire.dtl.DTLVardef@1f3c35a_HPS_FORMAT_FIGEXP M_FIG C_FIG