Shifting baselines: Physiological legacies contribute to the response of reef corals to frequent heatwaves

Global climate change is altering coral reef ecosystems. Notably, marine heatwaves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid-century. Responses of corals to elevated seawater temperatures are modulated by abiotic factors (e.g. environmental regimes) and dominant Symbiodiniaceae endosymbionts that can shift coral traits and contribute to physiological legacy effects on future response trajectories. It is critical, therefore, to characterize shifting physiological and cellular states driven by these factors and evaluate their influence on in situ bleaching (and recovery) events. We use back-to-back bleaching events (2014, 2015) in Hawai\u27i to characterize the cellular and organismal phenotypes of Montipora capitata corals dominated by heat-sensitive Cladocopium or heat-tolerant Durusdinium Symbiodiniaceae at two reef sites. Despite fewer degree heating weeks in the first-bleaching event relative to the second (7 vs. 10), M. capitata bleaching severity was greater [bleached cover: ~70% (2014) vs. 50% (2015)] and environmental history (site effects) on coral phenotypes were more pronounced. Symbiodiniaceae affected bleaching responses, but immunity and antioxidant activity was similar in all corals, despite differences in bleaching phenotypes. We demonstrate that repeat bleaching triggers cellular responses that shift holobiont multivariate phenotypes. These perturbed multivariate phenotypes constitute physiological legacies, which set corals on trajectories (positive and/or negative) that influence future coral performance. Collectively, our data support the need for greater tracking of stress response in a multivariate context to better understand the biology and ecology of corals in the Anthropocene. A free Plain Language Summary can be found within the Supporting Information of this article