Shifting Baselines: Repeat bleaching drives coral physiotypes through environmental legacy and cellular memory

Abstract

O_LIGlobal climate change is altering coral reef ecosystems. Notably, marine heat waves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid-century. C_LIO_LIThe response of corals to elevated seawater temperatures can be modulated by abiotic factors at site of origin and dominant endosymbiont type, which can result in a shift in multiple coral traits and drive physiological legacy effects that influence the trajectory of reef corals under subsequent thermal stress events. It is critical, therefore, to evaluate the potential for shifting physiological and cellular baselines driven by these factors in in situ bleaching (and recovery) events. Here, we use the back-to-back regional bleaching events of 2014 and 2015 in the Hawaiian Islands and subsequent recovery periods to test the hypothesis that coral multivariate trait space (here termed physiotype, sensu (Van Straalen, 2003) shift in multiple bleaching events, modulated by both environmental histories and symbiotic partnerships (Symbiodiniaceae). C_LIO_LIDespite fewer degree heating weeks in the first-bleaching event relative to the second (7 vs. 10), bleaching severity in a dominant reef building coral on Hawaiian reefs, Montipora capitata, was greater (~70% vs. 50% bleached cover) and differences due to environmental history (reef site) were more pronounced. Melanin, an immune cytotoxic response, provided an initial defense during the first event, potentially priming antioxidant activity, which peaked in the second-bleaching event (i.e., a legacy effect). While magnitude of bleaching differed, immune response patterns were shared among corals harboring heat-sensitive and heat-tolerant Symbiodiniaceae. This supports a pattern of increased constitutive immunity in corals resulting from repeat bleaching events, with greater specialized enzymes (catalase, peroxidase, superoxide dismutase) and attenuated melanin synthesis. C_LIO_LIThis study demonstrates bleaching events have implications for reef corals beyond shaping their ecological assemblages. These events can change the magnitude and/or identity of response variables contributing to physiotype, thus generating physiological legacies carried over into the future. Quantifying baseline coral physiotypes and tracking their shifts will be critical to understanding and forecasting the effects of increased bleaching frequency on coral biology and ecology in the Anthropocene. C_LI