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

Abstract

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'i 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.

Transcriptomic plasticity and symbiont shuffling underpin Pocillopora acclimatization across heat-stress regimes in the Pacific Ocean

“…Constrained correspondence analysis of expression variation between islands, indicated that the strongest environmental factor contributing to colony gene expression was historical SST (Figure 6, Table S11). This is unsurprising given the primacy of temperature as an abiotic driver in ectothermic organisms generally (Somero et al 2017) and given its specific, disruptory, effects on regulatory homeostasis within scleractinian corals (Hughes et al 2018;Wall et al 2021). In addition, discriminant analysis of principal components of host gene expression indicated that one of the two top discriminant functions was tightly linked to historical SST (DF2).…”

“…In other cases, rapid thermal acclimation is achieved through altered gene expression in the host and/or symbiont (i.e., transcriptomic plasticity) resulting in increased whole organism (holobiont) thermal tolerance (Kenkel and Matz 2017;Savary et al 2021). Coral holobiont thermal sensitivity is therefore dependent on an array of interacting drivers, including environmental history (Middlebrook et al 2008;Safaie et al 2018;Schoepf et al 2020;Wall et al 2021;Savary et al 2021), endosymbiont community composition (Hoadley et al 2019;Qin et al 2019;Cunning and Baker 2020;Dilworth et al 2021), and host genotype (Barshis et al 2013;Dilworth et al 2021;Drury et al 2021). However, the relative role of each of these factors in determining holobiont expression in situ remains poorly resolved.…”

The Bouraké semi-enclosed lagoon (New Caledonia) – a natural laboratory to study the lifelong adaptation of a coral reef ecosystem to extreme environmental conditions

“…The reference collection is housed at the Institut de Recherche pour le Développement (IRD), Nouméa. Microscopic examination of the skeletal features allowed species-level identification following the reference literature (Veron and Wallace, 1984;Wallace, 1999;Veron, 2000). Sponges were identified based on their spicules' morphological characteristics (i.e., shape, length, and width) or using a series of morphological descriptors (e.g., shape, size, color, texture, surface ornamentations, fibers) for species without spicules.…”

“…Abiotic and biotic cover percentages averaged per transect and species richness, calculated as the number of species in the transect, were plotted using non-metric multidimensional scaling (nMDS) based on Bray-Curtis dissimilarities ("vegan" package in R) of square-root-transformed data. Finally, the best number of clusters for the whole Bouraké lagoon was determined using the gap statistic method ("cluster" and "factorextra" packages in R) and used for the hierarchical clustering representation (Ward, 1963). The cluster separation was verified with a two-way ANOSIM (ANalysis Of Similarities).…”

Coral environmental history is primary driver of algal symbiont composition, despite a mass bleaching event

“…The frequency of mass coral bleaching events worldwide has increased nearly fivefold in the past four decades (14)(15)(16)(17), resulting in significant losses of live coral in many parts of the world (18,19). Despite visual recovery, the impacts of bleaching may persist for years (10,20) and the increasing frequency and duration of marine heatwaves suggests there might not be enough time for corals to recover between bleaching events (18,21). Ocean temperatures are predicted to rise 1-2 o C under best-case emission scenarios (22), and coral persistence through increasingly frequent and severe heatwaves is dependent on the capacity to acclimatize or adapt to a rapidly changing environment (14,(23)(24)(25).…”