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1. Trophic provisioning and parental trade-offs lead to successful reproductive performance in corals after a bleaching event

   https://doi.org/10.1038/s41598-022-21998-4  

   Rodrigues, Lisa J. ; Padilla-Gamiño, Jacqueline L. ( November 2022 , Scientific Reports)

   Warming ocean temperatures are severely compromising the health and resilience of coral reefs worldwide. Coral bleaching can affect coral physiology and the energy available for corals to reproduce. Mechanisms associated with reproductive allocation in corals are poorly understood, especially after a bleaching event occurs. Using isotopic labeling techniques, we traced the acquisition and allocation of carbon from adults to gametes by autotrophy and heterotrophy in previously bleached and non-bleachedMontipora capitataandPorites compressacorals. Experiments revealed that both species: (1) relied only on autotrophy to allocate carbon to gametes, while heterotrophy was less relied upon as a carbon source; (2) experienced a trade-off with less carbon available for adult tissues when provisioning gametes, especially when previously bleached; and (3) used different strategies for allocating carbon to gametes. Over time,M. capitataallocated 10% more carbon to gametes despite bleaching by limiting the allocation of carbon to adult tissues, with 50–80% less carbon allocated to bleached compared to non-bleached colonies. Over the same time period,P. compressamaintained carbon allocation to adult tissues, before allocating carbon to gametes. Our study highlights the importance of autotrophy for carbon allocation from adult corals to gametes, and species-specific differences in carbon allocation depending on bleaching susceptibility.

    

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

   https://doi.org/10.1111/1365-2435.13795  

   Wall, Christopher B. ; Ricci, Contessa A. ; Wen, Alexandra D. ; Ledbetter, Bren E. ; Klinger, Delania E. ; Mydlarz, Laura D. ; Gates, Ruth D. ; Putnam, Hollie M. ( April 2021 , Functional Ecology)

   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 ofMontipora capitatacorals dominated by heat‐sensitiveCladocopiumor heat‐tolerantDurusdiniumSymbiodiniaceae at two reef sites.

   Despite fewer degree heating weeks in the first‐bleaching event relative to the second (7 vs. 10),M. capitatableaching 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 freePlain Language Summarycan be found within the Supporting Information of this article.

    

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3. Shotgun Proteomics Identifies Active Metabolic Pathways in Bleached Coral Tissue and Intraskeletal Compartments

   https://doi.org/10.3389/fmars.2022.797517  

   Axworthy, J ; Timmins-Schiffman, E ; Brown, T ; Rodrigues, L ; Nunn, B ; PadillaGamino, JL. ( January 2022 , Frontiers in marine science)

   Seveso, D (Ed.)

   Coral bleaching events are increasing with such frequency and intensity that many of the world’s reef-building corals are in peril. Some corals appear to be more resilient after bleaching but the mechanisms underlying their ability to recover from bleaching and persist are not fully understood. We used shotgun proteomics to compare the proteomes of the outer layer (OL) tissue and inner core (IC) tissue and skeleton compartments of experimentally bleached and control (i.e., non-bleached) colonies of Montipora capitata, a perforate Hawaiian species noted for its resilience after bleaching. We identified 2,361 proteins in the OL and IC compartments for both bleached and non-bleached individuals. In the OL of bleached corals, 63 proteins were significantly more abundant and 28 were significantly less abundant compared to the OL of nonbleached corals. In the IC of bleached corals, 22 proteins were significantly more abundant and 17 were significantly less abundant compared to the IC of non-bleached corals. Gene ontology (GO) and pathway analyses revealed metabolic processes that were occurring in bleached corals but not in non-bleached corals. The OL of bleached corals used the glyoxylate cycle to derive carbon from internal storage compounds such as lipids, had a high protein turnover rate, and shifted reliance on nitrogen from ammonia to nitrogen produced from the breakdown of urea and betaine. The IC of bleached corals compartmentalized the shunting of glucose to the pentose phosphate pathway. Bleached corals increased abundances of several antioxidant proteins in both the OL and IC compartments compared to non-bleached corals. These results highlight contrasting strategies for responding to bleaching stress in different compartments of bleached M. capitata and shed light on some potential mechanisms behind bleaching resilience. 

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4. Divergent bleaching and recovery trajectories in reef-building corals following a decade of successive marine heatwaves

   https://doi.org/10.1073/pnas.2312104120  

   Brown, Kristen T. ; Lenz, Elizabeth A. ; Glass, Benjamin H. ; Kruse, Elisa ; McClintock, Rayna ; Drury, Crawford ; Nelson, Craig E. ; Putnam, Hollie M. ; Barott, Katie L. ( December 2023 , Proceedings of the National Academy of Sciences)

   Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,Montipora capitataandPorites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressaexhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitatarepeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitatadisplayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressaappeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene.

    

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5. Nitrogen pollution interacts with heat stress to increase coral bleaching across the seascape

   https://doi.org/10.1073/pnas.1915395117  

   Donovan, Mary K. ; Adam, Thomas C. ; Shantz, Andrew A. ; Speare, Kelly E. ; Munsterman, Katrina S. ; Rice, Mallory M. ; Schmitt, Russell J. ; Holbrook, Sally J. ; Burkepile, Deron E. ( February 2020 , Proceedings of the National Academy of Sciences)

   Climate change is increasing the frequency and magnitude of temperature anomalies that cause coral bleaching, leading to widespread mortality of stony corals that can fundamentally alter reef structure and function. However, bleaching often is spatially variable for a given heat stress event, and drivers of this heterogeneity are not well resolved. While small-scale experiments have shown that excess nitrogen can increase the susceptibility of a coral colony to bleaching, we lack evidence that heterogeneity in nitrogen pollution can shape spatial patterns of coral bleaching across a seascape. Using island-wide surveys of coral bleaching and nitrogen availability within a Bayesian hierarchical modeling framework, we tested the hypothesis that excess nitrogen interacts with temperature anomalies to alter coral bleaching for the two dominant genera of branching corals in Moorea, French Polynesia. For both coral genera,PocilloporaandAcropora, heat stress primarily drove bleaching prevalence (i.e., the proportion of colonies on a reef that bleached). In contrast, the severity of bleaching (i.e., the proportion of an individual colony that bleached) was positively associated with both heat stress and nitrogen availability for both genera. Importantly, nitrogen interacted with heat stress to increase bleaching severity up to twofold when nitrogen was high and heat stress was relatively low. Our finding that excess nitrogen can trigger severe bleaching even under relatively low heat stress implies that mitigating nutrient pollution may enhance the resilience of coral communities in the face of mounting stresses from global climate change.

    

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