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1. Persistence of phenotypic responses to short-term heat stress in the tabletop coral Acropora hyacinthus

   https://doi.org/10.1371/journal.pone.0269206  

   Walker, Nia S. ; Cornwell, Brendan H. ; Nestor, Victor ; Armstrong, Katrina C. ; Golbuu, Yimnang ; Palumbi, Stephen R. ( September 2022 , PLOS ONE)

   Voolstra, Christian R. (Ed.)

   Widespread mapping of coral thermal resilience is essential for developing effective management strategies and requires replicable and rapid multi-location assays of heat resistance and recovery. One- or two-day short-term heat stress experiments have been previously employed to assess heat resistance, followed by single assays of bleaching condition. We tested the reliability of short-term heat stress resistance, and linked resistance and recovery assays, by monitoring the phenotypic response of fragments from 101Acropora hyacinthuscolonies located in Palau (Micronesia) to short-term heat stress. Following short-term heat stress, bleaching and mortality were recorded after 16 hours, daily for seven days, and after one and two months of recovery. To follow corals over time, we utilized a qualitative, non-destructive visual bleaching score metric that correlated with standard symbiont retention assays. The bleaching state of coral fragments 16 hours post-heat stress was highly indicative of their state over the next 7 days, suggesting that symbiont population sizes within corals may quickly stabilize post-heat stress. Bleaching 16 hours post-heat stress predicted likelihood of mortality over the subsequent 3–5 days, after which there was little additional mortality. Together, bleaching and mortality suggested that rapid assays of the phenotypic response following short-term heat stress were good metrics of the total heat treatment effect. Additionally, our data confirm geographic patterns of intraspecific variation in Palau and show that bleaching severity among colonies was highly correlated with mortality over the first week post-stress. We found high survival (98%) and visible recovery (100%) two months after heat stress among coral fragments that survived the first week post-stress. These findings help simplify rapid, widespread surveys of heat sensitivity inAcropora hyacinthusby showing that standardized short-term experiments can be confidently assayed after 16 hours, and that bleaching sensitivity may be linked to subsequent survival using experimental assessments.

    

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2. Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

   https://doi.org/10.1111/gcb.17088  

   Vompe, Alex D. ; Epstein, Hannah E. ; Speare, Kelly E. ; Schmeltzer, Emily R. ; Adam, Thomas C. ; Burkepile, Deron E. ; Sharpton, Thomas J. ; Vega Thurber, Rebecca ( December 2023 , Global Change Biology)

   Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large‐scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long‐term (28 months, 2018–2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves inAcropora retusa,Porites lobata, andPocilloporaspp., which included: microbiome acclimatization inA. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocilloporaspp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusaboth significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobatacolonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality inA. retusa. This study reveals evidence for coral species‐specific microbial responses to repeated heatwaves and, importantly, suggests that host‐dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.

    

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3. Divergent responses of the coral holobiont to deoxygenation and prior environmental stress

   https://doi.org/10.3389/fmars.2023.1301474  

   Swaminathan, Sara D. ; Meyer, Julie L. ; Johnson, Maggie D. ; Paul, Valerie J. ; Bartels, Erich ; Altieri, Andrew H. ( February 2024 , Frontiers in Marine Science)

   Ocean deoxygenation is intensifying globally due to human activities – and is emerging as a grave threat to coral reef ecosystems where it can cause coral bleaching and mass mortality. However, deoxygenation is one of many threats to coral reefs, making it essential to understand how prior environmental stress may influence responses to deoxygenation. To address this question, we examined responses of the coral holobiont (i.e., the coral host, Symbiodiniaceae, and the microbiome) to deoxygenation in corals with different environmental stress backgrounds. We outplantedAcropora cervicornisfragments of known genotypes from anin situnursery to two sites in the Florida Keys spanning an inshore-offshore gradient. After four months, fragments from the outplanted corals were transferred to the laboratory, where we tested differences in survivorship, tissue loss, photosynthetic efficiency, Symbiodiniaceae cell density, and coral microbiome composition after persistent exposure to one of four oxygen treatments ranging from extreme deoxygenation (0.5 mg L^-1) to normoxia (6 mg L^-1). We found that, for the short duration of exposure tested in this study (four days), the entire coral holobiont was resistant to dissolved oxygen (DO) concentrations as low as 2.0 mg L^-1, but that the responses of members of the holobiont decoupled at 0.5 mg L^-1. In this most extreme treatment, the coral host showed decreased photosynthetic efficiency, tissue loss, and mortality, and lower Symbiodiniaceae densities in a bleaching response, but most microbial taxa remained stable. Although deoxygenation did not cause major community shifts in microbiome composition, the population abundance of some microbial taxa did respond. Site history influenced some responses of the coral host and endosymbiont, but not the coral microbiome, with corals from the more stressful inshore site showing greater susceptibility to subsequent deoxygenation. Our study reveals that coral holobiont members respond differently to deoxygenation, with greater sensitivity in the coral host and Symbiodiniaceae and greater resistance in the coral microbiome, and that prior stress exposure can decrease host tolerance to deoxygenation.

    

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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. The Coral Bleaching Automated Stress System (CBASS): A low‐cost, portable system for standardized empirical assessments of coral thermal limits

   https://doi.org/10.1002/lom3.10555  

   Evensen, Nicolas R. ; Parker, Katherine E. ; Oliver, Thomas A. ; Palumbi, Stephen R. ; Logan, Cheryl A. ; Ryan, James S. ; Klepac, Courtney N. ; Perna, Gabriela ; Warner, Mark E. ; Voolstra, Christian R. ; et al ( May 2023 , Limnology and Oceanography: Methods)

   Ocean warming is increasingly affecting marine ecosystems across the globe. Reef‐building corals are particularly affected by warming, with mass bleaching events increasing in frequency and leading to widespread coral mortality. Yet, some corals can resist or recover from bleaching better than others. Such variability in thermal resilience could be critical to reef persistence; however, the scientific community lacks standardized diagnostic approaches to rapidly and comparatively assess coral thermal vulnerability prior to bleaching events. We present the Coral Bleaching Automated Stress System (CBASS) as a low‐cost, open‐source, field‐portable experimental system for rapid empirical assessment of coral thermal thresholds using standardized temperature stress profiles and diagnostics. The CBASS consists of four or eight flow‐through experimental aquaria with independent water masses, lighting, and individual automated temperature controls capable of delivering custom modulating thermal profiles. The CBASS is used to conduct daily thermal stress exposures that typically include 3‐h temperature ramps to multiple target temperatures, a 3‐h hold period at the target temperatures, and a 1‐h ramp back down to ambient temperature, followed by an overnight recovery period. This mimics shallow water temperature profiles observed in coral reefs and prompts a rapid acute heat stress response that can serve as a diagnostic tool to identify putative thermotolerant corals for in‐depth assessments of adaptation mechanisms, targeted conservation, and possible use in restoration efforts. The CBASS is deployable within hours and can assay up to 40 coral fragments/aquaria/day, enabling high‐throughput, rapid determination of thermal thresholds for individual genotypes, populations, species, and sites using a standardized experimental framework.

    

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