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1. 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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2. Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata

   https://doi.org/10.7717/peerj.12335  

   Williams, Amanda ; Pathmanathan, Jananan S. ; Stephens, Timothy G. ; Su, Xiaoyang ; Chiles, Eric N. ; Conetta, Dennis ; Putnam, Hollie M. ; Bhattacharya, Debashish ( January 2021 , PeerJ)

   Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata . Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata . Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata , which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species. 

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3. 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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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. Effects of sediment exposure on corals: a systematic review of experimental studies

   https://doi.org/10.1186/s13750-022-00256-0  

   Tuttle, Lillian J. ; Donahue, Megan J. ( December 2022 , Environmental Evidence)

   Abstract Background Management actions that address local-scale stressors on coral reefs can rapidly improve water quality and reef ecosystem condition. In response to reef managers who need actionable thresholds for coastal runoff and dredging, we conducted a systematic review and meta-analysis of experimental studies that explore the effects of sediment on corals. We identified exposure levels that ‘adversely’ affect corals while accounting for sediment bearing (deposited vs. suspended), coral life-history stage, and species, thus providing empirically based estimates of stressor thresholds on vulnerable coral reefs. Methods We searched online databases and grey literature to obtain a list of potential studies, assess their eligibility, and critically appraise them for validity and risk of bias. Data were extracted from eligible studies and grouped by sediment bearing and coral response to identify thresholds in terms of the lowest exposure levels that induced an adverse physiological and/or lethal effect. Meta-regression estimated the dose–response relationship between exposure level and the magnitude of a coral’s response, with random-effects structures to estimate the proportion of variance explained by factors such as study and coral species. Review findings After critical appraisal of over 15,000 records, our systematic review of corals’ responses to sediment identified 86 studies to be included in meta-analyses (45 studies for deposited sediment and 42 studies for suspended sediment). The lowest sediment exposure levels that caused adverse effects in corals were well below the levels previously described as ‘normal’ on reefs: for deposited sediment, adverse effects occurred as low as 1 mg/cm 2 /day for larvae (limited settlement rates) and 4.9 mg/cm 2 /day for adults (tissue mortality); for suspended sediment, adverse effects occurred as low as 10 mg/L for juveniles (reduced growth rates) and 3.2 mg/L for adults (bleaching and tissue mortality). Corals take at least 10 times longer to experience tissue mortality from exposure to suspended sediment than to comparable concentrations of deposited sediment, though physiological changes manifest 10 times faster in response to suspended sediment than to deposited sediment. Threshold estimates derived from continuous response variables (magnitude of adverse effect) largely matched the lowest-observed adverse-effect levels from a summary of studies, or otherwise helped us to identify research gaps that should be addressed to better quantify the dose–response relationship between sediment exposure and coral health. Conclusions We compiled a global dataset that spans three oceans, over 140 coral species, decades of research, and a range of field- and lab-based approaches. Our review and meta-analysis inform the no-observed and lowest-observed adverse-effect levels (NOAEL, LOAEL) that are used in management consultations by U.S. federal agencies. In the absence of more location- or species-specific data to inform decisions, our results provide the best available information to protect vulnerable reef-building corals from sediment stress. Based on gaps and limitations identified by our review, we make recommendations to improve future studies and recommend future synthesis to disentangle the potentially synergistic effects of multiple coral-reef stressors. 

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