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1. Marine heatwaves depress metabolic activity and impair cellular acid–base homeostasis in reef‐building corals regardless of bleaching susceptibility

   https://doi.org/10.1111/gcb.15622  

   Innis, Teegan ; Allen‐Waller, Luella ; Brown, Kristen T. ; Sparagon, Wesley ; Carlson, Christopher ; Kruse, Elisa ; Huffmyer, Ariana S. ; Nelson, Craig E. ; Putnam, Hollie M. ; Barott, Katie L. ( April 2021 , Global Change Biology)

   Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching‐resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular‐level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching‐resistant and bleaching‐susceptible corals throughout the 2019 marine heatwave in Hawai'i, a repeat bleaching event that occurred 4 years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching‐susceptible corals had lower intracellular pH than bleaching‐resistant corals at the peak of bleaching for both symbiont‐hosting and symbiont‐free cells, indicating greater disruption of acid–base homeostasis in bleaching‐susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid–base regulation was significantly impaired at the cellular level even in bleaching‐resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid–base regulation may further exacerbate the physiological effects of climate change.

    

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2. The Costs and Benefits of Environmental Memory for Reef-Building Corals Coping with Recurring Marine Heatwaves

   https://doi.org/10.1093/icb/icac074  

   Brown, Kristen T. ; Barott, Katie L. ( June 2022 , Integrative And Comparative Biology)

   Marine heatwaves are occurring more frequently as climate change intensifies, resulting in global mass coral bleaching events several times per decade. Despite the time between marine heatwaves decreasing, there is evidence that reef-building corals can develop increased bleaching resistance across repetitive marine heatwaves. This phenomenon of acclimatization via environmental memory may be an important strategy to ensure coral persistence; however, we still understand very little about the apparent acclimatization or, conversely, sensitization (i.e., stress accumulation or weakening) of reef-building corals to consecutive heatwaves and its implications for the trajectory and resilience of coral reefs. Here, we highlight that not only will some corals become stress hardened via marine heatwaves, but many other individuals will suffer sensitization during repeat heatwaves that further exacerbates their stress response during repeat events and depresses fitness. Under current and predicted climate change, it is necessary to gain a better understanding of the acclimatization vs. sensitization trajectories of different species and individuals on the reef, as well as identify whether changes in bleaching susceptibility relates to physiological acclimatization, trade-offs with other biological processes, and ultimately coral persistence in the Anthropocene.

    

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3. Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

   https://doi.org/10.1111/gcb.14545  

   Manzello, Derek P. ; Matz, Mikhail V. ; Enochs, Ian C. ; Valentino, Lauren ; Carlton, Renee D. ; Kolodziej, Graham ; Serrano, Xaymara ; Towle, Erica K. ; Jankulak, Mike ( January 2019 , Global Change Biology)

   Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coralOrbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRADand profiled for algal symbiont abundance and type.O. faveolataat the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerantDurusdinium trenchii(formerlySymbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated byD. trenchii. 2bRADhost genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion ofD. trenchiiwas attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably,D. trenchiiwas rarely dominant inO. faveolatafrom the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance ofD. trenchiiwas likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys,O. faveolatawas most abundant, had the highest bleaching resistance, and contained the most corals dominated byD. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.

    

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4. Coral bleaching resistance variation is linked to differential mortality and skeletal growth during recovery

   https://doi.org/10.1111/eva.13500  

   Walker, Nia S. ; Nestor, Victor ; Golbuu, Yimnang ; Palumbi, Stephen R. ( February 2023 , Evolutionary Applications)

   The prevalence of global coral bleaching has focused much attention on the possibility of interventions to increase heat resistance. However, if high heat resistance is linked to fitness tradeoffs that may disadvantage corals in other areas, then a more holistic view of heat resilience may be beneficial. In particular, overall resilience of a species to heat stress is likely to be the product of both resistance to heat and recovery from heat stress. Here, we investigate heat resistance and recovery among individualAcropora hyacinthuscolonies in Palau. We divided corals into low, moderate, and high heat resistance categories based on the number of days (4–9) needed to reach significant pigmentation loss due to experimental heat stress. Afterward, we deployed corals back onto a reef in a common garden 6‐month recovery experiment that monitored chlorophylla, mortality, and skeletal growth. Heat resistance was negatively correlated with mortality during early recovery (0–1 month) but not late recovery (4–6 months), and chlorophyllaconcentration recovered in heat‐stressed corals by 1‐month postbleaching. However, moderate‐resistance corals had significantly greater skeletal growth than high‐resistance corals by 4 months of recovery. High‐ and low‐resistance corals on average did not exhibit skeletal growth within the observed recovery period. These data suggest complex tradeoffs may exist between coral heat resistance and recovery and highlight the importance of incorporating multiple aspects of resilience into future reef management programs.

    

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5. Coral thermal stress and bleaching enrich and restructure reef microbial communities via altered organic matter exudation

   https://doi.org/10.1038/s42003-023-05730-0  

   Sparagon, Wesley J. ; Arts, Milou G. I. ; Quinlan, Zachary A. ; Wegley Kelly, Linda ; Koester, Irina ; Comstock, Jacqueline ; Bullington, Jessica A. ; Carlson, Craig A. ; Dorrestein, Pieter C. ; Aluwihare, Lihini I. ; et al ( February 2024 , Communications Biology)

   Coral bleaching is a well-documented and increasingly widespread phenomenon in reefs across the globe, yet there has been relatively little research on the implications for reef water column microbiology and biogeochemistry. A mesocosm heating experiment and bottle incubation compared how unbleached and bleached corals alter dissolved organic matter (DOM) exudation in response to thermal stress and subsequent effects on microbial growth and community structure in the water column. Thermal stress of healthy corals tripled DOM flux relative to ambient corals. DOM exudates from stressed corals (heated and/or previously bleached) were compositionally distinct from healthy corals and significantly increased growth of bacterioplankton, enriching copiotrophs and putative pathogens. Together these results demonstrate how the impacts of both short-term thermal stress and long-term bleaching may extend into the water column, with altered coral DOM exudation driving microbial feedbacks that influence how coral reefs respond to and recover from mass bleaching events.

    

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