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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. Size‐dependent mortality of corals during marine heatwave erodes recovery capacity of a coral reef

   https://doi.org/10.1111/gcb.16000  

   Speare, Kelly E. ; Adam, Thomas C. ; Winslow, Erin M. ; Lenihan, Hunter S. ; Burkepile, Deron E. ( December 2021 , Global Change Biology)

   For many long‐lived taxa, such as trees and corals, older, and larger individuals often have the lowest mortality and highest fecundity. However, climate change‐driven disturbances such as droughts and heatwaves may fundamentally alter typical size‐dependent patterns of mortality and reproduction in these important foundation taxa. Working in Moorea, French Polynesia, we investigated how a marine heatwave in 2019, one of the most intense marine heatwaves at our sites over the past 30 years, drove patterns of coral bleaching and mortality. The marine heatwave drove island‐wide mass coral bleaching that killed up to 76% and 65% of the largest individuals of the two dominant coral genera,PocilloporaandAcropora, respectively. Colonies ofPocilloporaandAcropora≥30 cm diameter were ~3.5× and ~1.3×, respectively, more likely to die than colonies <30‐cm diameter. Typically, annual mortality in these corals is concentrated on the smallest size classes. Yet, this heatwave dramatically reshaped this pattern, with heat stress disproportionately killing larger coral colonies and equalizing annual mortality rates across the size spectrum. This shift in the size‐mortality relationship reduced the overall fecundity of these genera by >60% because big corals are disproportionately important for reproduction on reefs. Additionally, the survivorship of microscopic coral recruits, critical for the recovery of corals following disturbances, declined to 2%, over an order of magnitude lower compared to a year without elevated thermal stress, where 33% of coral recruits survived. While other research has shown that larger corals can bleach more frequently than smaller corals, we show the severe impact this phenomenon can have at the reef‐wide scale. As marine heatwaves become more frequent and intense, disproportionate mortality of the largest, most fecund corals and near‐complete loss of entire cohorts of newly‐settled coral recruits will likely reduce the recovery capacity of these iconic ecosystems.

    

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3. 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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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 legacy of stress: Coral bleaching impacts reproduction years later

   https://doi.org/10.1111/1365-2435.13653  

   Johnston, Erika C. ; Counsell, Chelsie W. W. ; Sale, Tayler L. ; Burgess, Scott C. ; Toonen, Robert J. ; Hopkins, ed., William ( August 2020 , Functional Ecology)

   The extent to which populations persist under environmental stress depends on the reproductive output of individuals that survive the stress. In coral systems, corals bleach in response to stress from elevated water temperature. However, little is known of the extent to which thermal stress impairs the reproductive capacity of the survivors over the following years, limiting the capacity to predict how populations will persist in the Anthropocene.

   Using histology to quantify the abundance and size of oocytes and spermaries per polyp, we tested how bleaching impairs the reproductive response of the coralPocillopora meandrinaover two reproductive seasons following the 2015 mass bleaching event in the Hawaiian Islands.

   We found that smaller colonies not only had a greater probability of bleaching but also suffered greater reproductive impacts over a longer time. In contrast, larger colonies generated comparable reproductive output regardless of bleaching severity, although bleached colonies generated smaller oocytes the year after bleaching.

   These results show that reproductive impacts of bleaching are more complex and size‐specific than commonly assumed. Therefore, estimates of bleaching mortality may underestimate the true impact of thermal stress on populations, especially as populations lose larger individuals from repeated and co‐occurring stressors.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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