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1. Coral trophic pathways impact the allocation of carbon and nitrogen for egg development after bleaching

   https://doi.org/10.3389/fevo.2023.1251220  

   Jaffe, Melissa D; Padilla-Gamiño, Jacqueline L; Nunn, Brook L; Rodrigues, Lisa J (November 2023, Frontiers in Ecology and Evolution)

   The persistence of coral reefs requires the survival of adult coral colonies and their continued sexual reproduction despite thermal stress. To assess the trophic pathway (i.e., autotrophy and/or heterotrophy) used to develop gametes following bleaching, we thermally stressedMontipora capitatafor one month at a time when corals in Hawai’i typically experience elevated seawater temperatures. After six and nine months of recovery, we pulse-chased non-bleached and previously bleached colonies using a dual-label design to compare the allocation of carbon and nitrogen at significant stages of gamete development. Dissolved inorganic carbon- (DI¹³C) and nitrogen- (DI¹⁵N) labelled seawater or¹³C- and¹⁵N-labelled rotifers were used to assess the autotrophic and heterotrophic pathways, respectively. At multiple time points for up to two years later, we collected adult coral fragments and isolated host tissue, Symbiodiniaceae cells, and developing eggs and captured gamete bundles to analyze their carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes. We found that the presence of Symbiodiniaceae was important for gametogenesis in both non-bleached and previously bleached colonies in two main ways. First, autotrophically-acquired carbon and nitrogen were both allocated to gametes during development, suggesting that recovery of photosynthesis after bleaching is critical for gametogenesis. Second, only heterotrophically-acquired nitrogen, not carbon, was incorporated into gametes and was readily recycled between host tissues and Symbiodiniaceae cells. This suggests that one of the purposes of heterotrophy following coral bleaching forM. capitatamay be to supplement the nitrogen pool, providing available nutrients for endosymbiotic algal growth. Allocation of carbon and nitrogen to eggs coincided with the period when vertical transmission of symbionts to gametes occurs, further supporting the important relationship between gametogenesis and availability of Symbiodiniaceae forM. capitata. 

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2. 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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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. Parental effects provide an opportunity for coral resilience following major bleaching events

   https://doi.org/10.1371/journal.pone.0290479  

   Lenz, Elizabeth A; Donahue, Megan J; Gates, Ruth D; Putnam, Hollie M; van_der_Steeg, Eveline; Padilla-Gamiño, Jacqueline L (January 2025, PLOS ONE)

   Fujimura, Atsushi (Ed.)

   Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the speciesMontipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor × sperm donor: B × B, B × NB, NB × B, and NB × NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues inM.capitatapost-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs. 

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5. Physiological acclimatization in Hawaiian corals following a 22-month shift in baseline seawater temperature and pH

   https://doi.org/10.1038/s41598-022-06896-z  

   McLachlan, Rowan H.; Price, James T.; Muñoz-Garcia, Agustí; Weisleder, Noah L.; Levas, Stephen J.; Jury, Christopher P.; Toonen, Robert J.; Grottoli, Andréa G. (December 2022, Scientific Reports)

   Abstract Climate change poses a major threat to coral reefs. We conducted an outdoor 22-month experiment to investigate if coral could not just survive, but also physiologically cope, with chronic ocean warming and acidification conditions expected later this century under the Paris Climate Agreement. We recorded survivorship and measured eleven phenotypic traits to evaluate the holobiont responses of Hawaiian coral: color, Symbiodiniaceae density, calcification, photosynthesis, respiration, total organic carbon flux, carbon budget, biomass, lipids, protein, and maximum Artemia capture rate. Survivorship was lowest in Montipora capitata and only some survivors were able to meet metabolic demand and physiologically cope with future ocean conditions. Most M. capitata survivors bleached through loss of chlorophyll pigments and simultaneously experienced increased respiration rates and negative carbon budgets due to a 236% increase in total organic carbon losses under combined future ocean conditions. Porites compressa and Porites lobata had the highest survivorship and coped well under future ocean conditions with positive calcification and increased biomass, maintenance of lipids, and the capacity to exceed their metabolic demand through photosynthesis and heterotrophy. Thus, our findings show that significant biological diversity within resilient corals like Porites , and some genotypes of sensitive species, will persist this century provided atmospheric carbon dioxide levels are controlled. Since Porites corals are ubiquitous throughout the world’s oceans and often major reef builders, the persistence of this resilient genus provides hope for future reef ecosystem function globally. 

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