High nutrient concentrations as well as elevated temperature above summer mean monthly maximums have significant negative impacts on the physiology of the coral holobiont. However, moderate nutrient concentrations (< 6 μmol L−1 NO3− and 0.40 μmol L PO43−) have been shown to have a positive effect on coral and endosymbiont physiology and to minimize or mitigate the negative effects of summertime elevated temperature. As the oceans continue to warm, corals will face elevated temperatures in winter as well as summer. Yet, few studies have assessed the potential impacts of increases in winter temperature on corals and none have evaluated the possible mitigating or exacerbating effect of nutrients during warmer winters of the future. Here, we tested the effects of elevated temperature and moderate nutrients for 22 days during the winter on Montipora monasteriata, Acropora muricata, and Pocillopora damicornis in a fully factorial experiment with two seawater temperatures (average winter temperature and projected winter temperature later this century of + 4 °C) and two nutrient levels (ambient nutrients and moderate nutrients of + 4.0 μmol L−1 NO3− and + 0.20 μmol L−1 PO4−3). Coral tissue δ15N composition indicated that the added nitrate was taken up by the algal endosymbionts and transferred to the coral host in all three species under both temperature regimes. All three species significantly differed in their physiological profiles (chlorophyll a, protein, lipids, carbohydrates, biomass, and δ13Ch-e) and had species-specific physiological responses to the individual and synergistic effects of increased wintertime temperatures and moderate nutrients. Montipora monasteriata and A. muricata increased one or more energy reserves in response to the individual effects of moderate nutrients or increased temperatures. Pocillopora damicornis shifted their trophic status toward greater photoautotrophy under the combined effects of moderate nutrients and increased temperatures. Overall, our results indicate an overall net positive species-specific physiological responses to the individual and combined effects of moderate nutrients and increased winter temperatures.

Chlorophyll a is an essential photosynthetic pigment in the coral endosymbiotic algae (Symbiodiniaceae). In healthy corals there is often an exponential decay relationship between chlorophyll a per Symbiodiniaceae cell and Symbiodiniaceae cell density. However, few studies have explored the surface area normalized relationship of these two metrics. Here, we evaluated the strength and variability of these relationships between chlorophyll a concentration and Symbiodiniaceae cell density, chlorophyll a per Symbiodiniaceae cell and Symbiodiniaceae cell density, and how these relationships differ between regions, species, and coral health status. We performed regression analyses on 482 data points from 10 coral species originating from four regions. As expected overall, chlorophyll a increased as Symbiodiniaceae cell density increased and there was an exponential decay relationship between chlorophyll a per Symbiodiniaceae cell and Symbiodiniaceae cell density. However, the strength and statistical significance of these relationships varied, sometimes dramatically, among regions, species, and with coral health status. Thus, measurements of one of these variables is not always a good proxy for another, highlighting the importance of measuring both chlorophyll a and Symbiodiniaceae cell density when quantifying this aspect of coral physiology.

Coral reefs of the Florida Keys experienced the hottest summer on record in 2023, causing mass bleaching and mortality of scleractinian corals. Sea surface temperatures remained above 31°C for 41 days, exceeding all prior records for the region. Branching corals fared especially poorly, especially Acropora palmata, which has now been deemed functionally extinct across the entire Florida Reef Tract. High temperatures and prolonged thermal stress were the major causes of mortality. Our study investigates additional stressors contributing to coral mortality during the heatwave. Using benthic imagery, we show that during bleaching, coral tissue death is accelerated by proximity to disease. Using a Cox proportional hazard model, we found that, compared to initially healthy tissue on the same colony, disease lesions and neighboring tissue had a 3.8 times and 1.5 times higher risk of death, respectively. We show that these two stressors, working at different spatial scales, acted synergistically to increase mortality. Furthermore, from our in situ reef structural measurements, we found that during bleaching, coral survival was greatest along the reef edge. The reef displaces water, resulting in faster local velocity, which we hypothesize reduces the boundary layer at the tissue-water interface and thus simultaneously enhances the removal of cytotoxic metabolic wastes and the opportunity for coral heterotrophic feeding. Our findings reinforce the importance of the interactive effects of disease and reef topography on coral mortality, and suggest that restoration efforts should focus on reef edges where the chance of survival is improved relative to the reef interior.

Coral resilience to heat stress is higher in corals that eat more zooplankton. In addition, coral feeding on zooplankton increases as zooplankton concentrations increase. To leverage the advantage that zooplankton feeding has on coral resilience, we developed the Underwater Zooplankton Enhancement Light Array (UZELA). UZELA is a patented autonomous, submersible, and programmable underwater light that is deployable for 6 months on a single battery. With 1 h of operation per night, it locally concentrates naturally occurring zooplankton, providing corals with greater feeding opportunities. Field tests show that UZELA increases local zooplankton concentrations by sevenfold compared to adjacent non-UZELA controls and coral feeding rates by 10 to 50-fold in both healthy and bleached Montipora capitata and Porites compressa corals compared to conspecifics without UZELA. With the continuing decline of coral reefs, technologies that can enhance coral feeding could play a critical role in coral resilience for coral in restoration nurseries and on the reef.

Regulatory action could facilitate cross-border efforts to retain ecosystem function

Coral reefs are threatened worldwide from unprecedented increases in ocean temperatures, resulting in corals gradually living closer to their maximum thermal threshold. With ocean temperatures expected to warm up to 3 °C by 2100, understanding the effects of chronic elevated baseline temperature is important in determining the thermal physiological limits of corals and developing realistic restoration strategies to ensure the future of coral reefs. Here, we tested the effects of 26 weeks (i.e., six months) of elevated temperatures of + 2.5 °C (27.5 °C) and + 5 °C (30 °C) above a baseline of 25 °C on surface area growth, metabolic rates, energy reserves, assimilation of heterotrophically acquired food, and Symbiodiniaceae species composition in the aquaria-reared thermally tolerant coral Stylophorapistillata sourced from the northern Red Sea. Corals initially catabolized lipids while maintaining growth after 4 weeks of elevated baseline temperatures but acclimated after only 11 weeks. However, there was evidence of a long-term cumulative impact of chronic elevated temperatures after 26 weeks at 30 °C with corals experiencing higher metabolic demand and lower growth while maintaining biomass and energy reserves. Therefore, maintenance of tissue biomass and energy reserves appears to come at the cost of skeletal accretion but allows these corals to survive changes in baseline temperatures up to 30 °C. These physiological changes were not associated with Symbiodiniaceae species composition, which remained constant throughout the experiment. We also discovered that a return to 25 °C for four weeks allowed for recovery of metabolic demand and growth. Our data suggests that chronic exposure to high, sub-bleaching temperatures, a plausible scenario in the near future, will have some negative effects on coral growth and metabolism, but not survival. Thus, while S. pistillata survives but does not thrive under projected shifts in baseline temperature, this study shows hope for acclimatization to temperature shifts expected in the next 50 years.

Recruitment is a vital demographic process that replenishes populations and increases genetic variation, making it fundamental to ecological resilience. On coral reefs, rates of coral recruitment and post-recruitment survivorship are naturally low, resulting in a bottleneck to population growth and restoration efforts. Therefore, we investigated the potential that two technologies, specialized settlement modules and the Underwater Zooplankton Enhancement Light Array (UZELA), improve early life success. We hypothesized that greater complexity of specialized settlement modules increases larval settlement rates in tanks and the combination of settlement modules with UZELA increases subsequent recruit survivorship and growth on the reef. We found that complex settlement modules enhanced recruit settlement, survivorship, and growth relative to the lowest complexity module. The addition of UZELA to the settlement modules further doubled survivorship and quadrupled growth. Our experiment demonstrates a proof-of-concept that combining these novel technologies offers promise for reducing the time for corals to complete their most vulnerable phase of life, accelerating the timeline for establishing genetically diverse coral populations, and offering a possible step-function change in coral recruitment success that could help overcome the recruit survivorship bottleneck in coral restoration.

Coral bleaching is the largest global threat to coral reef ecosystem persistence this century. Advancing our understanding of coral bleaching and developing solutions to protect corals and the reefs they support are critical. In the present article, we, the US National Science Foundation-funded Coral Bleaching Research Coordination Network, outline future directions for coral bleaching research. Specifically, we address the need for embedded inclusiveness, codevelopment, and capacity building as a foundation for excellence in coral bleaching research and the critical role of coral-bleaching science in shaping policy. We outline a path for research innovation and technology and propose the formation of an international coral bleaching consortium that, in coordination with existing multinational organizations, could be a hub for planning, coordinating, and integrating global-scale coral bleaching research, innovation, and mitigation strategies. This proposed strategy for future coral bleaching research could facilitate a step-function change in how we address the coral bleaching crisis.

Coral ecosystems support a diverse array of marine life and healthy ecological functioning, yet they are vulnerable to decreases in ocean pH caused by anthropogenic carbon dioxide emissions. In temperate rocky reefs of the Mediterranean, the corals Cladocora caespitosa and Astroides calycularis live at sites with ambient seawater pH and at adjacent submarine volcanic CO2 vent sites with low seawater pH where it is more energetically demanding to grow. We collected corals from distinct ambient pH (average pHT 8.05) and lower pH CO2 vent sites (average pHT 7.74–7.90) and quantified their physiological health and heterotrophic capacity (i.e., feeding capacity). Both species at CO2 vent sites had higher heterotrophic capacity than their ambient site counterparts, enabling them to maintain energy reserves. Our results indicate that high heterotrophic capacity underlies the success of these two temperate corals at CO2 vent sites. Therefore, conservation of CO2 vent coral could be strategically important to maintaining rocky reef ecosystem function and ecological resilience in the Mediterranean.

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

Under the ongoing global change, a sustained reliance of symbiotic coral species on heterotrophy may support their resistance to climatic stressors. However, much remains unknown about the role of heterotrophy on coral reproduction, despite its key role in the persistence of coral populations and connectivity. In this study, we experimentally investigated how heterotrophic feeding of parental colonies of a symbiotic gorgonian may affect the larval release and their survival and settlement rates under both optimal and heat stress temperatures. A one-week delay in larval release in absence of heterotrophic inputs highlights its significant contribution to the gametogenesis. Moreover, heterotrophy also plays a crucial role in sustaining larval survival, as low-quality or smaller eggs produced in absence of heterotrophic inputs lead to significantly higher mortality of the resulting larvae, independently to their exposure to natural or warming temperatures. Overall, this study contributes to increase our understanding of the broader consequences of global change on coral populations under the globally forecasted reduction of primary production and zooplankton abundance.

Coral reefs are among the most sensitive ecosystems affected by ocean warming and acidification, and are predicted to collapse over the next few decades. Reefs are predicted to shift from net accreting calcifier-dominated systems with exceptionally high biodiversity to net eroding algal-dominated systems with dramatically reduced biodiversity. Here, we present a two-year experimental study examining the responses of entire mesocosm coral reef communities to warming (+2 °C), acidification (-0.2 pH units), and combined future ocean (+2 °C, -0.2 pH) treatments. Contrary to modeled projections, we show that under future ocean conditions, these communities shift structure and composition yet persist as novel calcifying ecosystems with high biodiversity. Our results suggest that if climate change is limited to Paris Climate Agreement targets, coral reefs could persist in an altered state rather than collapse.

AbstractUnder predicted future ocean conditions, corals will experience frequent and intense thermal stress events while simultaneously being exposed to chronic ocean acidification. Yet, some corals will likely be more resistant and/or resilient to these predicted conditions than others and may be critical to reef persistence in the future. Following natural thermal stress in two consecutive years (2014 and 2015), we evaluated the effects of feeding and simulated ocean acidification on the physiological recovery of Montipora capitata and Porites compressa sourced from Kāneʻohe Bay and Waimānalo Bay, Hawaiʻi. Following the 2014 thermal stress event, simulated ocean acidification did not slow recovery of the holobiont and feeding enhanced recovery. However, feeding did not decrease susceptibility to the 2015 thermal stress event, and simulated ocean acidification did not increase susceptibility. Recovery strategies employed between species and between sites clearly differed, highlighting that coral reef restoration and management should consider species-level and site-specific vulnerabilities. Overall, our findings call attention to the immediate threat which ocean warming presents, the lack of additional stress to the holobiont from ocean acidification, the importance of heterotrophy in coral resilience, and the potential significance of additional local biotic stressors (i.e., predator outbreaks) for coral resiliency under annual thermal stress.

As climate change intensifies, a primary role of coral restoration is to maintain genetic diversity and ecosystem function while preventing species extinction, at least until global measures to slow the rate of climate change take effect. Recently, the idea of selectively breeding corals with higher heat tolerance (sometimes called “super corals”), and using them to repopulate reefs, has gained wide attention. We outline several reasons why selective breeding for heat tolerance alone is unlikely to yield corals that could be used universally for restoring natural reefs. We propose a managed breeding strategy where a range of traits is considered when choosing corals for breeding and where success is more likely when young offspring bred for these traits are exposed to natural selection in the wild, rather than to artificial selection in nurseries or tanks. However, as extinction risk increases, managing to increase population size becomes the primary goal and all causes of mortality may need to be minimized. In light of these considerations, there is an urgent need to formulate genetic management plans that consider demographic and genetic information for each population under restoration.

The global increase in anthropogenic CO2 is leading to ocean warming and acidification, which is threatening corals. In Ischia, Italy, two species of Mediterranean scleractinian corals-the symbiotic Cladocora caespitosa and the asymbiotic Astroides calycularis-were collected from ambient pH sites (average pHT = 8.05) and adjacent CO2 vent sites (average pHT = 7.8) to evaluate their response to ocean acidification. Coral colonies from both sites were reared in a laboratory setting for six months at present day pH (pHT ~ 8.08) or low pH (pHT ~7.72). Previous work showed that these corals were tolerant of low pH and maintained positive calcification rates throughout the experiment. We hypothesized that these corals cope with low pH by increasing their heterotrophic capacity (i.e., feeding and/or proportion of heterotrophically derived compounds incorporated in their tissues), irrespective of site of origin, which was quantified indirectly by measuring δ13C, δ15N, and sterols. To further characterize coral health, we quantified energy reserves by measuring biomass, total lipids, and lipid classes. Additional analysis for C. caespitosa included carbohydrates (an energy reserve) and chlorophyll a (an indicator of photosynthetic capacity). Isotopic evidence shows that ambient-sourced Mediterranean corals, of both species, decreased heterotrophy in response to six months of low pH. Despite maintaining energy reserves, lower net photosynthesis (C. caespitosa) and a trend of declining calcification (A. calycularis) suggest a long-term cost to low heterotrophy under ocean acidification conditions. Conversely, vent-sourced corals maintained moderate (C. caespitosa) or high (A. calycularis) heterotrophic capacity and increased photosynthesis rates (C. caespitosa) in response to six months at low pH, allowing them to sustain themselves physiologically. Provided there is sufficient zooplankton and/or organic matter to meet their heterotrophic needs, vent-sourced corals are more likely to persist this century and potentially be a source for new corals in the Mediterranean.

The plasticity of some coral-associated microbial communities under stressors like warming and ocean acidification suggests the microbiome has a role in the acclimatization of corals to future ocean conditions. Here, we evaluated the acclimatization potential of coral-associated microbial communities of four Hawaiian coral species (Porites compressa, Porites lobata, Montipora capitata, and Pocillopora acuta) over 22-month mesocosm experiment. The corals were exposed to one of four treatments: control, ocean acidification, ocean warming, or combined future ocean conditions. Over the 22-month study, 33-67% of corals died or experienced a loss of most live tissue coverage in the ocean warming and future ocean treatments while only 0-10% died in the ocean acidification and control. Among the survivors, coral-associated microbial communities responded to the chronic future ocean treatment in one of two ways: (1) microbial communities differed between the control and future ocean treatment, suggesting the potential capacity for acclimatization, or (2) microbial communities did not significantly differ between the control and future ocean treatment. The first strategy was observed in both Porites species and was associated with higher survivorship compared to M. capitata and P. acuta which exhibited the second strategy. Interestingly, the microbial community responses to chronic stressors were independent of coral physiology. These findings indicate acclimatization of microbial communities may confer resilience in some species of corals to chronic warming associated with climate change. However, M. capitata genets that survived the future ocean treatment hosted significantly different microbial communities from those that died, suggesting the microbial communities of the survivors conferred some resilience. Thus, even among coral species with inflexible microbial communities, some individuals may already be tolerant to future ocean conditions. These findings suggest that coral-associated microbial communities could play an important role in the persistence of some corals and underlie climate change-driven shifts in coral community composition.

The iconic and threatened Caribbean coral, Acropora palmata , is an essential reef-ecosystem engineer. Understanding the processes underpinning this coral’s survival and growth is essential to restoring this foundational species. Here, we compared replicate A. palmata colonies transplanted along 350 km of Florida’s offshore coral reef to determine holobiont and/or environmental variables that predict transplant success. We found a west-to-east gradient in coral physiology coupled with site-specific coral-associated microbiomes. Interestingly, no variables were linked to coral genet. Our results suggest that the unique oceanographic conditions with periodic upwelling events in the Dry Tortugas provide corals with greater opportunity for heterotrophy that in turn enhances coral growth and survivorship, and positively influences the microbiome. Our findings indicate that restoration efforts in the Dry Tortugas, and other places exhibiting higher food availability, could be most effective for A. palmata .

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.

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at −80 °C to −20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses.