Heterotrophy in marine animal forests in an era of climate change.

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.

Long-term coral microbial community acclimatization is associated with coral survival in a changing climate.

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.

Unified methods in collecting, preserving, and archiving coral bleaching and restoration specimens to increase sample utility and interdisciplinary collaboration.

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.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

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

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.

A review of coral bleaching specimen collection, preservation, and laboratory processing methods.

Under current climate warming predictions, the future of coral reefs is dire. With projected coral reef decline, it is likely that coral specimens for bleaching research will increasingly become a more limited resource in the future. By adopting a holistic approach through increased collaborations, coral bleaching scientists can maximize a specimen's investigative yield, thus reducing the need to remove more coral material from the reef. Yet to expand a specimen's utility for additional analytic methods, information on how corals are collected is essential as many methods are variably sensitive to upstream handling and processing. In an effort to identify common practices for coral collection, sacrifice, preservation, and processing in coral bleaching research, we surveyed the literature from the last 6.5 years and created and analyzed the resulting dataset of 171 publications. Since January 2014, at least 21,890 coral specimens were collected for bleaching surveys or bleaching experiments. These specimens spanned 122 species of scleractinian corals where the most frequently sampled were Acropora millepora, Pocillopora damicornis, and Stylophora pistillata. Almost 90% of studies removed fragments from the reef, 6% collected skeletal cores, and 3% collected mucus specimens. The most common methods for sacrificing specimens were snap freezing with liquid nitrogen, chemical preservation (e.g., with ethanol or nucleic acid stabilizing buffer), or airbrushing live fragments. We also characterized 37 distinct methodological pathways from collection to processing of specimens in preparation for a variety of physiological, -omic, microscopy, and imaging analyses. Interestingly, almost half of all studies used only one of six different pathways. These similarities in collection, preservation, and processing methods illustrate that archived coral specimens could be readily shared among researchers for additional analyses. In addition, our review provides a reference for future researchers who are considering which methodological pathway to select to maximize the utility of coral bleaching specimens that they collect.

Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic.

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self-sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first-generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef-building corals facing a rapidly changing environment.

Coral physiology and microbiome dynamics under combined warming and ocean acidification.

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 µatm) and treatment (29.0°C and pCO2 of 750 µatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

Microelectrode characterization of coral daytime interior pH and carbonate chemistry.

Reliably predicting how coral calcification may respond to ocean acidification and warming depends on our understanding of coral calcification mechanisms. However, the concentration and speciation of dissolved inorganic carbon (DIC) inside corals remain unclear, as only pH has been measured while a necessary second parameter to constrain carbonate chemistry has been missing. Here we report the first carbonate ion concentration ([CO3(2-)]) measurements together with pH inside corals during the light period. We observe sharp increases in [CO3(2-)] and pH from the gastric cavity to the calcifying fluid, confirming the existence of a proton (H(+)) pumping mechanism. We also show that corals can achieve a high aragonite saturation state (Ωarag) in the calcifying fluid by elevating pH while at the same time keeping [DIC] low. Such a mechanism may require less H(+)-pumping and energy for upregulating pH compared with the high [DIC] scenario and thus may allow corals to be more resistant to climate change related stressors.

Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: Understanding the unique host+symbiont response.

The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.

Annual coral bleaching and the long-term recovery capacity of coral.

Mass bleaching events are predicted to occur annually later this century. Nevertheless, it remains unknown whether corals will be able to recover between annual bleaching events. Using a combined tank and field experiment, we simulated annual bleaching by exposing three Caribbean coral species (Porites divaricata, Porites astreoides and Orbicella faveolata) to elevated temperatures for 2.5 weeks in 2 consecutive years. The impact of annual bleaching stress on chlorophyll a, energy reserves, calcification, and tissue C and N isotopes was assessed immediately after the second bleaching and after both short- and long-term recovery on the reef (1.5 and 11 months, respectively). While P. divaricata and O. faveolata were able to recover from repeat bleaching within 1 year, P. astreoides experienced cumulative damage that prevented full recovery within this time frame, suggesting that repeat bleaching had diminished its recovery capacity. Specifically, P. astreoides was not able to recover protein and carbohydrate concentrations. As energy reserves promote bleaching resistance, failure to recover from annual bleaching within 1 year will likely result in the future demise of heat-sensitive coral species.

Short-term coral bleaching is not recorded by skeletal boron isotopes.

Coral skeletal boron isotopes have been established as a proxy for seawater pH, yet it remains unclear if and how this proxy is affected by seawater temperature. Specifically, it has never been directly tested whether coral bleaching caused by high water temperatures influences coral boron isotopes. Here we report the results from a controlled bleaching experiment conducted on the Caribbean corals Porites divaricata, Porites astreoides, and Orbicella faveolata. Stable boron (δ11B), carbon (δ13C), oxygen (δ18O) isotopes, Sr/Ca, Mg/Ca, U/Ca, and Ba/Ca ratios, as well as chlorophyll a concentrations and calcification rates were measured on coral skeletal material corresponding to the period during and immediately after the elevated temperature treatment and again after 6 weeks of recovery on the reef. We show that under these conditions, coral bleaching did not affect the boron isotopic signature in any coral species tested, despite significant changes in coral physiology. This contradicts published findings from coral cores, where significant decreases in boron isotopes were interpreted as corresponding to times of known mass bleaching events. In contrast, δ13C and δ18O exhibited major enrichment corresponding to decreases in calcification rates associated with bleaching. Sr/Ca of bleached corals did not consistently record the 1.2°C difference in seawater temperature during the bleaching treatment, or alternatively show a consistent increase due to impaired photosynthesis and calcification. Mg/Ca, U/Ca, and Ba/Ca were affected by coral bleaching in some of the coral species, but the observed patterns could not be satisfactorily explained by temperature dependence or changes in coral physiology. This demonstrates that coral boron isotopes do not record short-term bleaching events, and therefore cannot be used as a proxy for past bleaching events. The robustness of coral boron isotopes to changes in coral physiology, however, suggests that reconstruction of seawater pH using boron isotopes should be uncompromised by short-term bleaching events.

The cumulative impact of annual coral bleaching can turn some coral species winners into losers.

Mass coral bleaching events caused by elevated seawater temperatures result in extensive coral loss throughout the tropics, and are projected to increase in frequency and severity. If bleaching becomes an annual event later in this century, more than 90% of coral reefs worldwide may be at risk of long-term degradation. While corals can recover from single isolated bleaching and can acclimate to recurring bleaching events that are separated by multiple years, it is currently unknown if and how they will survive and possibly acclimatize to annual coral bleaching. Here, we demonstrate for the first time that annual coral bleaching can dramatically alter thermal tolerance in Caribbean corals. We found that high coral energy reserves and changes in the dominant algal endosymbiont type (Symbiodinium spp.) facilitated rapid acclimation in Porites divaricata, whereas low energy reserves and a lack of algal phenotypic plasticity significantly increased susceptibility in Porites astreoides to bleaching the following year. Phenotypic plasticity in the dominant endosymbiont type of Orbicella faveolata did not prevent repeat bleaching, but may have facilitated rapid recovery. Thus, coral holobiont response to an isolated single bleaching event is not an accurate predictor of its response to bleaching the following year. Rather, the cumulative impact of annual coral bleaching can turn some coral species 'winners' into 'losers', and can also facilitate acclimation and turn some coral species 'losers' into 'winners'. Overall, these findings indicate that cumulative impact of annual coral bleaching could result in some species becoming increasingly susceptible to bleaching and face a long-term decline, while phenotypically plastic coral species will acclimatize and persist. Thus, annual coral bleaching and recovery could contribute to the selective loss of coral diversity as well as the overall decline of coral reefs in the Caribbean.

Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress?

Thermally induced bleaching has caused a global decline in corals and the frequency of such bleaching events will increase. Thermal bleaching severely disrupts the trophic behaviour of the coral holobiont, reducing the photosynthetically derived energy available to the coral host. In the short term this reduction in energy transfer from endosymbiotic algae results in an energy deficit for the coral host. If the bleaching event is short-lived then the coral may survive this energy deficit by depleting its lipid reserves, or by increasing heterotrophic energy acquisition. We show for the first time that the coral animal is capable of increasing the amount of heterotrophic carbon incorporated into its tissues for almost a year following bleaching. This prolonged heterotrophic compensation could be a sign of resilience or prolonged stress. If the heterotrophic compensation is in fact an acclimatization response, then this physiological response could act as a buffer from future bleaching by providing sufficient heterotrophic energy to compensate for photoautotrophic energy losses during bleaching, and potentially minimizing the effect of subsequent elevated temperature stresses. However, if the elevated incorporation of zooplankton is a sign that the effects of bleaching continue to be stressful on the holobiont, even after 11 months of recovery, then this physiological response would indicate that complete coral recovery requires more than 11 months to achieve. If coral bleaching becomes an annual global phenomenon by mid-century, then present temporal refugia will not be sufficient to allow coral colonies to recover between bleaching events and coral reefs will become increasingly less resilient to future climate change. If, however, increasing their sequestration of zooplankton-derived nutrition into their tissues over prolonged periods of time is a compensating mechanism, the impacts of annual bleaching may be reduced. Thus, some coral species may be better equipped to face repeated bleaching stress than previously thought.

Coral energy reserves and calcification in a high-CO2 world at two temperatures.

Rising atmospheric CO2 concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO2 and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO2 levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0 °C) within each pCO2 level. After one month under experimental conditions, only A. millepora decreased calcification (-53%) in response to seawater pCO2 expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO2 and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO2 and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO2 level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO2 effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO2 world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.

Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals.

Mounding corals survive bleaching events in greater numbers than branching corals. However, no study to date has determined the underlying physiological and biogeochemical trait(s) that are responsible for mounding coral holobiont resilience to bleaching. Furthermore, the potential of dissolved organic carbon (DOC) as a source of fixed carbon to bleached corals has never been determined. Here, Porites lobata corals were experimentally bleached for 23 days and then allowed to recover for 0, 1, 5, and 11 months. At each recovery interval a suite of analyses were performed to assess their recovery (photosynthesis, respiration, chlorophyll a, energy reserves, tissue biomass, calcification, δ(13)C of the skeletal, δ(13)C, and δ(15)N of the animal host and endosymbiont fractions). Furthermore, at 0 months of recovery, the assimilation of photosynthetically acquired and zooplankton-feeding acquired carbon into the animal host, endosymbiont, skeleton, and coral-mediated DOC were measured via (13)C-pulse-chase labeling. During the first month of recovery, energy reserves and tissue biomass in bleached corals were maintained despite reductions in chlorophyll a, photosynthesis, and the assimilation of photosynthetically fixed carbon. At the same time, P. lobata corals catabolized carbon acquired from zooplankton and seemed to take up DOC as a source of fixed carbon. All variables that were negatively affected by bleaching recovered within 5 to 11 months. Thus, bleaching resilience in the mounding coral P. lobata is driven by its ability to actively catabolize zooplankton-acquired carbon and seemingly utilize DOC as a significant fixed carbon source, facilitating the maintenance of energy reserves and tissue biomass. With the frequency and intensity of bleaching events expected to increase over the next century, coral diversity on future reefs may favor not only mounding morphologies but species like P. lobata, which have the ability to utilize heterotrophic sources of fixed carbon that minimize the impact of bleaching and promote fast recovery.

Long-term changes in the chlorophyll fluorescence of bleached and recovering corals from Hawaii.

Chlorophyll fluorescence has been used to predict and monitor coral bleaching over short timescales (hours to days), but long-term changes during recovery remain largely unknown. To evaluate changes in fluorescence during long-term bleaching and recovery, Porites compressa and Montipora capitata corals were experimentally bleached in tanks at 30 degrees C for 1 month, while control fragments were maintained at 27 degrees C. A pulse amplitude modulated fluorometer measured the quantum yield of photosystem II fluorescence (Fv/Fm) of the zooxanthellae each week during bleaching, and after 0, 1.5, 4 and 8 months recovery. M. capitata appeared bleached 6 days sooner than P. compressa, yet their fluorescence patterns during bleaching did not significantly differ. Changes in minimum (Fo), maximum (Fm) and variable (Fv) fluorescence throughout bleaching and recovery indicated periods of initial photoprotection followed by photodamage in both species, with P. compressa requiring less time for photosystem II (PS II) repair than M. capitata. Fv/Fm fully recovered 6.5 months earlier in P. compressa than M. capitata, suggesting that the zooxanthellae of P. compressa were more resilient to bleaching stress.

Heterotrophic plasticity and resilience in bleached corals.

Mass coral bleaching events caused by elevated seawater temperatures have resulted in extensive coral mortality throughout the tropics over the past few decades. With continued global warming, bleaching events are predicted to increase in frequency and severity, causing up to 60% coral mortality globally within the next few decades. Although some corals are able to recover and to survive bleaching, the mechanisms underlying such resilience are poorly understood. Here we show that the coral host has a significant role in recovery and resilience. Bleached and recovering Montipora capitata (branching) corals met more than 100% of their daily metabolic energy requirements by markedly increasing their feeding rates and CHAR (per cent contribution of heterotrophically acquired carbon to daily animal respiration), whereas Porites compressa (branching) and Porites lobata (mounding) corals did not. These findings suggest that coral species with high-CHAR capability during bleaching and recovery, irrespective of morphology, will be more resilient to bleaching events over the long term, could become the dominant coral species on reefs, and may help to safeguard affected reefs from potential local and global extinction.