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.

Ecological succession of the sponge cryptofauna in Hawaiian reefs add new insights to detritus production by pioneering species.

Successional theory proposes that fast growing and well dispersed opportunistic species are the first to occupy available space. However, these pioneering species have relatively short life cycles and are eventually outcompeted by species that tend to be longer-lived and have lower dispersal capabilities. Using Autonomous Reef Monitoring Structures (ARMS) as standardized habitats, we examine the assembly and stages of ecological succession among sponge species with distinctive life history traits and physiologies found on cryptic coral reef habitats of Kane'ohe Bay, Hawai'i. Sponge recruitment was monitored bimonthly over 2 years on ARMS deployed within a natural coral reef habitat resembling the surrounding climax community and on ARMS placed in unestablished mesocosms receiving unfiltered seawater directly from the natural reef deployment site. Fast growing haplosclerid and calcareous sponges initially recruited to and dominated the mesocosm ARMS. In contrast, only slow growing long-lived species initially recruited to the reef ARMS, suggesting that despite available space, the stage of ecological succession in the surrounding habitat influences sponge community development in uninhabited space. Sponge composition and diversity between early summer and winter months within mesocosm ARMS shifted significantly as the initially recruited short-lived calcareous and haplosclerid species initially recruit and then died off. The particulate organic carbon contribution of dead sponge tissue from this high degree of competition-free community turnover suggests a possible new component to the sponge loop hypothesis which remains to be tested among these pioneering species. This source of detritus could be significant in early community development of young coastal habitats but less so on established coral reefs where the community is dominated by long-lived colonial sponges.

Nitric oxide production rather than oxidative stress and cell death is associated with the onset of coral bleaching in Pocillopora acuta.

Elevated seawater temperatures associated with climate change lead to coral bleaching. While the ultimate causes of bleaching are well understood, the proximate physiological mechanisms underlying the bleaching response are not as well defined. Here we measured nitric oxide synthase activity, oxidative stress, and cell death in algal symbionts (Symbiodinaceae) freshly isolated from the reef-building coral Pocillopora acuta collected in the field under natural non-bleaching conditions and from corals experimentally exposed to elevated temperatures. Nitric oxide synthase activity in the algal symbionts was >3 orders of magnitude higher than that of the host and increased dramatically with increasing temperature and time of exposure (up to 72 h), consistent with the onset of bleaching for these corals. Oxidative stress and cell death among the algal symbionts were highest in coral holobionts exposed to intermediate as opposed to maximal temperatures, suggesting that these mechanisms are not proximal triggers for bleaching in this species. Our results point to nitric oxide production by the algal symbionts, rather than symbiont dysfunction, as a more important driver of coral bleaching under acute thermal stress in this coral.

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.

Growth and survival among Hawaiian corals outplanted from tanks to an ocean nursery are driven by individual genotype and species differences rather than preconditioning to thermal stress.

The drastic decline in coral coverage has stimulated an interest in reef restoration, and various iterations of coral nurseries have been used to augment restoration strategies. Here we examine the growth of two species of Hawaiian Montipora that were maintained in mesocosms under either ambient or warmed annual bleaching conditions for two consecutive years prior to outplanting to determine whether preconditioning aided coral restoration efforts. Using coral trees to create a nearby ocean nursery, we examined whether: (1) previous ex situ mesocosm growth would mirror in situ coral tree nursery growth; and (2) thermal ex situ stress-hardening would predict future success during natural warming events in situ for corals moved from tanks to trees. For Montipora capitata, we found that variation in growth was explained primarily by genotype; growth rates in the mesocosms were similar to those in situ, irrespective of preconditioning. Variation in M. flabellata growth, however, was explained by both genotype and culture method such that an individual M. flabellata colony that grew well in the tanks did not necessarily perform as well on the coral trees. For both species, previous exposure to elevated temperatures in the mesocosms provided no benefit to either growth or survival during a warming event in the coral tree nursery compared to those grown in ambient temperatures. Overall, M. capitata performed better in the tree nursery with higher net growth, lower mortality, and was subject to less predation than M. flabellata. Our results show little benefit of the additional cost and time of stress-hardening these corals prior to outplanting because it is unlikely to aid resilience to future warming events. These results also suggest that selecting corals for restoration based on long-term genotype growth performance may be more effective for optimal outcomes but should be weighed against other factors, such as coral morphology, in situ nursery method, location, and other characteristics.

Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification.

Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (-0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity-function relationships and ecosystem responses to future climate conditions.

Abundance, size, and survival of recruits of the reef coral Pocillopora acuta under ocean warming and acidification.

Ocean warming and acidification are among the greatest threats to coral reefs. Massive coral bleaching events are becoming increasingly common and are predicted to be more severe and frequent in the near future, putting corals reefs in danger of ecological collapse. This study quantified the abundance, size, and survival of the coral Pocillopora acuta under future projections of ocean warming and acidification. Flow-through mesocosms were exposed to current and future projections of ocean warming and acidification in a factorial design for 22 months. Neither ocean warming or acidification, nor their combination, influenced the size or abundance of P. acuta recruits, but heating impacted subsequent health and survival of the recruits. During annual maximum temperatures, coral recruits in heated tanks experienced higher levels of bleaching and subsequent mortality. Results of this study indicate that P. acuta is able to recruit under projected levels of ocean warming and acidification but are susceptible to bleaching and mortality during the warmest months.

Adaptive responses and local stressor mitigation drive coral resilience in warmer, more acidic oceans.

Coral reefs have great biological and socioeconomic value, but are threatened by ocean acidification, climate change and local human impacts. The capacity for corals to adapt or acclimatize to novel environmental conditions is unknown but fundamental to projected reef futures. The coral reefs of Kane'ohe Bay, Hawai'i were devastated by anthropogenic insults from the 1930s to 1970s. These reefs experience naturally reduced pH and elevated temperature relative to many other Hawaiian reefs which are not expected to face similar conditions for decades. Despite catastrophic loss in coral cover owing to human disturbance, these reefs recovered under low pH and high temperature within 20 years after sewage input was diverted. We compare the pH and temperature tolerances of three dominant Hawaiian coral species from within Kane'ohe Bay to conspecifics from a nearby control site and show that corals from Kane'ohe are far more resistant to acidification and warming. These results show that corals can have different pH and temperature tolerances among habitats and understanding the mechanisms by which coral cover rebounded within two decades under projected future ocean conditions will be critical to management. Together these results indicate that reducing human stressors offers hope for reef resilience and effective conservation over coming decades.

High heritability of coral calcification rates and evolutionary potential under ocean acidification.

Estimates of heritability inform evolutionary potential and the likely outcome of many management actions, but such estimates remain scarce for marine organisms. Here, we report high heritability of calcification rate among the eight most dominant Hawaiian coral species under reduced pH simulating future ocean conditions. Coral colonies were sampled from up to six locations across a natural mosaic in seawater chemistry throughout Hawai'i and fragmented into clonal replicates maintained under both ambient and high pCO2 conditions. Broad sense heritability of calcification rates was high among all eight species, ranging from a low of 0.32 in Porites evermanni to a high of 0.61 in Porites compressa. The overall results were inconsistent with short-term acclimatization to the local environment or adaptation to the mean or ideal conditions. Similarly, in 'local vs. foreign' and 'home vs. away' tests there was no clear signature of local adaptation. Instead, the data are most consistent with a protected polymorphism as the mechanism which maintains differential pH tolerance within the populations. Substantial individual variation, coupled with high heritability and large population sizes, imply considerable scope for natural selection and adaptive capacity, which has major implications for evolutionary potential and management of corals in response to climate change.

Coral calcification mechanisms facilitate adaptive responses to ocean acidification.

Ocean acidification (OA) is a pressing threat to reef-building corals, but it remains poorly understood how coral calcification is inhibited by OA and whether corals could acclimatize and/or adapt to OA. Using a novel geochemical approach, we reconstructed the carbonate chemistry of the calcifying fluid in two coral species using both a pH and dissolved inorganic carbon (DIC) proxy (δ11B and B/Ca, respectively). To address the potential for adaptive responses, both species were collected from two sites spanning a natural gradient in seawater pH and temperature, and then subjected to three pHT levels (8.04, 7.88, 7.71) crossed by two temperatures (control, +1.5°C) for 14 weeks. Corals from the site with naturally lower seawater pH calcified faster and maintained growth better under simulated OA than corals from the higher-pH site. This ability was consistently linked to higher pH yet lower DIC values in the calcifying fluid, suggesting that these differences are the result of long-term acclimatization and/or local adaptation to naturally lower seawater pH. Nevertheless, all corals elevated both pH and DIC significantly over seawater values, even under OA. This implies that high pH upregulation combined with moderate levels of DIC upregulation promote resistance and adaptive responses of coral calcification to OA.

Coral-algae metabolism and diurnal changes in the CO2-carbonate system of bulk sea water.

Precise measurements were conducted in continuous flow seawater mesocosms located in full sunlight that compared metabolic response of coral, coral-macroalgae and macroalgae systems over a diurnal cycle. Irradiance controlled net photosynthesis (P net), which in turn drove net calcification (G net), and altered pH. P net exerted the dominant control on [CO3 (2-)] and aragonite saturation state (Ωarag) over the diel cycle. Dark calcification rate decreased after sunset, reaching zero near midnight followed by an increasing rate that peaked at 03:00 h. Changes in Ωarag and pH lagged behind G net throughout the daily cycle by two or more hours. The flux rate P net was the primary driver of calcification. Daytime coral metabolism rapidly removes dissolved inorganic carbon (DIC) from the bulk seawater and photosynthesis provides the energy that drives G net while increasing the bulk water pH. These relationships result in a correlation between G net and Ωarag, with Ωarag as the dependent variable. High rates of H(+) efflux continued for several hours following mid-day peak G net suggesting that corals have difficulty in shedding waste protons as described by the Proton Flux Hypothesis. DIC flux (uptake) followed P net and G net and dropped off rapidly following peak P net and peak G net indicating that corals can cope more effectively with the problem of limited DIC supply compared to the problem of eliminating H(+). Over a 24 h period the plot of total alkalinity (AT ) versus DIC as well as the plot of G net versus Ωarag revealed a circular hysteresis pattern over the diel cycle in the coral and coral-algae mesocosms, but not the macroalgae mesocosm. Presence of macroalgae did not change G net of the corals, but altered the relationship between Ωarag and G net. Predictive models of how future global changes will effect coral growth that are based on oceanic Ωarag must include the influence of future localized P net on G net and changes in rate of reef carbonate dissolution. The correlation between Ωarag and G net over the diel cycle is simply the response of the CO2-carbonate system to increased pH as photosynthesis shifts the equilibria and increases the [CO3 (2-)] relative to the other DIC components of [HCO3 (-)] and [CO2]. Therefore Ωarag closely tracked pH as an effect of changes in P net, which also drove changes in G net. Measurements of DIC flux and H(+) flux are far more useful than concentrations in describing coral metabolism dynamics. Coral reefs are systems that exist in constant disequilibrium with the water column.