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The gut microbiome of herbivorous animals consists of organisms that efficiently digest the structural carbohydrates of ingested plant material. Green turtles (Chelonia mydas) provide an interesting model of change in these microbial communities because they undergo a pronounced shift from a surface-pelagic distribution and omnivorous diet to a neritic distribution and herbivorous diet. As an alternative to direct sampling of the gut, we investigated the cloacal microbiomes of juvenile green turtles before and after recruitment to neritic waters to observe any changes in their microbial community structure. Cloacal swabs were taken from individual turtles for analysis of the 16S rRNA gene sequences using Illumina sequencing. One fecal sample was also obtained, allowing for a preliminary comparison with the bacterial community of the cloaca. We found significant variation in the juvenile green turtle bacterial communities between pelagic and neritic habitats, suggesting that environmental and dietary factors support different bacterial communities in green turtles from these habitats. This is the first study to characterize the cloacal microbiome of green turtles in the context of their ontogenetic shifts, which could provide valuable insight into the origins of their gut bacteria and how the microbial community supports their shift to herbivory.

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.

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.

For over three decades, scientists have conducted heat-stress experiments to predict how coral will respond to ocean warming due to global climate change. However, there are often conflicting results in the literature that are difficult to resolve, which we hypothesize are a result of unintended biases, variation in experimental design, and underreporting of critical methodological information. Here, we reviewed 255 coral heat-stress experiments to (1) document where and when they were conducted and on which species, (2) assess variability in experimental design, and (3) quantify the diversity of response variables measured. First, we found that two-thirds of studies were conducted in only three countries, three coral species were more heavily studied than others, and only 4% of studies focused on earlier life stages. Second, slightly more than half of all heat-stress exposures were less than 8 d in duration, only 17% of experiments fed corals, and experimental conditions varied widely, including the level and rate of temperature increase, light intensity, number of genets used, and the length of acclimation period. In addition, 95%, 55%, and > 35% of studies did not report tank flow conditions, light–dark cycle used, or the date of the experiment, respectively. Finally, we found that 21% of experiments did not measure any bleaching phenotype traits, 77% did not identify the Symbiodiniaceae endosymbiont, and the contribution of the coral host in the physiological response to heat-stress was often not investigated. This review highlights geographic, taxonomic, and heat-stress duration biases in our understanding of coral bleaching, and large variability in the reporting and design of heat-stress experiments that could account for some of the discrepancies in the literature. Development of some best practice recommendations for coral bleaching experiments could improve cross-studies comparisons and increase the efficiency of coral bleaching research at a time when it is needed most.

The resistance of corals to a changing climate has been linked to physiological parameters including heterotrophic capacity and energy reserves. Recently, the potential flexibility and diversity of coral-associated microbial communities have also been related to coral health and resistance to environmental stress. This study uses the island of O‘ahu in Hawai‘i, USA, as a natural laboratory to explore variability in the microbial community composition of four coral species (Porites compressa, Porites lobata, Pocillopora acuta, and Pocillopora meandrina) across a gradient of natural ocean conditions. In addition, we assessed potential relationships between the composition of coral-associated microbial communities with coral physiology. We found that microbial community composition differed among all coral species, as well as among several of the collection sites within species. Microbial community assembly appeared to be governed by a combination of deterministic and stochastic processes, and the composition of these communities was more often related to measurements of coral physiology than environmental parameters among the collection sites. Specifically, coral lipid and protein levels, two components of coral energy reserves, explained significant portions of microbial community composition in Porites lobata and Pocillopora acuta, respectively. Further, microbial community diversity decreased as the proportionate contribution of heterotrophy relative to photoautotrophy in coral tissues increased in Porites compressa and Pocillopora acuta, but the opposite was true for Porites lobata. These findings suggest that if coral heterotrophy increases with warming oceans, it could co-occur with shifts in microbial community diversity in some coral species, possibly from decreased production of photosynthates and/or changes in the nutritional makeup of the mucus layer. Overall, connections with energy reserves and heterotrophy suggest a role for coral resource use in shaping the composition of coral-associated microbial communities across a range of natural ocean conditions, a relationship that may be important as some corals acclimatize to global climate change.

To evaluate potential coral adaptive mechanisms, we investigated physiological traits (biomass, lipid, protein, chlorophyll, and isotopic proxies for trophic strategy) in eight Hawaiian corals species along an environmental gradient of significant wave height, sea surface temperature, and seawater chlorophyll a concentration around the island of O‘ahu, Hawai‘i. We used the amount of physiological variation expressed in corals, and the proportion of this variation that could be explained by environmental variables, to construct hypotheses about the relative capacity for each species to adapt or acclimatize to differing conditions. Genus-level analyses indicated that Montipora and Pocillopora phenotypes are influenced more strongly by the environment than Porites corals. Species-level analyses revealed that Montipora capitata and Pocillopora acuta have the widest physiological niche boundaries, whereas Porites evermanni and Pocillopora meandrina are more physiologically restricted. Correlations between individual traits and the environmental gradient provided insight into potential adaptive mechanisms employed by each species that allow them to persist in reefs such as those within Kāne’ohe Bay, where water flow is lowest, and temperature, acidity, and nutrient concentrations are highest relative to other reefs around O‘ahu. Potential adaptive mechanisms included (a) increased surface-area-to-volume ratios to facilitate higher material flux across the diffusive boundary layer and/or to maximize light harvesting (M. capitata and P. acuta), (b) strategic investment of metabolic energy toward energy reserves (Montipora and Pocillopora), (c) changes in protein management likely via differential expression and function (Porites), and d) increased chlorophyll concentration per Symbiodiniaceae cell to maximize photosynthesis (Porites compressa). Comparison of our results with established patterns in the relative abundance of these species around O‘ahu suggests that species with wide physiological niche boundaries like M. capitata and M. flabellata might be expected to do better under predicted future ocean conditions and outcompete species such as P. evermanni and P. meandrina, making them potential candidates for coral conservation efforts.

This erratum is published as reference list of this manuscript was listed.

The gut microbiome of herbivorous animals consists of organisms that efficiently digest the structural carbohydrates of ingested plant material. Green turtles (Chelonia mydas) provide an interesting model of change in these microbial communities because they undergo a pronounced shift from a surface-pelagic distribution and omnivorous diet to a neritic distribution and herbivorous diet. As an alternative to direct sampling of the gut, we investigated the cloacal microbiomes of juvenile green turtles before and after recruitment to neritic waters to observe any changes in their microbial community structure. Cloacal swabs were taken from individual turtles for analysis of the 16S rRNA gene sequences using Illumina sequencing. One fecal sample was also obtained, allowing for a preliminary comparison with the bacterial community of the cloaca. We found significant variation in the juvenile green turtle bacterial communities between pelagic and neritic habitats, suggesting that environmental and dietary factors support different bacterial communities in green turtles from these habitats. This is the first study to characterize the cloacal microbiome of green turtles in the context of their ontogenetic shifts, which could provide valuable insight into the origins of their gut bacteria and how the microbial community supports their shift to herbivory.

Corals obtain nutrition from the photosynthetic products of their algal endosymbionts and the ingestion of organic material and zooplankton from the water column. Here, we use stable carbon (δ13C) and nitrogen (δ15N) isotopes to assess the proportionate contribution of photoautotrophic and heterotrophic sources to seven Hawaiian coral species collected from six locations around the island of O‘ahu, Hawaiʻi. We analyzed the δ13C and δ15N of coral tissues and their algal endosymbionts, as well as that of dissolved inorganic matter, particulate organic matter, and zooplankton from each site. Estimates of heterotrophic contribution varied among coral species and sites. Bayesian mixing models revealed that heterotrophic sources (particulate organic material and zooplankton) contributed the most to Pocillopora acuta and Montipora patula coral tissues at 49.3% and 48.0%, respectively, and the least to Porites lobata at 28.7%, on average. Estimates of heterotrophic contribution based on the difference between δ13C of the host and algal endosymbiont (δ13Ch–e) and isotopic niche overlap often differed, while estimates based on δ15Nh–e were slightly more aligned with the estimates produced using Bayesian mixing models. These findings suggest that the utility of each approach may vary with coral health status, regions, and coral species. Overall, we find that the mean heterotrophic contribution to Hawaiian coral tissues ranges from 20% to 50%, suggesting a variety of trophic strategies. However, these findings did not always match past direct measurements of heterotrophic feeding, indicating that heterotrophically acquired nutrition does not necessarily get incorporated into tissues but can be respired or exuded in mucus.

Global increases in atmospheric CO2 are leading to ocean warming and acidification, causing more frequent occurrences of coral bleaching, outbreaks of disease, and as a result, widespread coral mortality. Yet, some corals appear to be more tolerant of the effects of a changing climate than others. This has been attributed to several parameters of coral physiology, including greater levels of energy reserves and the ability to incorporate more heterotrophic resources, or hosting more thermally tolerant lineages of endosymbiotic algae (i.e., Symbiodiniaceae). The bacteria and archaea associated with a coral, hereafter referred to as microbial communities, are also thought to support corals by changing in response to environmental conditions, potentially providing a first line of defense as corals attempt to acclimatize. However, it is unclear whether most corals will be able to adapt or acclimatize to ocean warming and acidification expected by the end of this century. Further, little is known about potential connections between parameters of coral physiology and their associated microbial communities, and how they may affect the ability of a coral to persist in the face of global climate change. To explore this, a two-pronged approach was used: (1) a natural survey of corals around the island of O`ahu, Hawai`i, with corals collected from several sites across a gradient of ocean conditions to assess natural variability in the coral-associated microbial community composition and coral trophic strategies, and (2) a 22-month mesocosm experiment, where corals were exposed to chronic temperature and pH stress to explore potential relationships between coral-associated microbial communities and the ability of corals to persist in end-of-century ocean conditions. The natural survey revealed a diversity of microbial associates and trophic strategies among the Hawaiian corals, with the greatest differences often occurring among species rather than among locations. For the first time, the microbial community diversity was also found to correlate with the relative contribution of heterotrophy among corals, suggesting that resource use by Hawaiian corals and the structure of their microbial communities are intertwined. The 22-month mesocosm experiment revealed connections between coral-associated microbial community composition and coral mortality under predicted end-of-century ocean conditions. Specifically, two patterns were found, where Porites compressa and Porites lobata had lower mortality and their microbial communities changed in response to experimental heat and acidity stress, while Montipora capitata and Pocillopora acuta had greater mortality and their microbial communities appeared generally inflexible.Overall, the findings of this dissertation research suggest that Hawaiian corals host a diverse range of microbial communities and employ a variety of trophic strategies, such that Porites compressa and Porites lobata corals are likely to be more tolerant of stress than others and more likely to persist through this century. The coral trophic strategies were also related to the composition of the microbial communities, supporting past hypotheses of close connections between coral health and the microbiome. This was confirmed in the mesocosm experiment, as Porites compressa and Porites lobata hosted flexible microbial communities and had lower mortality in predicted end-of-century conditions than Montipora capitata and Pocillopora acuta, suggesting that those corals which are more plastic in their response will likely be more tolerant of changing ocean conditions. However, some species and populations of coral remain susceptible to the stresses expected with global climate change by the end of this century and are less likely to persist.