Heat stress in symbiotic dinoflagellates: Implications on oxidative stress and cellular changes.

Global warming has been shown to harmfully affect symbiosis between Symbiodiniaceae and other marine invertebrates. When symbiotic dinoflagellates (the genus Breviolum) were in vitro exposed to acute heat stress of +7 °C for a period of 5 days, the results revealed the negative impact on all physiological and other cellular parameters measured. Elevated temperatures resulted in a severe reduction in algal density of up to 9.5-fold, as well as pigment concentrations, indicating the status of the physiological stress and early signs of photo-bleaching. Reactive oxygen species (ROS) were increased in all heated dinoflagellate cells, while the antioxidant-reduced glutathione levels initially dropped on day one but increased under prolonged temperature stress. The cell viability parameters were reduced by 97 % over the heating period, with an increased proportion of apoptotic and necrotic cells. Autofluorescence (AF) for Cy5-PE 660-20 was reduced from 1.7-fold at day 1 to up to 50-fold drop at the end of heating time, indicating that the AF changes were highly sensitive to heat stress and that it could be an extremely sensitive tool for assessing the functionality of algal photosynthetic machinery. The addition of the drug 5-AZA-2'-deoxycytidine (5-AZA), which inhibits DNA methylation processes, was assessed in parallel and contributed to some alterations in algal cellular stress response. The presence of drug 5-AZA combined with the temperature stress had an additional impact on Symbiodiniaceae density and cell complexity, including the AF levels. These variations in cellular stress response under heat stress and compromised DNA methylation conditions may indicate the importance of this epigenetic mechanism for symbiotic dinoflagellate thermal tolerance adaptability over a longer period, which needs further exploration. Consequently, the increased ROS levels and changes in AF signals reported during ongoing heat stress in dinoflagellate cells could be used as early stress biomarkers in these microalgae and potentially other photosynthetic species.

Coral reefs in peril in a record-breaking year.

Climate change and its impacts on coral reefs have reached unchartered territory.

Marine heatwaves modulate the genotypic and physiological responses of reef-building corals to subsequent heat stress.

Back-to-back marine heatwaves in 2016 and 2017 resulted in severe coral bleaching and mortality across the Great Barrier Reef (GBR). Encouragingly, some corals that survived these events exhibit increased bleaching resistance and may represent thermally tolerant populations that can better cope with ocean warming. Using the GBR as a natural laboratory, we investigated whether a history of minimal (Heron Island) or severe (Lizard Island) coral bleaching in 2016 and 2017 equates to stress tolerance in a successive heatwave (2020). We examined the genetic diversity, physiological performance, and trophic plasticity of juvenile (<10 cm) and adult (>25 cm) corals of two common genera (Pocillopora and Stylophora). Despite enduring greater cumulative heat stress (6.3°C week-1 vs. 5.6°C week-1), corals that experienced the third marine heatwave in 5 years (Lizard) exhibited twice as high survival and visual bleaching thresholds compared to corals that had not experienced significant bleaching in >10 years (Heron). Surprisingly, only one shared host-Symbiodiniaceae association was uncovered between locations (Stylophora pistillata-Cladocopium "C8 group") and there was no genetic overlap in Pocillopora-Cladocopium partnerships, suggesting turnover in species composition from recent marine heatwaves. Corals within the species complex Pocillopora that survived the 2016 and 2017 marine heatwaves at Lizard Island were the most resilient, exhibiting three times greater calcification rates than conspecifics at Heron Island. Further, surviving corals (Lizard) had distinct isotopic niches, lower host carbon, and greater host protein, while conspecifics that had not experienced recent bleaching (Heron) had two times greater symbiont carbon content, suggesting divergent trophic strategies that influenced survival (i.e., greater reliance on heterotrophy vs. symbiont autotrophy, respectively). Ultimately, while corals may experience less bleaching and survive repeated thermal stress events, species-specific trade-offs do occur, leaving open many questions related to the long-term health and recovery of coral reef ecosystems in the face of intensifying marine heatwaves.

Systematic review of clinical practice guidelines for acne vulgaris published between January 2017 and July 2021.

Background: Acne is very common, can cause considerable negative impact on quality of life and there is increasing concern over the use of long courses of oral antibiotics for this condition. Objectives: (1) To critically appraise reporting in acne guidelines and compare this with previous systematic review of acne guidelines. (2) Examine acne treatment guidance on pre-specified acne treatments of interest and compare between acne guidelines. Methods: Searches for new or updated guidelines were carried out in MEDLINE, Embase, Google Scholar, LILACS from 1 January 2017 to 31 July 2021, supplemented by searching a guideline-specific depository and checking for updates to guidelines included in previous review. We included guidelines, consensus statements or care protocols on the medical treatment of acne vulgaris in adults and/or children and excluded those that focused on a single intervention or subgroup of acne, regional adaptations of guidelines or guidelines included in previous review. AGREE II checklist was applied to critically appraise reporting of guidelines. Results were synthesised narratively. Results: Of 807 abstracts identified nine guidelines were identified that were eligible for inclusion. All guidelines had AGREE II scores above average in at least one domain and reporting was substantially improved compared to the systematic review of acne carried out 5 years previously. There was consensus between guidelines on the key role of topical treatments as first-line acne treatment and most recommended continuing topical treatments as maintenance therapy. There was considerable variation between guidelines on classification of severity, indications for commencing oral antibiotics and on maximum duration of oral antibiotics. However, there was consensus on the need for co-prescription of a non-antibiotic topical treatment when using oral antibiotics. There were notable differences on recommendations regarding provision of information for patients on how to use topical treatments or how to mitigate against side effects. Conclusions: Substantial differences in classification of acne severity hampered comparisons between guidelines. Although development and reporting of guidelines has improved over the past 5 years, differences in key recommendations remain, possibly reflecting uncertainties in the underlying evidence base. Differences between guidelines could have substantial implications for prevalence of antibiotic prescribing for acne.

Fine-scale heterogeneity reveals disproportionate thermal stress and coral mortality in thermally variable reef habitats during a marine heatwave.

Increasing ocean temperatures threaten coral reefs globally, but corals residing in habitats that experience high thermal variability are thought to be better adapted to survive climate-induced heat stress. Here, we used long-term ecological observations and in situ temperature data from Heron Island, southern Great Barrier Reef to investigate how temperature dynamics within various thermally variable vs. thermally stable reef habitats change during a marine heatwave and the resulting consequences for coral community survival. During the heatwave, thermally variable habitats experienced larger surges in daily mean and maxima temperatures compared to stable sites, including extreme hourly incursions up to 36.5 °C. The disproportionate increase in heat stress in variable habitats corresponded with greater subsequent declines in hard coral cover, including a three-times greater decline within the thermally variable Reef Flat (70%) and Deep Lagoon (83%) than within thermally stable habitats along sheltered and exposed areas of the reef slope (0.3-19%). Interestingly, the thermally variable Reef Crest experienced comparatively small declines (26%), avoiding the most severe tidal ponding and resultant heat stress likely due to proximity to the open ocean equating to lower seawater residence times, greater mixing, and/or increased flow. These results highlight that variable thermal regimes, and any acclimatization or adaptation to elevated temperatures that may lead to, do not necessarily equate to protection against bleaching and mortality during marine heatwaves. Instead, thermally stable habitats that have greater seawater exchange with the open ocean may offer the most protection to corals during the severe marine heatwaves that accompany a changing climate. Supplementary Information: The online version contains supplementary material available at 10.1007/s00338-022-02328-6.

Environmental memory gained from exposure to extreme pCO2 variability promotes coral cellular acid-base homeostasis.

Ocean acidification is a growing threat to coral growth and the accretion of coral reef ecosystems. Corals inhabiting environments that already endure extreme diel pCO2 fluctuations, however, may represent acidification-resilient populations capable of persisting on future reefs. Here, we examined the impact of pCO2 variability on the reef-building coral Pocillopora damicornis originating from reefs with contrasting environmental histories (variable reef flat versus stable reef slope) following reciprocal exposure to stable (218 ± 9) or variable (911 ± 31) diel pCO2 amplitude (µtam) in aquaria over eight weeks. Endosymbiont density, photosynthesis and net calcification rates differed between origins but not treatment, whereas primary calcification (extension) was affected by both origin and acclimatization to novel pCO2 conditions. At the cellular level, corals from the variable reef flat exhibited less intracellular pH (pHi) acidosis and faster pHi recovery rates in response to experimental acidification stress (pH 7.40) than corals originating from the stable reef slope, suggesting environmental memory gained from lifelong exposure to pCO2 variability led to an improved ability to regulate acid-base homeostasis. These results highlight the role of cellular processes in maintaining acidification resilience and suggest that prior exposure to pCO2 variability may promote more acidification-resilient coral populations in a changing climate.

Colonies of Acropora formosa with greater survival potential have reduced calcification rates.

Coral reefs are facing increasingly devasting impacts from ocean warming and acidification due to anthropogenic climate change. In addition to reducing greenhouse gas emissions, potential solutions have focused either on reducing light stress during heating, or on the potential for identifying or engineering "super corals". A large subset of these studies, however, have tended to focus primarily on the bleaching response of corals, and assume erroneously that corals that bleach earlier in a thermal event die first. Here, we explore how survival, observable bleaching, coral skeletal growth (as branch extension and densification), and coral tissue growth (protein and lipid concentrations) varies for conspecifics collected from distinctive reef zones at Heron Island on the Southern Great Barrier Reef. A reciprocal transplantation experiment was undertaken using the dominant reef building coral (Acropora formosa) between the highly variable reef flat and the less variable reef slope environments. Coral colonies originating from the reef flat had higher rates of survival and amassed greater protein densities but calcified at reduced rates compared to conspecifics originating from the reef slope. The energetics of both populations however potentially benefited from greater light intensity present in the shallows. Reef flat origin corals moved to the lower light intensity of the reef slope reduced protein density and calcification rates. For A. formosa, genetic differences, or long-term entrainment to a highly variable environment, appeared to promote coral survival at the expense of calcification. The response decouples coral survival from carbonate coral reef resilience, a response that was further exacerbated by reductions in irradiance. As we begin to discuss interventions necessitated by the CO2 that has already been released into the atmosphere, we need to prioritise our focus on the properties that maintain valuable carbonate ecosystems. Rapid and dense calcification by corals such as branching Acropora is essential to the ability of carbonate coral reefs to rebound following disturbance events and maintain 3D structure but may be the first property that is sacrificed to enable coral genet survival under stress.

Asymmetric physiological response of a reef-building coral to pulsed versus continuous addition of inorganic nutrients.

Coral reefs, especially those located near-shore, are increasingly exposed to anthropogenic, eutrophic conditions that are often chronic. Yet, corals under unperturbed conditions may frequently receive natural and usually temporary nutrient supplementation through biological sources such as fishes. We compared physiological parameters indicative of long- and short-term coral health (day and night calcification, fragment surface area, productivity, energy reserves, and tissue stoichiometry) under continuous and temporary nutrient enrichment. The symbiotic coral Acropora intermedia was grown for 7 weeks under continuously elevated (press) levels of ammonium (14 µmol L-1) and phosphate (10 µmol L-1) as separate and combined treatments, to discern the individual and interactive nutrient effects. Another treatment exposed A. intermedia twice-daily to an ammonium and phosphate pulse of the same concentrations as the press treatments to simulate natural biotic supplementation. Press exposure to elevated ammonium or phosphate produced mixed effects on physiological responses, with little interaction between the nutrients in the combined treatment. Overall, corals under press exposure transitioned resources away from calcification. However, exposure to nutrient pulses often enhanced physiological responses. Our findings indicate that while continuous nutrient enrichment may pose a threat to coral health, episodic nutrient pulses that resemble natural nutrient supplementation may significantly benefit coral health and physiology.

Morphological stasis masks ecologically divergent coral species on tropical reefs.

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging "common garden" conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

A contemporary baseline record of the world's coral reefs.

Addressing the global decline of coral reefs requires effective actions from managers, policymakers and society as a whole. Coral reef scientists are therefore challenged with the task of providing prompt and relevant inputs for science-based decision-making. Here, we provide a baseline dataset, covering 1300 km of tropical coral reef habitats globally, and comprised of over one million geo-referenced, high-resolution photo-quadrats analysed using artificial intelligence to automatically estimate the proportional cover of benthic components. The dataset contains information on five major reef regions, and spans 2012-2018, including surveys before and after the 2016 global bleaching event. The taxonomic resolution attained by image analysis, as well as the spatially explicit nature of the images, allow for multi-scale spatial analyses, temporal assessments (decline and recovery), and serve for supporting image recognition developments. This standardised dataset across broad geographies offers a significant contribution towards a sound baseline for advancing our understanding of coral reef ecology and thereby taking collective and informed actions to mitigate catastrophic losses in coral reefs worldwide.

High light alongside elevated PCO2 alleviates thermal depression of photosynthesis in a hard coral (Pocillopora acuta).

The absorbtion of human-emitted CO2 by the oceans (elevated PCO2 ) is projected to alter the physiological performance of coral reef organisms by perturbing seawater chemistry (i.e. ocean acidification). Simultaneously, greenhouse gas emissions are driving ocean warming and changes in irradiance (through turbidity and cloud cover), which have the potential to influence the effects of ocean acidification on coral reefs. Here, we explored whether physiological impacts of elevated PCO2  on a coral-algal symbiosis (Pocillopora acuta-Symbiodiniaceae) are mediated by light and/or temperature levels. In a 39 day experiment, elevated PCO2  (962 versus 431 µatm PCO2 ) had an interactive effect with midday light availability (400 versus 800 µmol photons m-2 s-1) and temperature (25 versus 29°C) on areal gross and net photosynthesis, for which a decline at 29°C was ameliorated under simultaneous high-PCO2  and high-light conditions. Light-enhanced dark respiration increased under elevated PCO2  and/or elevated temperature. Symbiont to host cell ratio and chlorophyll a per symbiont increased at elevated temperature, whilst symbiont areal density decreased. The ability of moderately strong light in the presence of elevated PCO2  to alleviate the temperature-induced decrease in photosynthesis suggests that higher substrate availability facilitates a greater ability for photochemical quenching, partially offsetting the impacts of high temperature on the photosynthetic apparatus. Future environmental changes that result in moderate increases in light levels could therefore assist the P. acuta holobiont to cope with the 'one-two punch' of rising temperatures in the presence of an acidifying ocean.

Paradise lost: End-of-century warming and acidification under business-as-usual emissions have severe consequences for symbiotic corals.

Despite recent efforts to curtail greenhouse gas emissions, current global emission trajectories are still following the business-as-usual representative concentration pathway (RCP) 8.5 emission pathway. The resulting ocean warming and acidification have transformative impacts on coral reef ecosystems, detrimentally affecting coral physiology and health, and these impacts are predicted to worsen in the near future. In this study, we kept fragments of the symbiotic corals Acropora intermedia (thermally sensitive) and Porites lobata (thermally tolerant) for 7 weeks under an orthogonal design of predicted end-of-century RCP8.5 conditions for temperature and pCO2 (3.5°C and 570 ppm above present-day, respectively) to unravel how temperature and acidification, individually or interactively, influence metabolic and physiological performance. Our results pinpoint thermal stress as the dominant driver of deteriorating health in both species because of its propensity to destabilize coral-dinoflagellate symbiosis (bleaching). Acidification had no influence on metabolism but had a significant negative effect on skeleton growth, particularly when photosynthesis was absent such as in bleached corals or under dark conditions. Total loss of photosynthesis after bleaching caused an exhaustion of protein and lipid stores and collapse of calcification that ultimately led to A. intermedia mortality. Despite complete loss of symbionts from its tissue, P. lobata maintained small amounts of photosynthesis and experienced a weaker decline in lipid and protein reserves that presumably contributed to higher survival of this species. Our results indicate that ocean warming and acidification under business-as-usual CO2 emission scenarios will likely extirpate thermally sensitive coral species before the end of the century, while slowing the recovery of more thermally tolerant species from increasingly severe mass coral bleaching and mortality. This could ultimately lead to the gradual disappearance of tropical coral reefs globally, and a shift on surviving reefs to only the most resilient coral species.

Seasonal shifts in the competitive ability of macroalgae influence the outcomes of coral-algal competition.

Understanding the effects of natural processes on coral-algal competition is an important step in identifying the role of macroalgae in perturbed coral reef ecosystems. However, studies investigating coral-algal interactions are often conducted in response to a disturbance, and rarely incorporate seasonal variability. Here, naturally occurring coral-algal interactions were assessed in situ four times a year over 2 years across eight sites spanning diverse benthic communities. In over 6500 recorded coral-algal interactions, cyanobacteria and turf algae were found to be the most damaging regardless of season, resulting in visible damage to coral in greater than 95% of interactions. Macroalgae that primarily compete using chemical mechanisms were found to be more damaging than those that compete using physical mechanisms (e.g. abrasion), with both groups demonstrating decreased competitive ability in summer. While crustose coralline algae were the least damaging to competing coral, during summer, it became three times more competitive. Our results demonstrate that the competitive ability of macroalgae and the outcomes of coral-algal competition can fluctuate in seasonal cycles that may be related to biomass, production of chemical defences and/or physical toughness. The results of this study have important implications for understanding the trajectory and resilience of coral reef ecosystems into the future.

Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter.

Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15N- and 13C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sponge, providing visual evidence of their capacity to process DOM through pinocytosis without mediation of resident bacteria. Subsequent enrichment of the endosymbiotic dinoflagellates also suggests sharing of host nitrogenous wastes. Our results shed light on the physiological mechanism behind the ecologically important ability of sponges to cycle DOM via the recently described sponge loop.

Evaluating coral trophic strategies using fatty acid composition and indices.

The ecological success of shallow water reef-building corals has been linked to the symbiosis between the coral host and its dinoflagellate symbionts (herein 'symbionts'). As mixotrophs, symbiotic corals depend on nutrients 1) transferred from their photosynthetic symbionts (autotrophy) and 2) acquired by host feeding on particulate organic resources (heterotrophy). However, coral species differ in the extent to which they depend on heterotrophy for nutrition and these differences are typically poorly defined. Here, a multi-tracer fatty acid approach was used to evaluate the trophic strategies of three species of common reef-building coral (Galaxea fascicularis, Pachyseris speciosa, and Pocillopora verrucosa) whose trophic strategies had previously been identified using carbon stable isotopes. The composition and various indices of fatty acids were compared to examine the relative contribution of symbiont autotrophy and host heterotrophy in coral energy acquisition. A linear discriminant analysis (LDA) was used to estimate the contribution of polyunsaturated fatty acids (PUFA) derived from various potential sources to the coral hosts. The total fatty acid composition and fatty acid indices revealed differences between the more heterotrophic (P. verrucosa) and more autotrophic (P. speciosa) coral hosts, with the coral host G. fascicularis showing overlap with the other two species and greater variability overall. For the more heterotrophic P. verrucosa, the fatty acid indices and LDA results both indicated a greater proportion of copepod-derived fatty acids compared to the other coral species. Overall, the LDA estimated that PUFA derived from particulate resources (e.g., copepods and diatoms) comprised a greater proportion of coral host PUFA in contrast to the lower proportion of symbiont-derived PUFA. These estimates provide insight into the importance of heterotrophy in coral nutrition, especially in productive reef systems. The study supports carbon stable isotope results and demonstrates the utility of fatty acid analyses for exploring the trophic strategies of reef-building corals.

Ecological changes over 90 years at Low Isles on the Great Barrier Reef.

Coral reefs are under increasing stress from local and global factors. Long-term perspectives are becoming increasingly important for understanding ecosystem responses. Here, we provide insights from a 91-year study of the Low Isles on the northern Great Barrier Reef (GBR) that begins with the pioneering Great Barrier Reef Expedition (1928-29). We show that intertidal communities have experienced major phase-shifts since 1928, with few signs of a return to the initial state. Coral communities demolished by cyclones 50 years ago and exposed to multiple stressors have yet to recover. Richness and diversity of these communities systematically declined for corals and other invertebrates. Specifically, massive corals have replaced branching corals, and soft corals have become much more numerous. The long-term perspective of this study illustrates the importance of considering multiple factors in reef decline, and potential recovery, of coral reefs, and the importance of tracking changes in community structure as well as coral abundance over long periods.

Living coral tissue slows skeletal dissolution related to ocean acidification.

Climate change is causing major changes to marine ecosystems globally, with ocean acidification of particular concern for coral reefs. Using a 200 d in situ carbon dioxide enrichment study on Heron Island, Australia, we simulated future ocean acidification conditions, and found reduced pH led to a drastic decline in net calcification of living corals to no net growth, and accelerated disintegration of dead corals. Net calcification declined more severely than in previous studies due to exposure to the natural community of bioeroding organisms in this in situ study and to a longer experimental duration. Our data suggest that reef flat corals reach net dissolution at an aragonite saturation state (ΩAR) of 2.3 (95% confidence interval: 1.8-2.8) with 100% living coral cover and at ΩAR > 3.5 with 30% living coral cover. This model suggests that areas of the reef with relatively low coral mortality, where living coral cover is high, are likely to be resistant to carbon dioxide-induced reef dissolution.

Bleaching and mortality of a photosymbiotic bioeroding sponge under future carbon dioxide emission scenarios.

The bioeroding sponge Cliona orientalis is photosymbiotic with dinoflagellates of the genus Symbiodinium and is pervasive on the Great Barrier Reef. We investigated how C. orientalis responded to past and future ocean conditions in a simulated community setting. The experiment lasted over an Austral summer under four carbon dioxide emission scenarios: a pre-industrial scenario (PI), a present-day scenario (PD; control), and two future scenarios of combined ocean acidification and ocean warming, i.e., B1 (intermediate) and A1FI (extreme). The four scenarios also simulated natural variability of carbon dioxide partial pressure and temperature in seawater. Responses of C. orientalis generally remained similar between the PI and PD treatments. C. orientalis under B1 displayed a dramatic increase in lateral tissue extension, but bleached and displayed reduced rates of respiration and photosynthesis. Some B1 sponge replicates died by the end of the experiment. Under A1FI, strong bleaching and subsequent mortality of all C. orientalis replicates occurred at an early stage of the experiment. Mortality arrested bioerosion by C. orientalis under B1 and A1FI. Overall, the absolute amount of calcium carbonate eroded by C. orientalis under B1 or A1FI was similar to that under PI or PD at the end of the experiment. Although bioerosion rates were raised by short-term experimental acidification in previous studies, our findings from the photosymbiotic C. orientalis imply that the effects of bioerosion on reef carbonate budgets may only be temporary if the bioeroders cannot survive long-term in the future oceans.

Single-cell measurement of ammonium and bicarbonate uptake within a photosymbiotic bioeroding sponge.

Some of the most aggressive coral-excavating sponges host intracellular dinoflagellates from the genus Symbiodinium, which are hypothesized to provide the sponges with autotrophic energy that powers bioerosion. Investigations of the contribution of Symbiodinium to host metabolism and particularly inorganic nutrient recycling are complicated, however, by the presence of alternative prokaryotic candidates for this role. Here, novel methods are used to study nutrient assimilation and transfer within and between the outer-layer cells of the Indopacific bioeroding sponge Cliona orientalis. Combining stable isotope labelling, transmission electron microscopy (TEM) and nanoscale secondary ion mass spectrometry (NanoSIMS), we visualize and measure metabolic activity at the individual cell level, tracking the fate of 15N-ammonium and 13C-bicarbonate within the intact holobiont. We found strong uptake of both inorganic sources (especially 13C-bicarbonate) by Symbiodinium cells. Labelled organic nutrients were translocated from Symbiodinium to the Symbiodinium-hosting sponge cells within 6 h, and occasionally to other sponge cells within 3 days. By contrast, prokaryotic symbionts were not observed to participate in inorganic nutrient assimilation in the outer layers of the sponge. Our findings strongly support the metabolic interaction between the sponge and dinoflagellates, shedding light on the ecological advantages and adaptive capacity of photosymbiotic bioeroding sponges in oligotrophic marine habitats.

Altered sediment biota and lagoon habitat carbonate dynamics due to sea cucumber bioturbation in a high-pCO2 environment.

The effects of global change on biological systems and functioning are already measurable, but how ecological interactions are being altered is poorly understood. Ecosystem resilience is strengthened by ecological functionality, which depends on trophic interactions between key species and resilience generated through biogenic buffering. Climate-driven alterations to coral reef metabolism, structural complexity and biodiversity are well documented, but the feedbacks between ocean change and trophic interactions of non-coral invertebrates are understudied. Sea cucumbers, some of the largest benthic inhabitants of tropical lagoon systems, can influence diel changes in reef carbonate dynamics. Whether they have the potential to exacerbate or buffer ocean acidification over diel cycles depends on their relative production of total alkalinity (AT ) through the dissolution of ingested calcium carbonate (CaCO3 ) sediments and release of dissolved inorganic carbon (CT ) through respiration and trophic interactions. In this study, the potential for the sea cucumber, Stichopus herrmanni, a bêche-de-mer (fished) species listed as vulnerable to extinction, to buffer the impacts of ocean acidification on reef carbonate chemistry was investigated in lagoon sediment mesocosms across diel cycles. Stichopus herrmanni directly reduced the abundance of meiofauna and benthic primary producers through its deposit-feeding activity under present-day and near-future pCO2 . These changes in benthic community structure, as well as AT (sediment dissolution) and CT (respiration) production by S. herrmanni, played a significant role in modifying seawater carbonate dynamics night and day. This previously unappreciated role of tropical sea cucumbers, in support of ecosystem resilience in the face of global change, is an important consideration with respect to the bêche-de-mer trade to ensure sea cucumber populations are sustained in a future ocean.