Algal symbiont diversity in Acropora muricata from the extreme reef of Bouraké associated with resistance to coral bleaching.

Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among individual of the same species, between different species, and across localities; what causes this variability remains unresolved. Here, we tracked bleached and non-bleached colonies of Acropora muricata to see if they recovered or died following a stress event inside the semi-enclosed lagoon of Bouraké (New Caledonia), where corals are long-term acclimatized to extreme conditions of temperature, pH and dissolved oxygen, and at a nearby control reef where conditions are more benign. We describe Symbiodiniaceae community changes based on next-generation sequencing of the ITS2 marker, metabolic responses, and energetic reserve measures (12 physiological traits evaluated) during the La Niña warm and rainy summer in 2021. Widespread coral bleaching (score 1 and 2 on the coral colour health chart) was observed only in Bouraké, likely due to the combination of the high temperatures (up to 32°C) and heavy rain. All colonies (i.e., Bouraké and reference site) associated predominantly with Symbiodinaceae from the genera Cladocopium. Unbleached colonies in Bouraké had a specific ITS2-type profile (proxies for Symbiodiniaceae genotypes), while the bleached colonies in Bouraké had the same ITS2-type profile of the reef control colonies during the stress event. After four months, the few bleached colonies that survived in Bouraké (B2) acquired the same ITS2 type profiles of the unbleached colonies in Bouraké. In terms of physiological performances, all bleached corals showed metabolic depression (e.g., Pgross and Rdark). In contrast, unbleached colonies in Bouraké maintained higher metabolic rates and energetic reserves compared to control corals. Our study suggests that Acropora muricata enhanced their resistance to bleaching thanks to specific Symbiodiniaceae associations, while energetic reserves may increase their resilience after stress.

Corals adapted to extreme and fluctuating seawater pH increase calcification rates and have unique symbiont communities.

Ocean acidification (OA) is a severe threat to coral reefs mainly by reducing their calcification rate. Identifying the resilience factors of corals to decreasing seawater pH is of paramount importance to predict the survivability of coral reefs in the future. This study compared corals adapted to variable pHT (i.e., 7.23-8.06) from the semi-enclosed lagoon of Bouraké, New Caledonia, to corals adapted to more stable seawater pHT (i.e., 7.90-8.18). In a 100-day aquarium experiment, we examined the physiological response and genetic diversity of Symbiodiniaceae from three coral species (Acropora tenuis, Montipora digitata, and Porites sp.) from both sites under three stable pHNBS conditions (8.11, 7.76, 7.54) and one fluctuating pHNBS regime (between 7.56 and 8.07). Bouraké corals consistently exhibited higher growth rates than corals from the stable pH environment. Interestingly, A. tenuis from Bouraké showed the highest growth rate under the 7.76 pHNBS condition, whereas for M. digitata, and Porites sp. from Bouraké, growth was highest under the fluctuating regime and the 8.11 pHNBS conditions, respectively. While OA generally decreased coral calcification by ca. 16%, Bouraké corals showed higher growth rates than corals from the stable pH environment (21% increase for A. tenuis to 93% for M. digitata, with all pH conditions pooled). This superior performance coincided with divergent symbiont communities that were more homogenous for Bouraké corals. Corals adapted to variable pH conditions appear to have a better capacity to calcify under reduced pH compared to corals native to more stable pH condition. This response was not gained by corals from the more stable environment exposed to variable pH during the 100-day experiment, suggesting that long-term exposure to pH fluctuations and/or differences in symbiont communities benefit calcification under OA.

Sponge organic matter recycling: Reduced detritus production under extreme environmental conditions.

Sponges are a key component of coral reef ecosystems and play an important role in carbon and nutrient cycles. Many sponges are known to consume dissolved organic carbon and transform this into detritus, which moves through detrital food chains and eventually to higher trophic levels via what is known as the sponge loop. Despite the importance of this loop, little is known about how these cycles will be impacted by future environmental conditions. During two years (2018 and 2020), we measured the organic carbon, nutrient recycling, and photosynthetic activity of the massive HMA, photosymbiotic sponge Rhabdastrella globostellata at the natural laboratory of Bouraké in New Caledonia, where the physical and chemical composition of seawater regularly change according to the tide. We found that while sponges experienced acidification and low dissolved oxygen at low tide in both sampling years, a change in organic carbon recycling whereby sponges stopped producing detritus (i.e., the sponge loop) was only found when sponges also experienced higher temperature in 2020. Our findings provide new insights into how important trophic pathways may be affected by changing ocean conditions.

Corals at the edge of environmental limits: A new conceptual framework to re-define marginal and extreme coral communities.

The worldwide decline of coral reefs has renewed interest in coral communities at the edge of environmental limits because they have the potential to serve as resilience hotspots and climate change refugia, and can provide insights into how coral reefs might function in future ocean conditions. These coral communities are often referred to as marginal or extreme but few definitions exist and usage of these terms has therefore been inconsistent. This creates significant challenges for categorising these often poorly studied communities and synthesising data across locations. Furthermore, this impedes our understanding of how coral communities can persist at the edge of their environmental limits and the lessons they provide for future coral reef survival. Here, we propose that marginal and extreme coral communities are related but distinct and provide a novel conceptual framework to redefine them. Specifically, we define coral reef extremeness solely based on environmental conditions (i.e., large deviations from optimal conditions in terms of mean and/or variance) and marginality solely based on ecological criteria (i.e., altered community composition and/or ecosystem functioning). This joint but independent assessment of environmental and ecological criteria is critical to avoid common pitfalls where coral communities existing outside the presumed optimal conditions for coral reef development are automatically considered inferior to coral reefs in more traditional settings. We further evaluate the differential potential of marginal and extreme coral communities to serve as natural laboratories, resilience hotspots and climate change refugia, and discuss strategies for their conservation and management as well as priorities for future research. Our new classification framework provides an important tool to improve our understanding of how corals can persist at the edge of their environmental limits and how we can leverage this knowledge to optimise strategies for coral reef conservation, restoration and management in a rapidly changing ocean.

Phototrophic sponge productivity may not be enhanced in a high CO2 world.

Sponges are major components of benthic communities across the world and have been identified as potential "winners" on coral reefs in the face of global climate change as result of their tolerance to ocean warming and acidification (OA). Previous studies have also hypothesised that photosymbiont-containing sponges might have higher productivity under future OA conditions as a result of photosymbionts having increased access to CO2 and subsequently greater carbon production. Here we test this hypothesis for a widespread and abundant photosymbiont-containing sponge species Lamellodysidea herbacea at a CO2 seep in Papua New Guinea simulating OA conditions. We found seep sponges had relatively higher cyanobacterial abundance, chlorophyll concentrations and symbiont photosynthetic efficiency than non-seep sponges, and a three-fold higher sponge abundance at the seep site. However, while gross oxygen production was the same for seep and non-seep sponges, seep sponge dark respiration rates were higher and instantaneous photosynthesis: respiration (P:R) ratios were lower. We show that while photosymbiont containing sponges may not have increased productivity under OA, they are able to show flexibility in their relationships with microbes and offset increased metabolic costs associated with climate change associated stress.

Ingestion of Diazotrophs Makes Corals More Resistant to Heat Stress.

Over the past decade, coral bleaching events have continued to recur and intensify. During bleaching, corals expel millions of their symbionts, depriving the host from its main food source. One mechanism used by corals to resist bleaching consists in exploiting food sources other than autotrophy. Among the food sources available in the reefs, dinitrogen (N2)-fixing prokaryotes or planktonic diazotrophs (hereafter called 'PD') have the particularity to reduce atmospheric dinitrogen (N2) and release part of this nitrogen (diazotroph-derived nitrogen or DDN) in bioavailable form. Here, we submitted coral colonies of Stylophora pistillata, fed or not with planktonic diazotrophs, to a temperature stress of up to 31 ± 0.5 °C and measured their physiological responses (photosynthetic efficiency, symbiont density, and growth rates). Heat-unfed colonies died 8 days after the heat stress while heat-PD-fed corals remained alive after 10 days of heat stress. The supply of PD allowed corals to maintain minimal chlorophyll concentration and symbiont density, sustaining photosynthetic efficiency and stimulating coral growth of up to 48% compared to unfed ones. By providing an alternative source of bioavailable nitrogen and carbon, this specific planktonic diazotroph feeding may have a profound potential for coral bleaching recovery.

Rapid evolution fuels transcriptional plasticity to ocean acidification.

Ocean acidification (OA) is postulated to affect the physiology, behavior, and life-history of marine species, but potential for acclimation or adaptation to elevated pCO2 in wild populations remains largely untested. We measured brain transcriptomes of six coral reef fish species at a natural volcanic CO2  seep and an adjacent control reef in Papua New Guinea. We show that elevated pCO2 induced common molecular responses related to circadian rhythm and immune system but different magnitudes of molecular response across the six species. Notably, elevated transcriptional plasticity was associated with core circadian genes affecting the regulation of intracellular pH and neural activity in Acanthochromis polyacanthus. Gene expression patterns were reversible in this species as evidenced upon reduction of CO2 following a natural storm-event. Compared with other species, Ac. polyacanthus has a more rapid evolutionary rate and more positively selected genes in key functions under the influence of elevated CO2 , thus fueling increased transcriptional plasticity. Our study reveals the basis to variable gene expression changes across species, with some species possessing evolved molecular toolkits to cope with future OA.

pH variability at volcanic CO2 seeps regulates coral calcifying fluid chemistry.

Coral reefs are iconic ecosystems with immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification (OA). Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance in predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO2 seeps in Papua New Guinea to assess their capacity to control their calcifying fluid (CF) chemistry. Several coral species living under conditions of low mean seawater pH, but with either low or high variability in seawater pH, were examined and compared with those living in 'normal' (non-seep) ambient seawater pH. We show that when mean seawater pH is low but highly variable, corals have a greater ability to maintain constant pHcf in their CF, but this characteristic was not linked with changes in abundance. Within less variable low pH seawater, corals with limited reductions in pHcf at the seep sites compared with controls tended to be more abundant at the seep site than at the control site. However, this finding was strongly influenced by a single species (Montipora foliosa), which was able to maintain complete pHcf homeostasis. Overall, although our findings indicate that there might be an association between ecological success and greater pHcf homeostasis, further research with additional species and at more sites with differing seawater pH regimes is required to solidify inferences regarding coral ecological success under future OA.

Microbes support enhanced nitrogen requirements of coral holobionts in a high CO2 environment.

Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO2 conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfil their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO2  seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO2 conditions. Our results demonstrate for the first time that under high pCO2 conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph-derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO2 control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha-proteobacterium. Further, corals at the high CO2  site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N-rich picoplankton sources to offset their increased N requirements may be able to cope better in a high pCO2 world.

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc.

Environmentally-induced changes in fitness are mediated by direct effects on physiology and behaviour, which are tightly linked. We investigated how predicted ocean warming (OW) and acidification (OA) affect key ecological behaviours (locomotion speed and foraging success) and metabolic rate of a keystone marine mollusc, the sea hare Stylocheilus striatus, a specialist grazer of the toxic cyanobacterium Lyngbya majuscula. We acclimated sea hares to OW and/or OA across three developmental stages (metamorphic, juvenile, and adult) or as adults only, and compare these to sea hares maintained under current-day conditions. Generally, locomotion speed and time to locate food were reduced ~1.5- to 2-fold when the stressors (OW or OA) were experienced in isolation, but reduced ~3-fold when combined. Decision-making was also severely altered, with correct foraging choice nearly 40% lower under combined stressors. Metabolic rate appeared to acclimate to the stressors in isolation, but was significantly elevated under combined stressors. Overall, sea hares that developed under OW and/or OA exhibited a less severe impact, indicating beneficial phenotypic plasticity. Reduced foraging success coupled with increased metabolic demands may impact fitness in this species and highlight potentially large ecological consequences under unabated OW and OA, namely in regulating toxic cyanobacteria blooms on coral reefs.

Acclimatization of massive reef-building corals to consecutive heatwaves.

Reef-building corals typically live close to the upper limits of their thermal tolerance and even small increases in summer water temperatures can lead to bleaching and mortality. Projections of coral reef futures based on forecasts of ocean temperatures indicate that by the end of this century, corals will experience their current thermal thresholds annually, which would lead to the widespread devastation of coral reef ecosystems. Here, we use skeletal cores of long-lived Porites corals collected from 14 reefs across the northern Great Barrier Reef, the Coral Sea, and New Caledonia to evaluate changes in their sensitivity to heat stress since 1815. High-density 'stress bands'-indicative of past bleaching-first appear during a strong pre-industrial El Niño event in 1877 but become significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming. However, the proportion of cores with stress bands declines following successive bleaching events in the twenty-first century despite increasing exposure to heat stress. Our findings demonstrate an increase in the thermal tolerance of reef-building corals and offer a glimmer of hope that at least some coral species can acclimatize fast enough to keep pace with global warming.

Effects of temperature and UVR on organic matter fluxes and the metabolic activity of Acropora muricata.

Coral bleaching events are predicted to occur more frequently in the coming decades with global warming. The susceptibility of corals to bleaching during thermal stress episodes depends on many factors, including the magnitude of thermal stress and irradiance. The interactions among these two factors, and in particular with ultra-violet radiation (UVR), the most harmful component of light, are more complex than assumed, and are not yet well understood. This paper explores the individual and combined effects of temperature and UVR on the metabolism of Acropora muricata, one of the most abundant coral species worldwide. Particulate and dissolved organic matter (POM/DOM) fluxes and organic matter (OM) degradation by the mucus-associated bacteria were also monitored in all conditions. The results show that UVR exposure exacerbated the temperature-induced bleaching, but did not affect OM fluxes, which were only altered by seawater warming. Temperature increase induced a shift from POM release and DOM uptake in healthy corals to POM uptake and DOM release in stressed ones. POM uptake was linked to a significant grazing of pico- and nanoplankton particles during the incubation, to fulfil the energetic requirements of A. muricata in the absence of autotrophy. Finally, OM degradation by mucus-associated bacterial activity was unaffected by UVR exposure, but significantly increased under high temperature. Altogether, our results demonstrate that seawater warming and UVR not only affect coral physiology, but also the way corals interact with the surrounding seawater, with potential consequences for coral reef biogeochemical cycles and food webs.

Reef-building corals thrive within hot-acidified and deoxygenated waters.

Coral reefs are deteriorating under climate change as oceans continue to warm and acidify and thermal anomalies grow in frequency and intensity. In vitro experiments are widely used to forecast reef-building coral health into the future, but often fail to account for the complex ecological and biogeochemical interactions that govern reefs. Consequently, observations from coral communities under naturally occurring extremes have become central for improved predictions of future reef form and function. Here, we present a semi-enclosed lagoon system in New Caledonia characterised by diel fluctuations of hot-deoxygenated water coupled with tidally driven persistently low pH, relative to neighbouring reefs. Coral communities within the lagoon system exhibited high richness (number of species = 20) and cover (24-35% across lagoon sites). Calcification rates for key species (Acropora formosa, Acropora pulchra, Coelastrea aspera and Porites lutea) for populations from the lagoon were equivalent to, or reduced by ca. 30-40% compared to those from the reef. Enhanced coral respiration, alongside high particulate organic content of the lagoon sediment, suggests acclimatisation to this trio of temperature, oxygen and pH changes through heterotrophic plasticity. This semi-enclosed lagoon therefore provides a novel system to understand coral acclimatisation to complex climatic scenarios and may serve as a reservoir of coral populations already resistant to extreme environmental conditions.

Ocean acidification affects fish spawning but not paternity at CO2 seeps.

Fish exhibit impaired sensory function and altered behaviour at levels of ocean acidification expected to occur owing to anthropogenic carbon dioxide emissions during this century. We provide the first evidence of the effects of ocean acidification on reproductive behaviour of fish in the wild. Satellite and sneaker male ocellated wrasse (Symphodus ocellatus) compete to fertilize eggs guarded by dominant nesting males. Key mating behaviours such as dominant male courtship and nest defence did not differ between sites with ambient versus elevated CO2 concentrations. Dominant males did, however, experience significantly lower rates of pair spawning at elevated CO2 levels. Despite the higher risk of sperm competition found at elevated CO2, we also found a trend of lower satellite and sneaker male paternity at elevated CO2 Given the importance of fish for food security and ecosystem stability, this study highlights the need for targeted research into the effects of rising CO2 levels on patterns of reproduction in wild fish.

Responses of two scleractinian corals to cobalt pollution and ocean acidification.

The effects of ocean acidification alone or in combination with warming on coral metabolism have been extensively investigated, whereas none of these studies consider that most coral reefs near shore are already impacted by other natural anthropogenic inputs such as metal pollution. It is likely that projected ocean acidification levels will aggravate coral reef health. We first investigated how ocean acidification interacts with one near shore locally abundant metal on the physiology of two major reef-building corals: Stylophora pistillata and Acropora muricata. Two pH levels (pHT 8.02; pCO2 366 µatm and pHT 7.75; pCO2 1140 µatm) and two cobalt concentrations (natural, 0.03 µg L-1 and polluted, 0.2 µg L-1) were tested during five weeks in aquaria. We found that, for both species, cobalt input decreased significantly their growth rates by 28% while it stimulated their photosystem II, with higher values of rETRmax (relative Electron Transport Rate). Elevated pCO2 levels acted differently on the coral rETRmax values and did not affect their growth rates. No consistent interaction was found between pCO2 levels and cobalt concentrations. We also measured in situ the effect of higher cobalt concentrations (1.06 ± 0.16 µg L-1) on A. muricata using benthic chamber experiments. At this elevated concentration, cobalt decreased simultaneously coral growth and photosynthetic rates, indicating that the toxic threshold for this pollutant has been reached for both host cells and zooxanthellae. Our results from both aquaria and in situ experiments, suggest that these coral species are not particularly sensitive to high pCO2 conditions but they are to ecologically relevant cobalt concentrations. Our study reveals that some reefs may be yet subjected to deleterious pollution levels, and even if no interaction between pCO2 levels and cobalt concentration has been found, it is likely that coral metabolism will be weakened if they are subjected to additional threats such as temperature increase, other heavy metals, and eutrophication.

Calcification is not the Achilles' heel of cold-water corals in an acidifying ocean.

Ocean acidification is thought to be a major threat to coral reefs: laboratory evidence and CO2 seep research has shown adverse effects on many coral species, although a few are resilient. There are concerns that cold-water corals are even more vulnerable as they live in areas where aragonite saturation (Ωara ) is lower than in the tropics and is falling rapidly due to CO2 emissions. Here, we provide laboratory evidence that net (gross calcification minus dissolution) and gross calcification rates of three common cold-water corals, Caryophyllia smithii, Dendrophyllia cornigera, and Desmophyllum dianthus, are not affected by pCO2 levels expected for 2100 (pCO2  1058 µatm, Ωara 1.29), and nor are the rates of skeletal dissolution in D. dianthus. We transplanted D. dianthus to 350 m depth (pHT 8.02; pCO2  448 µatm, Ωara 2.58) and to a 3 m depth CO2 seep in oligotrophic waters (pHT 7.35; pCO2  2879 µatm, Ωara 0.76) and found that the transplants calcified at the same rates regardless of the pCO2 confirming their resilience to acidification, but at significantly lower rates than corals that were fed in aquaria. Our combination of field and laboratory evidence suggests that ocean acidification will not disrupt cold-water coral calcification although falling aragonite levels may affect other organismal physiological and/or reef community processes.

Metagenomics Reveals Planktonic Bacterial Community Shifts across a Natural CO2 Gradient in the Mediterranean Sea.

Bacterial communities at a CO2 vent (pH 6.7) were compared with those at control (pH 8.0) and transition sites (pH 7.6) using 16S rRNA metagenomics. Firmicutes and unclassified bacteria dominated across all sites, Proteobacteria, especially Gammaproteobacteria, declined, and Epsilonproteobacteria increased in the vent with an increase in Bacteroidetes at both the vent and transition sites.

Decline in coccolithophore diversity and impact on coccolith morphogenesis along a natural CO2 gradient.

A natural pH gradient caused by marine CO2 seeps off Vulcano Island (Italy) was used to assess the effects of ocean acidification on coccolithophores, which are abundant planktonic unicellular calcifiers. Such seeps are used as natural laboratories to study the effects of ocean acidification on marine ecosystems, since they cause long-term changes in seawater carbonate chemistry and pH, exposing the organisms to elevated CO2 concentrations and therefore mimicking future scenarios. Previous work at CO2 seeps has focused exclusively on benthic organisms. Here we show progressive depletion of 27 coccolithophore species, in terms of cell concentrations and diversity, along a calcite saturation gradient from Ωcalcite 6.4 to <1. Water collected close to the main CO2 seeps had the highest concentrations of malformed Emiliania huxleyi. These observations add to a growing body of evidence that ocean acidification may benefit some algae but will likely cause marine biodiversity loss, especially by impacting calcifying species, which are affected as carbonate saturation falls.

Ocean acidification impairs vermetid reef recruitment.

Vermetids form reefs in sub-tropical and warm-temperate waters that protect coasts from erosion, regulate sediment transport and accumulation, serve as carbon sinks and provide habitat for other species. The gastropods that form these reefs brood encapsulated larvae; they are threatened by rapid environmental changes since their ability to disperse is very limited. We used transplant experiments along a natural CO2 gradient to assess ocean acidification effects on the reef-building gastropod Dendropoma petraeum. We found that although D. petraeum were able to reproduce and brood at elevated levels of CO2, recruitment success was adversely affected. Long-term exposure to acidified conditions predicted for the year 2100 and beyond caused shell dissolution and a significant increase in shell Mg content. Unless CO2 emissions are reduced and conservation measures taken, our results suggest these reefs are in danger of extinction within this century, with significant ecological and socioeconomic ramifications for coastal systems.

Thermally tolerant corals have limited capacity to acclimatize to future warming.

Thermal stress affects organism performance differently depending on the ambient temperature to which they are acclimatized, which varies along latitudinal gradients. This study investigated whether differences in physiological responses to temperature are consistent with regional differences in temperature regimes for the stony coral Oculina patagonica. To resolve this question, we experimentally assessed how colonies originating from four different locations characterized by >3 °C variation in mean maximum annual temperature responded to warming from 20 to 32 °C. We assessed plasticity in symbiont identity, density, and photosynthetic properties, together with changes in host tissue biomass. Results show that, without changes in the type of symbiont hosted by coral colonies, O. patagonica has limited capacity to acclimatize to future warming. We found little evidence of variation in overall thermal tolerance, or in thermal optima, in response to spatial variation in ambient temperature. Given that the invader O. patagonica is a relatively new member of the Mediterranean coral fauna, our results also suggest that coral populations may need to remain isolated for a long period of time for thermal adaptation to potentially take place. Our study indicates that for O. patagonica, mortality associated with thermal stress manifests primarily through tissue breakdown under moderate but prolonged warming (which does not impair symbiont photosynthesis and, therefore, does not lead to bleaching). Consequently, projected global warming is likely to cause repeat incidents of partial and whole colony mortality and might drive a gradual range contraction of Mediterranean corals.