Mitigating the ecological collapse of coral reef ecosystems: Effective strategies to preserve coral reef ecosystems: Effective strategies to preserve coral reef ecosystems.

Global warming is decimating coral reefs. We need to implement mitigation and restoration strategies now to prevent coral reefs from disappearing altogether.

Nutrient depletion and heat stress impair the assimilation of nitrogen compounds in a scleractinian coral.

Concentrations of dissolved nitrogen in seawater can affect the resilience of the cnidarian-dinoflagellate symbiosis to climate change-induced bleaching. However, it is not yet known how the assimilation and translocation of the various nitrogen forms change during heat stress, nor how the symbiosis responds to nutrient depletion, which may occur due to increasing water stratification. Here, the tropical scleractinian coral Stylophora pistillata, in symbiosis with dinoflagellates of the genus Symbiodinium, was grown at different temperatures (26°C, 30°C and 34°C), before being placed in nutrient-replete or -depleted seawater for 24 h. The corals were then incubated with 13C-labelled sodium bicarbonate and different 15N-labelled nitrogen forms (ammonium, urea and dissolved free amino acids) to determine their assimilation rates. We found that nutrient depletion inhibited the assimilation of all nitrogen sources studied and that heat stress reduced the assimilation of ammonium and dissolved free amino acids. However, the host assimilated over 3-fold more urea at 30°C relative to 26°C. Overall, both moderate heat stress (30°C) and nutrient depletion individually decreased the total nitrogen assimilated by the symbiont by 66%, and combined, they decreased assimilation by 79%. This led to the symbiotic algae becoming nitrogen starved, with the C:N ratio increasing by over 3-fold at 34°C, potentially exacerbating the impacts of coral bleaching.

Species-Specific Response of Corals to Imbalanced Ratios of Inorganic Nutrients.

Dissolved inorganic phosphorus (DIP) is a limiting nutrient in the physiology of scleractinian corals. Anthropogenic addition of dissolved inorganic nitrogen (DIN) to coastal reefs increases the seawater DIN:DIP ratio and further increases P limitation, which is detrimental to coral health. The effects of imbalanced DIN:DIP ratios on coral physiology require further investigation in coral species other than the most studied branching corals. Here we investigated the nutrient uptake rates, elemental tissue composition and physiology of a foliose stony coral, Turbinaria reniformis, and a soft coral, Sarcophyton glaucum, exposed to four different DIN: DIP ratios (0.5:0.2, 0.5:1, 3:0.2, 3:1). The results show that T. reniformis had high uptake rates of DIN and DIP, proportional to the seawater nutrient concentrations. DIN enrichment alone led to an increase in tissue N content, shifting the tissue N:P ratio towards P limitation. However, S. glaucum had 5 times lower uptake rates and only took up DIN when the seawater was simultaneously enriched with DIP. This double uptake of N and P did not alter tissue stoichiometry. This study allows us to better understand the susceptibility of corals to changes in the DIN:DIP ratio and predict how coral species will respond under eutrophic conditions in the reef.

The Effect of Thermal Stress on the Physiology and Bacterial Communities of Two Key Mediterranean Gorgonians.

Gorgonians are important habitat-providing species in the Mediterranean Sea, but their populations are declining due to microbial diseases and repeated mass mortality events caused by summer heat waves. Elevated seawater temperatures may impact the stress tolerance and disease resistance of gorgonians and lead to disturbances in their microbiota. However, our knowledge of the biological response of the gorgonian holobiont (i.e., the host and its microbiota) to thermal stress remains limited. Here, we investigated how the holobiont of two gorgonian species (Paramuricea clavata and Eunicella cavolini) are affected throughout a 7-week thermal stress event by following both the corals' physiology and the composition of their bacterial communities. We found that P. clavata was more sensitive to elevated seawater temperatures than E. cavolini, showing a greater loss in energy reserves, reduced feeding ability, and partial mortality. This lower thermotolerance may be linked to the ∼20× lower antioxidant defense capacity in P. clavata compared with E. cavolini. In the first 4 weeks of thermal stress, we also observed minor shifts in the microbiota of both species, suggesting that the microbiota likely plays a limited role in thermal acclimation of the holobiont. However, major stochastic changes occurred later on in some colonies, which were of a transient nature in E. cavolini, but were linked to partial colony mortality in P. clavata. Overall, our results show significant, but differential, effects of thermal stress on the holobionts of both E. cavolini and P. clavata and predict potentially severe impacts on gorgonian populations under future climate scenarios. IMPORTANCE In the Mediterranean Sea, the tree-shaped gorgonian corals form large forests that provide a place to live for many species. Because of this important ecological role, it is crucial to understand how common habitat-forming gorgonians, like Eunicella cavolini and Paramuricea clavata, are affected by high seawater temperatures that are expected in the future due to climate change. We found that both species lost biomass, but P. clavata was more affected, being also unable to feed and showing signs of mortality. The microbiota of both gorgonians also changed substantively under high temperatures. Although this could be linked to partial colony mortality in P. clavata, the changes were temporary in E. cavolini. The overall higher resistance of E. cavolini may be related to its much higher antioxidant defense levels than P. clavata. Climate change may thus have severe impacts on gorgonian populations and the habitats they provide.

Desert dust deposition supplies essential bioelements to Red Sea corals.

Climate change-related increase in seawater temperature has become a leading cause of coral bleaching and mortality. However, corals from the northern Red Sea show high thermal tolerance and no recorded massive bleaching event. This specific region is frequently subjected to intense dust storms, coming from the surrounding arid deserts, which are expected to increase in frequency and intensity in the future. The aerial dust deposition supplies essential bioelements to the water column. Here, we investigated the effect of dust deposition on the physiology of a Red Sea coral, Stylophora pistillata. We measured the modifications in coral and Symbiodiniaceae metallome (cellular metal content), as well as the changes in photosynthesis and oxidative stress status of colonies exposed during few weeks to dust deposition. Our results show that 1 mg L-1 of dust supplied nanomolar amounts of nitrate and other essential bioelements, such as iron, manganese, zinc and copper, rapidly assimilated by the symbionts. At 25°C, metal bioaccumulation enhanced the chlorophyll concentration and photosynthesis of dust-exposed corals compared to control corals. These results suggest that primary production was limited by metal availability in seawater. A 5°C increase in seawater temperature enhanced iron assimilation in both control and dust-enriched corals. Temperature rise increased the photosynthesis of control corals only, dust-exposed ones having already reached maximal photosynthesis rates at 25°C. Finally, we observed a combined effect of temperature and bioelement concentration on the assimilation of molybdenum, cadmium, manganese and copper, which were in higher concentrations in symbionts of dust-exposed corals maintained at 30°C. All together these observations highlight the importance of dust deposition in the supply of essential bioelements, such as iron, to corals and its role in sustaining coral productivity in Red Sea reefs.

Symbiont regulation in Stylophora pistillata during cold stress: an acclimation mechanism against oxidative stress and severe bleaching.

Widespread coral bleaching and mortality, leading to coral reef decline, have been mainly associated with climate-change-driven increases in sea surface temperature. However, bleaching and mortality events have also been related to decreases in sea surface temperature, with cold stress events (e.g. La Niña events) being expected to increase in frequency or intensity as a result of a changing climate. Cold stress creates physiological symptoms in symbiotic reef-building corals similar to those observed when they are heat stressed, and the biochemical mechanisms underpinning cold stress in corals have been suggested to be related to an oxidative stress condition. However, up to now, this hypothesis had not been tested. This study assessed how short and long cold excursions in seawater temperature affect the physiology and biochemical processes related to oxidative stress in the reef-building coral Stylophora pistillata We provide, for the first time, direct evidence that the mechanisms underpinning cold stress and bleaching are related to the production of reactive oxygen species, and that rapid expulsion of a significant proportion of the symbiont population by the host during cooling conditions is an acclimation mechanism to avoid oxidative stress and, ultimately, severe bleaching. Furthermore, this study is one of the first to show that upwelling conditions (short-term cold stress+nutrient enrichment) can provoke a more severe oxidative stress condition in corals than cold stress alone.

Diazotrophic community and associated dinitrogen fixation within the temperate coral Oculina patagonica.

Dinitrogen (N2 ) fixing bacteria (diazotrophs) are an important source of new nitrogen in oligotrophic environments and represent stable members of the microbiome in tropical corals, while information on corals from temperate oligotrophic regions is lacking. Therefore, this study provides new insights into the diversity and activity of diazotrophs associated with the temperate coral Oculina patagonica from the Mediterranean Sea by combining metabarcoding sequencing of amplicons of both the 16S rRNA and nifH genes and 15 N2 stable isotope tracer analysis to assess diazotroph-derived nitrogen (DDN) assimilation by the coral. Results show that the diazotrophic community of O. patagonica is dominated by autotrophic bacteria (i.e. Cyanobacteria and Chlorobia). The majority of DDN was assimilated into the tissue and skeletal matrix, and DDN assimilation significantly increased in bleached corals. Thus, diazotrophs may constitute an additional nitrogen source for the coral host, when nutrient exchange with Symbiodinium is disrupted (e.g. bleaching) and external food supply is limited (e.g. oligotrophic summer season). Furthermore, we hypothesize that DDN can facilitate the fast proliferation of endolithic algae, which provide an alternative carbon source for bleached O. patagonica. Overall, O. patagonica could serve as a good model for investigating the importance of diazotrophs in coral recovery from bleaching.

Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts.

Massive coral bleaching events result in extensive coral loss throughout the world. These events are mainly caused by seawater warming, but are exacerbated by the subsequent decrease in nutrient availability in surface waters. It has therefore been shown that nitrogen, phosphorus or iron limitation contribute to the underlying conditions by which thermal stress induces coral bleaching. Generally, information on the trophic ecology of trace elements (micronutrients) in corals, and on how they modulate the coral response to thermal stress is lacking. Here, we demonstrate for the first time that heterotrophic feeding (i.e. the capture of zooplankton prey by the coral host) and thermal stress induce significant changes in micro element concentrations and isotopic signatures of the scleractinian coral Stylophora pistillata. The results obtained first reveal that coral symbionts are the major sink for the heterotrophically acquired micronutrients and accumulate manganese, magnesium and iron from the food. These metals are involved in photosynthesis and antioxidant protection. In addition, we show that fed corals can maintain high micronutrient concentrations in the host tissue during thermal stress and do not bleach, whereas unfed corals experience a significant decrease in copper, zinc, boron, calcium and magnesium in the host tissue and bleach. In addition, the significant increase in δ65 Cu and δ66 Zn signature of symbionts and host tissue at high temperature suggests that these isotopic compositions are good proxy for stress in corals. Overall, present findings highlight a new way in which coral heterotrophy and micronutrient availability contribute to coral resistance to global warming and bleaching.

Seasonal Stability in the Microbiomes of Temperate Gorgonians and the Red Coral Corallium rubrum Across the Mediterranean Sea.

Populations of key benthic habitat-forming octocoral species have declined significantly in the Mediterranean Sea due to mass mortality events caused by microbial disease outbreaks linked to high summer seawater temperatures. Recently, we showed that the microbial communities of these octocorals are relatively structured; however, our knowledge on the seasonal dynamics of these microbiomes is still limited. To investigate their seasonal stability, we collected four soft gorgonian species (Eunicella singularis, Eunicella cavolini, Eunicella verrucosa and Leptogorgia sarmentosa) and the precious red coral (Corallium rubrum) from two coastal locations with different terrestrial impact levels in the Mediterranean Sea, and used next-generation amplicon sequencing of the 16S rRNA gene. The microbiomes of all soft gorgonian species were dominated by the same 'core microbiome' bacteria belonging to the Endozoicomonas and the Cellvibrionales clade BD1-7, whereas the red coral microbiome was primarily composed of 'core' Spirochaetes, Oceanospirillales ME2 and Parcubacteria. The associations with these bacterial taxa were relatively consistent over time at each location for each octocoral species. However, differences in microbiome composition and seasonal dynamics were observed between locations and could primarily be attributed to locally variant bacteria. Overall, our data provide further evidence of the intricate symbiotic relationships that exist between Mediterranean octocorals and their associated microbes, which are ancient and highly conserved over both space and time, and suggest regulation of the microbiome composition by the host, depending on local conditions.

Computing the carbonate chemistry of the coral calcifying medium and its response to ocean acidification.

Critical to determining vulnerability or resilience of reef corals to Ocean Acidification (OA) is a clearer understanding of the extent to which corals can control carbonate chemistry in their Extracellular Calcifying Medium (ECM) where the CaCO3 skeleton is produced. Here, we employ a mathematical framework to calculate ECM aragonite saturation state (Ωarag.(ECM)) and carbonate system ion concentration using measurements of calcification rate, seawater characteristics (temperature, salinity and pH) and ECM pH (pH(ECM)). Our calculations of ECM carbonate chemistry at current-day seawater pH, indicate that Ωarag.(ECM) ranges from ∼10 to 38 (mean 20.41), i.e. about 5 to 6-fold higher than seawater. Accordingly, Dissolved Inorganic Carbon (DIC) and Total Alkalinity (TA) were calculated to be around 3 times higher in the ECM than in seawater. We also assessed the effects of acidification on ECM chemical properties of the coral Stylophora pistillata. At reduced seawater pH our calculations indicate that Ωarag.(ECM) remains almost constant. DIC(ECM) and TA(ECM) gradually increase as seawater pH declines, reaching values about 5 to 6-fold higher than in seawater, respectively for DIC and TA. We propose that these ECM characteristics buffer the effect of acidification and explain why certain corals continue to produce CaCO3 even when seawater chemistry is less favourable.

Comparative Assessment of Mediterranean Gorgonian-Associated Microbial Communities Reveals Conserved Core and Locally Variant Bacteria.

Gorgonians are key habitat-forming species of Mediterranean benthic communities, but their populations have suffered from mass mortality events linked to high summer seawater temperatures and microbial disease. However, our knowledge on the diversity, dynamics and function of gorgonian-associated microbial communities is limited. Here, we analysed the spatial variability of the microbiomes of five sympatric gorgonian species (Eunicella singularis, Eunicella cavolini, Eunicella verrucosa, Leptogorgia sarmentosa and Paramuricea clavata), collected from the Mediterranean Sea over a scale of ∼1100 km, using next-generation amplicon sequencing of the 16S rRNA gene. The microbiomes of all gorgonian species were generally dominated by members of the genus Endozoicomonas, which were at very low abundance in the surrounding seawater. Although the composition of the core microbiome (operational taxonomic units consistently present in a species) was found to be unique for each host species, significant overlap was observed. These spatially consistent associations between gorgonians and their core bacteria suggest intricate symbiotic relationships and regulation of the microbiome composition by the host. At the same time, local variations in microbiome composition were observed. Functional predictive profiling indicated that these differences could be attributed to seawater pollution. Taken together, our data indicate that gorgonian-associated microbiomes are composed of spatially conserved bacteria (core microbiome members) and locally variant members, and that local pollution may influence these local associations, potentially impacting gorgonian health.

Molecular assessment of the effect of light and heterotrophy in the scleractinian coral Stylophora pistillata.

Corals acquire nutrients via the transfer of photosynthates by their endosymbionts (autotrophy), or via zooplankton predation by the animal (heterotrophy). During stress events, corals lose their endosymbionts, and undergo starvation, unless they increase their heterotrophic capacities. Molecular mechanisms by which heterotrophy sustains metabolism in stressed corals remain elusive. Here for the first time, to the best of our knowledge, we identified specific genes expressed in heterotrophically fed and unfed colonies of the scleractinian coral Stylophora pistillata, maintained under normal and light-stress conditions. Physiological parameters and gene expression profiling demonstrated that fed corals better resisted stress than unfed ones by exhibiting less oxidative damage and protein degradation. Processes affected in light-stressed unfed corals (HLU), were related to energy and metabolite supply, carbohydrate biosynthesis, ion and nutrient transport, oxidative stress, Ca(2+) homeostasis, metabolism and calcification (carbonic anhydrases, calcium-transporting ATPase, bone morphogenetic proteins). Two genes (cp2u1 and cp1a2), which belong to the cytochrome P450 superfamily, were also upregulated 249 and 10 times, respectively, in HLU corals. In contrast, few of these processes were affected in light-stressed fed corals (HLF) because feeding supplied antioxidants and energetic molecules, which help repair oxidative damage. Altogether, these results show that heterotrophy helps prevent the cascade of metabolic problems downstream of oxidative stress.

Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas.

Endozoicomonas bacteria are emerging as extremely diverse and flexible symbionts of numerous marine hosts inhabiting oceans worldwide. Their hosts range from simple invertebrate species, such as sponges and corals, to complex vertebrates, such as fish. Although widely distributed, the functional role of Endozoicomonas within their host microenvironment is not well understood. In this review, we provide a summary of the currently recognized hosts of Endozoicomonas and their global distribution. Next, the potential functional roles of Endozoicomonas, particularly in light of recent microscopic, genomic, and genetic analyses, are discussed. These analyses suggest that Endozoicomonas typically reside in aggregates within host tissues, have a free-living stage due to their large genome sizes, show signs of host and local adaptation, participate in host-associated protein and carbohydrate transport and cycling, and harbour a high degree of genomic plasticity due to the large proportion of transposable elements residing in their genomes. This review will finish with a discussion on the methodological tools currently employed to study Endozoicomonas and host interactions and review future avenues for studying complex host-microbial symbioses.

New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4+ and NO3- supply.

Anthropogenic nutrient enrichment affects the biogeochemical cycles and nutrient stoichiometry of coastal ecosystems and is often associated with coral reef decline. However, the mechanisms by which dissolved inorganic nutrients, and especially nitrogen forms (ammonium versus nitrate) can disturb the association between corals and their symbiotic algae are subject to controversial debate. Here, we investigated the coral response to varying N : P ratios, with nitrate or ammonium as a nitrogen source. We showed significant differences in the carbon acquisition by the symbionts and its allocation within the symbiosis according to nutrient abundance, type and stoichiometry. In particular, under low phosphate concentration (0.05 µM), a 3 µM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P = 0.5 : 0.05), while these processes were significantly enhanced when nitrate was replaced by ammonium. A combined enrichment in ammonium and phosphorus (N : P = 3 : 1) induced a shift in nutrient allocation to the symbionts, at the detriment of the host. Altogether, these results shed light into the effect of nutrient enrichment on reef corals. More broadly, they improve our understanding of the consequences of nutrient loading on reef ecosystems, which is urgently required to refine risk management strategies.

Among-species variation in the energy budgets of reef-building corals: scaling from coral polyps to communities.

The symbiosis between corals and dinoflagellates promotes the rapid growth of corals in shallow tropical oceans, and the high overall productivity of coral reefs. The aim of this study was to quantify and understand variation in carbon acquisition and allocation among coral species. We measured multiple physiological traits (including symbiont density, calcification, photosynthesis and tissue composition) for the same coral fragments to facilitate direct comparisons between species (Stylophora pistillata, Pocillopora damicornis, Galaxea fascicularis, Turbinaria reniformis and Acropora sp.). Tissue protein content was highly sensitive to the availability of particulate food, increasing in fed colonies of all species. Despite among-species variation in physiology, and consistent effects of feeding on some traits, overall energy allocation to tissue compared with skeleton growth did not depend on food availability. Extrapolating from our results, estimated whole-assemblage carbon uptake varied >20-fold across different coral assemblages, but this variation was largely driven by differences in the tissue surface area of different colony morphologies, rather than by differences in surface-area-specific physiological rates. Our results caution against drawing conclusions about reef productivity based solely on physiological rates measured per unit tissue surface area. Understanding the causes and consequences of among-species variation in physiological energetics provides insight into the mechanisms that underlie the fluxes of organic matter within reefs, and between reefs and the open ocean.

Trophic dynamics of scleractinian corals: stable isotope evidence.

Reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. This symbiotic association has developed adaptations to acquire and share nutrients, which are essential for its survival and growth in nutrient-poor tropical waters. The host is thus able to prey on a wide range of organic food sources (heterotrophic nutrition) whereas the symbionts acquire most of the inorganic nutrients (autotrophic nutrition). However, nutrient fluxes between the two partners remain unclear, especially concerning heterotrophically acquired carbon and nitrogen. We combined physiological measurements and pulse-chase isotopic labeling of heterotrophic carbon and nitrogen, as well as autotrophic carbon to track nutrient fluxes in two coral species, Stylophora pistillata and Turbinaria reniformis, in symbiosis with Symbiodinium clades A, and C,D respectively. We showed a rapid acquisition, exchange and a long-term retention of heterotrophic nutrients within the symbiosis, whereas autotrophic nutrients were rapidly used to meet immediate metabolic needs. In addition, there was a higher retention of heterotrophic nitrogen compared with carbon, in agreement with the idea that tropical corals are nitrogen-limited. Finally, a coupling between auto- and heterotrophy was observed in the species S. pistillata, with a higher acquisition and retention of heterotrophic nutrients under low irradiance to compensate for a 50% reduction in autotrophic nutrient acquisition and translocation. Conversely, T. reniformis conserved an equivalent heterotrophic nutrient acquisition at both light levels because this coral species did not significantly reduce its rates of gross photosynthesis and autotrophic carbon acquisition between the two irradiances. These experiments advance the current understanding of the nutrient exchanges between the two partners of a symbiotic association, providing evidence of the complexity of the host-symbiont relationship.

Metal bioconcentration in the scleractinian coral Stylophora pistillata: investigating the role of different components of the holobiont using radiotracers.

Bioconcentration kinetics of five metals (Ag, Cd, Co, Mn, and Zn) were determined in the scleractinian coral Stylophora pistillata (entire symbiotic association vs. cultured symbionts), using radiotracer techniques. Among contrasting element behaviors observed in S. pistillata, the highest efficiency of concentration and retention was observed for Ag in the symbiotic association (CFss reaching 5000 and T b½>1 year). Predominant proportion of this metal was found associated with the skeleton whereas the other metals were mainly present in the coral tissues (including host tissues and symbionts). A 96-h exposure of cultured symbionts (isolated zooxantellae from S. pistillata) indicated that they displayed a very high potential for metal bioconcentration (higher by 1 to 3 orders of magnitude compared to the skeleton). In addition, among the five elements investigated, Ag had the highest concentration factor in the cultured symbionts. Contrasting kinetic characteristics of skeleton vs. tissues offer interesting implications for biomonitoring purposes. Indeed, the skeleton was shown to display stable metal concentrations after an exposure (long retention time) and thereby allows recording contamination event on the long term, whereas the concentrations within coral tissues rapidly increased during the exposure and dropped when non-contaminating conditions were restored, allowing information on the current (short term) contamination status. The present study confirms that the coral can be seen as a two-compartment box model for metal bioconcentration: the tissues sensus latto as a first box governing metal entrance (with a crucial role played by the symbionts) and the skeleton as a second box where metal detoxification (storage) is taking place; the first box also depurates toward the environment when non-contaminating conditions are restored.

Coral feeding on microalgae assessed with molecular trophic markers.

Herbivory in corals, especially for symbiotic species, remains controversial. To investigate the capacity of scleractinian and soft corals to capture microalgae, we conducted controlled laboratory experiments offering five algal species: the cryptophyte Rhodomonas marina, the haptophytes Isochrysis galbana and Phaeocystis globosa, and the diatoms Conticribra weissflogii and Thalassiosira pseudonana. Coral species included the symbiotic soft corals Heteroxenia fuscescens and Sinularia flexibilis, the asymbiotic scleractinian coral Tubastrea coccinea, and the symbiotic scleractinian corals Stylophora pistillata, Pavona cactus and Oculina arbuscula. Herbivory was assessed by end-point PCR amplification of algae-specific 18S rRNA gene fragments purified from coral tissue genomic DNA extracts. The ability to capture microalgae varied with coral and algal species and could not be explained by prey size or taxonomy. Herbivory was not detected in S. flexibilis and S. pistillata. P. globosa was the only algal prey that was never captured by any coral. Although predation defence mechanisms have been shown for Phaeocystis spp. against many potential predators, this study is the first to suggest this for corals. This study provides new insights into herbivory in symbiotic corals and suggests that corals may be selective herbivorous feeders.

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.

Nitrogen fixation in the mucus of Red Sea corals.

Scleractinian corals are essential constituents of tropical reef ecological diversity. They live in close association with diazotrophs [dinitrogen (N2)-fixing microbes], which can fix high rates of N2. Whether corals benefit from this extrinsic nitrogen source is still under debate. Until now, N2 fixation rates have been indirectly estimated using the acetylene reduction assay, which does not permit assessment of the amount of nitrogen incorporated into the different compartments of the coral holobiont. In the present study, the (15)N2 technique was applied for the first time on three Red Sea coral species. Significant (15)N enrichment was measured in particles released by corals to the surrounding seawater. N2 fixation rates were species specific and as high as 1.6-2 ng N day(-1) l(-1). However, no significant enrichment was measured in the symbiotic dinoflagellates or the coral host tissues, suggesting that corals do not benefit from diazotrophic N2 fixation.