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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., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

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., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

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., (© 2015. Published by The Company of Biologists Ltd.)

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., (© 2015. Published by The Company of Biologists Ltd.)

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., (© 2014. Published by The Company of Biologists Ltd.)

The physiological response of the scleractinian coral Turbinaria reniformis to ammonium enrichment (3 μmol l(-1)) was examined at 26°C as well as during a 7 day increase in temperature to 31°C (thermal stress). At 26°C, ammonium supplementation had little effect on the coral physiology. It induced a decrease in symbiont density, compensated by an increase in chlorophyll content per symbiont cell. Organic carbon release was reduced, likely because of a better utilization of the photosynthesized carbon (i.e. incorporation into proteins, kept in the coral tissue). The δ(15)N signatures of the ammonium-enriched symbionts and host tissue were also significantly decreased, by 4 and 2‰, respectively, compared with the non-enriched conditions, suggesting a significant uptake of inorganic nitrogen by the holobiont. Under thermal stress, coral colonies that were not nitrogen enriched experienced a drastic decrease in photosynthetic and photoprotective pigments (chlorophyll a, β-carotene, diadinoxanthin, diatoxanthin and peridinin), followed by a decrease in the rates of photosynthesis and calcification. Organic carbon release was not affected by this thermal stress. Conversely, nitrogen-enriched corals showed an increase in their pigment concentrations, and maintained rates of photosynthesis and calcification at ca. 60% and 100% of those measured under control conditions, respectively. However, these corals lost more organic carbon into the environment. Overall, these results indicate that inorganic nitrogen availability can be important to determining the resilience of some scleractinian coral species to thermal stress, and can have a function equivalent to that of heterotrophic feeding concerning the maintenance of coral metabolism under stress conditions.

Corals live in symbiosis with dinoflagellates of the genus Symbiodinum. These dinoflagellates translocate a large part of the photosynthetically fixed carbon to the host, which in turn uses it for its own needs. Assessing the carbon budget in coral tissue is a central question in reef studies that still vexes ecophysiologists. The amount of carbon fixed by the symbiotic association can be determined by measuring the rate of photosynthesis, but the amount of carbon translocated by the symbionts to the host and the fate of this carbon are more difficult to assess. In the present study, we propose a novel approach to calculate the budget of autotrophic carbon in the tissue of scleractinian corals, based on a new model and measurements made with the stable isotope (13)C. Colonies of the scleractinian coral Stylophora pistillata were incubated in H(13)CO (-)(3)-enriched seawater, after which the fate of (13)C was followed in the symbionts, the coral tissue and the released particulate organic carbon (i.e. mucus). Results obtained showed that after 15 min, ca. 60% of the carbon fixed was already translocated to the host, and after 48 h, this value reached 78%. However, ca. 48% of the photosynthetically fixed carbon was respired by the symbiotic association, and 28% was released as dissolved organic carbon. This is different from other coral species, where <1% of the total organic carbon released is from newly fixed carbon. Only 23% of the initially fixed carbon was retained in the symbionts and coral tissue after 48 h. Results show that our (13)C-based model could successfully trace the carbon flow from the symbionts to the host, and the photosynthetically acquired carbon lost from the symbiotic association.

Scleractinian cold-water corals (CWC) represent key taxa controlling deep-sea reef ecosystem functioning by providing structurally complex habitats to a high associated biodiversity, and by fuelling biogeochemical cycles via the release of organic matter. Nevertheless, our current knowledge on basic CWC properties, such as feeding ecology and key physiological processes (i.e. respiration, calcification and organic matter release), is still very limited. Here, we show evidence for the trophic significance of zooplankton, essentially sustaining levels of the investigated key physiological processes in the cosmopolitan CWC Desmophyllum dianthus (Esper 1794). Our results from laboratory studies reveal that withdrawal (for up to 3 weeks) of zooplankton food (i.e. Artemia salina) caused a significant decline in respiration (51%) and calcification (69%) rates compared with zooplankton-fed specimens. Likewise, organic matter release, in terms of total organic carbon (TOC), decreased significantly and eventually indicated TOC net uptake after prolonged zooplankton exclusion. In fed corals, zooplankton provided 1.6 times the daily metabolic C demand, while TOC release represented 7% of zooplankton-derived organic C. These findings highlight zooplankton as a nutritional source for D. dianthus, importantly sustaining respiratory metabolism, growth and organic matter release, with further implications for the role of CWC as deep-sea reef ecosystem engineers.

Several untested aspects of the regulation of inorganic nutrient uptake were examined using nutrient depletion experiments with the symbiotic coral Stylophora pistillata. The total inhibition of phosphate uptake in artificial seawater lacking sodium indicates the involvement of a sodium/phosphate symporter for the uptake of phosphate across host membranes. Addition of ammonium or nitrate (up to 6.0 μmol l(-1)) did not enhance saturated phosphate uptake rates, thus indicating that corals, or their symbiotic algae, were not, or not sufficiently, nitrogen limited to modify their phosphate needs. Conversely, the saturated uptake rate of ammonium increased by 2.5-fold in the presence of 3.0 μmol l(-1) of phosphate, thus indicating that the corals or their symbionts were lacking intracellular phosphate to take advantage of the inorganic nitrogen compounds dissolved in their surrounding medium. Overall, these results highlight some greater limitation in phosphate rather than in nitrogen. Finally, the rate of phosphate uptake decreased with particulate feeding of the host (organic phosphate source). Indeed, corals that were fed 1 and 3 days before the uptake experiment took up phosphate 42 and 19% slower, respectively, than corals that were fed 21 days before. This result provides additional evidence of phosphate limitation in S. pistillata. This study therefore brings new insights into the relationships between nutrients and symbiotic corals, and may provide a rapid and effective tool to investigate which nutrient is the most limiting for coral metabolism.

This study quantifies the relative contributions of autotrophy and heterotrophy to the energy budget of the temperate scleractinian species Cladocora caespitosa Linnaeus 1767. Colonies were incubated under different light and feeding regimes, and changes in carbon acquisition through photosynthesis and feeding were measured during a 2-month time period. This approach allowed us to quantify the rate at which adjustments to physiology occurred, as well as the magnitude of up- or downregulation of both feeding modes. In addition, we explored how shifts in carbon acquisition mode influenced tissue biomass (protein content), energy stores (lipid content) and colony growth (calcification). Increases in feeding capacity during prolonged exposure to darkness were correlated with decreases in photosynthetic capacity. However, feeding effort did not decrease when photosynthesis was high. In fact, feeding was maximal under high light conditions when food was not available. During starvation, colonies used their lipid stores to partially meet their metabolic requirements. Colonies kept in low light used nutrients from feeding to supplement calcification, whereas those kept at high light converted carbon from feeding into tissue biomass. This work provides the first estimates of rates of adjustment of heterotrophic feeding capacity in a Mediterranean scleractinian coral. For the study species, flexibility in carbon acquisition through heterotrophy was approximately equal to flexibility in photosynthesis both in magnitude and in the rate at which physiological adjustments occurred. The ability to alter feeding effort rapidly and strongly may explain the wide depth distribution of C. caespitosa, and its ability to survive in turbid coastal waters where light is often limited.

Increase in seawater temperature is one of the major effects of global climate change that affects marine organisms, including Cnidaria. Among them, gorgonians from the NW Mediterranean Sea, such as the species Eunicella singularis, have suffered spectacular and extensive damage. We thus investigated in a controlled laboratory experiment the response of E. singularis to a long-term increase in temperature and we took a special interest in its photosynthetic and calcification response to the stress. Two populations collected at 15 and 35 m depths were studied in order to determine whether there was a difference in sensitivity to thermal stress between living depths. Our results show: (a) that calcification and photosynthesis were impacted only when gorgonians were maintained for more than two weeks at 26 degrees C, and (b) that colonies of E. singularis living in shallow waters were less tolerant than those living in deep waters. Because E. singularis is a symbiotic species, we have also discussed the potential role of symbiosis in the thermotolerance response.

We investigated photoacclimation in the symbiotic Mediterranean coral Cladocora caespitosa by exposing it to three light levels (30, 80 and 250 micromol m(-2) s(-1)), which are in the range of those recorded for this species. The coral response to a change in both light and temperature was also assessed, by subjecting coral to two treatments corresponding to winter (14 degrees C and 30 micromol m(-2) s(-1)) and summer (23 degrees C and 250 micromol m(-2) s(-1)) conditions, as measured in the Ligurian Sea. Photosynthesis, measured using both respirometry and pulse amplitude modulated (PAM) fluorometry, revealed a linear relationship only at low light levels. At higher irradiance, relative electron transport rate (rETR) approached saturation more slowly than rates of oxygen production. At constant temperature, a change in light did not induce any change in zooxanthellae (zoox) and chlorophyll (Chla+c2) concentrations (mean 3.7 x 10(6) zoox cm(-2) and 14.1 microg cm(-2), respectively); however, chlorophyll concentrations significantly increased under low light and temperature, probably in order to maintain a sufficient level of autotrophy. Maximal gross photosynthesis (Pgmax) as well as the saturation irradiance (Ek) and the respiration rate (R) were, however, significantly higher at 250 micromol m(-2) s(-1) compared to the lower light treatments, independently of temperature conditions. Acclimation to high light appeared to be partly driven by a change in the non-photochemical quenching (NPQ) capacity of the algal cells, and to a maximal rate of photon utilization. Conversely, under low light conditions, coral polyps presented a lower Ek, but also lower respiration rates, which correspond to a decrease in the energy expenditure. This ability to acclimate to different light conditions, might allow C. caespitosa to rapidly regulate its autotrophic rate in the different light conditions encountered in its natural habitats.

This study was designed to assess the importance of dissolved free amino acids (DFAA) as a nitrogen source for the scleractinian coral Stylophora pistillata. For this purpose, experiments were performed using (15)N-enriched DFAAs, and %(15)N enrichment was measured both in animal tissue and zooxanthellae at different DFAA concentrations, incubation time and light levels. As previously observed for urea, which is another source of organic nitrogen, DFAA uptake exhibited a biphasic mode consisting of an active carrier-mediated transport for concentrations below 3 micromol l(-1) and a linear uptake for higher concentrations. The value of the carrier affinity (K(m)=1.23 micromol l(-1) DFAA) indicated good adaptation of the corals to the low levels of DFAA concentrations measured in most oligotrophic waters. DFAA uptake was also correlated with light. The DFAA contribution to the nitrogen requirements for tissue growth was compared to the contribution of ammonia, nitrate and urea, for which uptake was also measured in S. pistillata. Inorganic sources (NH(4)(+) and NO(3)(-)) contributed 75% of the daily nitrogen needs against 24% for organic sources. Taken altogether, dissolved organic and inorganic nitrogen can supply almost 100% of the nitrogen needs for tissue growth.

The Ligurian Sea (NW Mediterranean) experienced warm summers in 1998, 1999 and from 2003 to 2005. The temperature was 1-3 degrees C higher than the mean summer value (24 degrees C) and remained high over a long period. During these summers, mass-mortality events, affecting several sessile benthic species, were reported. In the present study, we tested the long-term (3-7 weeks) effect of different temperatures (20 degrees C measured in spring and autumn, 24 degrees C observed in summer, and 26 degrees C and 28 degrees C abnormal summer values) on two Mediterranean corals, Cladocora caespitosa and Oculina patagonica. Growth rate, photosynthetic efficiency (Fv/Fm), relative electron transport rate (ETR), zooxanthellae and chlorophyll (chl) contents were measured during 48 days incubation. At 20 degrees C, all parameters remained constant during the whole experiment for both species. At higher temperatures, most physiological parameters were affected by only 2-5 weeks at 24 degrees C, and were severely depressed at higher temperatures. Small replicate samples (nubbins) of O. patagonica significantly decreased their zooxanthellae and chl concentrations at all temperatures, after 2 weeks of incubation. Their Fv/Fm values, as well as their growth rates, were also gradually reduced during the incubation at all temperatures. However, only a few nubbins maintained at 28 degrees C showed signs of tissue necrosis after 34 days, and these gradually recovered tissue when temperature was returned to normal. In nubbins of C. caespitosa, chl and zooxanthellae concentrations decreased only after 34 days of incubation at 26 degrees C and 28 degrees C. At the same time, tissue necrosis was observed, explaining the loss of the symbionts. Fv/Fm was reduced only after 34 days of incubation at the different temperatures, and growth rate was first enhanced, before collapsing by 30% at 24 degrees C and by 90-100% at 26 degrees C and 28 degrees C. All samples maintained at 26 degrees C and 28 degrees C had died, due to tissue necrosis, by the end of the experiment. Results obtained suggest that O. patagonica is more able than C. caespitosa to resist high temperature conditions because of its rapid bleaching capacity. In contrast, it seems that C. caespitosa is living close to its thermal limit during the summer period; therefore, a long-term increase at 24 degrees C or above could be lethal for this coral, just as was observed in situ during the recent warm summers.

We investigated the effect of zooplankton feeding on tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Microcolonies were divided into two groups: starved corals (SC), which were not fed during the experiment, and fed corals (FC), which were abundantly fed with Artemia salina nauplii and freshly collected zooplankton. Changes in tissue growth, photosynthesis and calcification rates were measured after 3 and 8 weeks of incubation. Calcification is the deposition of both an organic matrix and a calcium carbonate layer, so we measured the effect of feeding on both these parameters, using incorporation of (14)C-aspartic acid and (45)Ca, respectively. Aspartic acid is one of the major components of the organic matrix in scleractinian corals. For both sampling times, protein concentrations were twice as high in FC than in SC (0.73 vs 0.42 mg P(-1) cm(-2) skeleton) and chlorophyll c(2) concentrations were 3-4 times higher in fed corals (2.1+/-0.3 micro g cm(-2)). Cell specific density (CSD), which corresponds to the number of algal cells inside a host cell, was also significantly higher in FC (1.416+/-0.028) than in SC (1.316+/-0.015). Fed corals therefore displayed a higher rate of photosynthesis per unit area (P(g)(max)= 570+/-60 nmol O(2) cm(-2) h(-1) and I(k)=403+/-27 micro mol photons m(-2) s(-1)). After 8 weeks, both light and dark calcification rates were twofold greater in FC (3323+/-508 and 416+/-58 nmol Ca(2+) 2 h(-1) g(-1) dry skeletal mass) compared to SC (1560+/-217 and 225+/-35 nmol Ca(2+) 2 h(-1) g(-1) dry skeletal mass, respectively, under light and dark conditions). Aspartic acid incorporation rates were also significantly higher in FC (10.44+/-0.69 and 1.36+/- 0.26%RAV 2 h(-1) g(-1) dry skeletal mass, where RAV is total radioactivity initially present in the external medium) than in SC (6.51+/-0.45 and 0.44+/-0.02%RAV 2 h(-1) g(-1) dry skeletal mass under dark and light conditions, respectively). Rates of dark aspartic acid incorporation were lower than the rates measured in the light. Our results suggest that the increase in the rates of calcification in fed corals might be induced by a feeding-stimulation of organic matrix synthesis.