Heterotrophy in marine animal forests in an era of climate change.

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

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.

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.

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.

Comment on Trophic strategy and bleaching resistance in reef-building corals.

In an era of major environmental changes, understanding corals' resistance to bleaching is as crucial as it is challenging. A promising framework for inferring corals' trophic strategies from Stable Isotope Bayesian Ellipses has been recently proposed to this end. As a contribution to this framework, we quantify a risk of bias inherent in its application and propose three alternative adjustments.

Bleaching forces coral's heterotrophy on diazotrophs and Synechococcus.

Coral reefs are threatened by global warming, which disrupts the symbiosis between corals and their photosynthetic symbionts (Symbiodiniaceae), leading to mass coral bleaching. Planktonic diazotrophs or dinitrogen (N2)-fixing prokaryotes are abundant in coral lagoon waters and could be an alternative nutrient source for corals. Here we incubated untreated and bleached coral colonies of Stylophora pistillata with a 15N2-pre-labelled natural plankton assemblage containing diazotrophs. 15N2 assimilation rates in Symbiodiniaceae cells and tissues of bleached corals were 5- and 30-fold higher, respectively, than those measured in untreated corals, demonstrating that corals incorporate more nitrogen derived from planktonic diazotrophs under bleaching conditions. Bleached corals also preferentially fed on Synechococcus, nitrogen-rich picophytoplanktonic cells, instead of Prochlorococcus and picoeukaryotes, which have a lower cellular nitrogen content. By providing an alternative source of bioavailable nitrogen, both the incorporation of nitrogen derived from planktonic diazotrophs and the ingestion of Synechococcus may have profound consequences for coral bleaching recovery, especially for the many coral reef ecosystems characterized by high abundance and activity of planktonic diazotrophs.

Evidence for mitigation of coral bleaching by manganese.

Unprecedented mass coral bleaching events due to global warming and overall seawater pollution have been observed worldwide over the last decades. Although metals are often considered as toxic substances for corals, some are essential at nanomolar concentrations for physiological processes such as photosynthesis and antioxidant defenses. This study was designed to elucidate, the individual and combined effects of nanomolar seawater enrichment in manganese (Mn) and iron (Fe), on the main physiological traits of Stylophora pistillata, maintained under normal growth and thermal stress conditions. We provide, for the first time, evidence that Mn is a key trace element for coral symbionts, enhancing cellular chlorophyll concentrations, photosynthetic efficiency and gross photosynthetic rates at ambient temperature. Our experiment also highlights the key role of Mn in increasing coral resistance to heat stress-induced bleaching. While Mn-enriched corals did not bleach and did not reduce their rates of photosynthesis and calcification, control corals experienced significant bleaching. On the contrary to Mn, Fe enrichment not only impaired calcification but induced significant bleaching. Such information is an important step towards a better understanding of the response of corals to seawater enrichment in metals. It can also explain, to some extent, species susceptibility to environmental stress.

Effects of ultraviolet radiation and nutrient level on the physiological response and organic matter release of the scleractinian coral Pocillopora damicornis following thermal stress.

Understanding which factors enhance or mitigate the impact of high temperatures on corals is crucial to predict the severity of coral bleaching worldwide. On the one hand, global warming is usually associated with high ultraviolet radiation levels (UVR), and surface water nutrient depletion due to stratification. On the other hand, eutrophication of coastal reefs increases levels of inorganic nutrients and decreases UVR, so that the effect of different combinations of these stressors on corals is unknown. In this study, we assessed the individual and crossed effects of high temperature, UVR and nutrient level on the key performance variables of the reef building coral Pocillopora damicornis. We found that seawater warming was the major stressor, which induced bleaching and impaired coral photosynthesis and calcification in all nutrient and UVR conditions. The strength of this effect however, was nutrient dependent. Corals maintained in nutrient-depleted conditions experienced the highest decrease in net photosynthesis under thermal stress, while nutrient enrichment (3 µM NO3- and 1 µM PO4+) slightly limited the negative impact of temperature through enhanced protein content, photosynthesis and respiration rates. UVR exposure had only an effect on total nitrogen release rates, which significantly decreased under normal growth conditions and tended to decrease also under thermal stress. This result suggests that increased level of UVR will lead to significant changes in the nutrient biogeochemistry of surface reef waters. Overall, our results show that environmental factors have different and interactive effects on each of the coral's physiological parameters, requiring multifactorial approaches to predict the future of coral reefs.

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.

Seabirds supply nitrogen to reef-building corals on remote Pacific islets.

Seabirds concentrate nutrients from large marine areas on their nesting islands playing an important ecological role in nutrient transfer between marine and terrestrial ecosystems. Here we investigate the role of guano on corals reefs across scales by analyzing the stable nitrogen isotopic (δ15N) values of the scleractinian coral Pocillopora damicornis on fringing reefs around two Pacific remote islets with large seabird colonies. Marine stations closest to the seabird colonies had higher nitrate + nitrite concentrations compared to more distant stations. Coral and zooxanthellae δ15N values were also higher at these sites, suggesting that guano-derived nitrogen is assimilated into corals and contributes to their nitrogen requirements. The spatial extent of guano influence was however restricted to a local scale. Our results demonstrate that seabird-derived nutrients not only spread across the terrestrial ecosystem, but also affect components of the adjacent marine ecosystem. Further studies are now needed to assess if this nutrient input has a positive or negative effect for corals. Such studies on remote islets also open fresh perspectives to understand how nutrients affect coral reefs isolated from other anthropogenic stressors.

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.

Diazotrophs: a non-negligible source of nitrogen for the tropical coral Stylophora pistillata.

Corals are mixotrophs: they are able to fix inorganic carbon through the activity of their symbiotic dinoflagellates and to gain nitrogen from predation on plankton and uptake of dissolved organic and inorganic nutrients. They also live in close association with diverse diazotrophic communities, inhabiting their skeleton, tissue and mucus layer, which are able to fix dinitrogen (N2). The quantity of fixed N2 transferred to the corals and its distribution within coral compartments as well as the quantity of nitrogen assimilated through the ingestion of planktonic diazotrophs are still unknown. Here, we quantified nitrogen assimilation via (i) N2 fixation by symbiont diazotrophs, (ii) ingestion of cultured unicellular diazotrophs and (iii) ingestion of natural planktonic diazotrophs. We estimate that the ingestion of diazotrophs provides 0.76±0.15 µg N cm(-2) h(-1), suggesting that diazotrophs represent a non-negligible source of nitrogen for scleractinian corals.

Species Specificity of Bacteria Associated to the Brown Seaweeds Lobophora (Dictyotales, Phaeophyceae) and Their Potential for Induction of Rapid Coral Bleaching in Acropora muricata.

While reef degradation is occurring worldwide, it is not uncommon to see phase shifts from coral to macroalgal dominated reefs. Numerous studies have addressed the mechanisms by which macroalgae may outcompete corals and a few recent studies highlighted the putative role of bacteria at the interface between macroalgae and corals. Some studies suggest that macroalgae may act as vectors and/or foster proliferation of microorganisms pathogenic for corals. Using a combination of high throughput sequencing, bacterial culturing, and in situ bioassays we question if the adversity of macroalgal-associated bacteria to corals is mediated by specific bacterial taxa. Using Illumina sequencing, we characterized and compared the bacterial community from two Lobophora (Dictyotales, Phaeophyceae) species. The two species presented distinctive bacterial communities. Both species shared approximately half of their OTUs, mainly the most abundant bacteria. Species-specific OTUs belong to Planctomycetes, Proteobacteria, and Bacteroidetes. In total, 16 culturable bacterial strain were isolated and identified from the Lobophora surface, consisting of 10 genera (from nine families, four classes, and three phyla), some of which are not known as, but are related to pathogens involved in coral diseases, and others are naturally associated to corals. When patches of marine agar with 24 h cultures of each of these bacteria were placed in direct contact with the branches of the scleractinian coral Acropora muricata, they caused severe bleaching after 24 h exposure. Results suggest that regardless of taxonomic affinities, increase in density of these bacteria can be adverse to corals. Nevertheless, the microbial community associated to macroalgal surface may not represent a threat to corals, because the specific bacterial screening and control exerted by the alga preventing specific bacterial proliferation.

Allelopathic interactions between the brown algal genus Lobophora (Dictyotales, Phaeophyceae) and scleractinian corals.

Allelopathy has been recently suggested as a mechanism by which macroalgae may outcompete corals in damaged reefs. Members of the brown algal genus Lobophora are commonly observed in close contact with scleractinian corals and have been considered responsible for negative effects of macroalgae to scleractinian corals. Recent field assays have suggested the potential role of chemical mediators in this interaction. We performed in situ bioassays testing the allelopathy of crude extracts and isolated compounds of several Lobophora species, naturally associated or not with corals, against four corals in New Caledonia. Our results showed that, regardless of their natural association with corals, organic extracts from species of the genus Lobophora are intrinsically capable of bleaching some coral species upon direct contact. Additionally, three new C21 polyunsaturated alcohols named lobophorenols A-C (1-3) were isolated and identified. Significant allelopathic effects against Acropora muricata were identified for these compounds. In situ observations in New Caledonia, however, indicated that while allelopathic interactions are likely to occur at the macroalgal-coral interface, Lobophora spp. rarely bleached their coral hosts. These findings are important toward our understanding of the importance of allelopathy versus other processes such as herbivory in the interaction between macroalgae and corals in reef ecosystems.

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.

Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH.

The effects of ocean acidification and elevated seawater temperature on coral calcification and photosynthesis have been extensively investigated over the last two decades, whereas they are still unknown on nutrient uptake, despite their importance for coral energetics. We therefore studied the separate and combined impacts of increases in temperature and pCO(2) on phosphate, ammonium, and nitrate uptake rates by the scleractinian coral S. pistillata. Three experiments were performed, during 10 days i) at three pH(T) conditions (8.1, 7.8, and 7.5) and normal temperature (26°C), ii) at three temperature conditions (26°, 29°C, and 33°C) and normal pH(T) (8.1), and iii) at three pH(T) conditions (8.1, 7.8, and 7.5) and elevated temperature (33°C). After 10 days of incubation, corals had not bleached, as protein, chlorophyll, and zooxanthellae contents were the same in all treatments. However, photosynthetic rates significantly decreased at 33°C, and were further reduced for the pH(T) 7.5. The photosynthetic efficiency of PSII was only decreased by elevated temperature. Nutrient uptake rates were not affected by a change in pH alone. Conversely, elevated temperature (33°C) alone induced an increase in phosphate uptake but a severe decrease in nitrate and ammonium uptake rates, even leading to a release of nitrogen into seawater. Combination of high temperature (33°C) and low pH(T) (7.5) resulted in a significant decrease in phosphate and nitrate uptake rates compared to control corals (26°C, pH(T) = 8.1). These results indicate that both inorganic nitrogen and phosphorus metabolism may be negatively affected by the cumulative effects of ocean warming and acidification.

Cadmium bioaccumulation and retention kinetics in the Chilean blue mussel Mytilus chilensis: seawater and food exposure pathways.

The Chilean blue mussel (Mytilus chilensis, Hupe 1854) represents the most important bivalve exploited along the Chilean coast and is a major food source for the Chilean population. Unfortunately, local fish and shellfish farming face severe problems as a result of bioaccumulation of toxic trace metals into shellfishes. Blue mussels collected along the Chilean coasts contain levels of Cd above the regulatory limits for human consumption. In this study, we examined the bioaccumulation, depuration and organ distribution of Cd in the M. chilensis, from 109Cd-labelled bulk seawater and from feeding with 109Cd-labelled algae. The uptake of 109Cd via seawater displayed a simple exponential kinetic model suggesting that cadmium activity tends to reach an equilibrium value of 1.838+/-0.175 ng g(-1) (mean+/-asymptotic standard error, p < 0.001) after 78+/-9 days. The depuration rate for 109Cd accumulated via seawater was slow, with only 21% of the total 109Cd accumulated in the whole mussel being eliminated after 52 days. Total elimination of Cd in mussels was adequately described by a double component kinetic model, in which the biological half-life for the long-lived component represents more than 6 months. In contrast, depuration after radiolabelled food uptake was fast, reaching only 20% of retention in 10 days. This knowledge of the long half-life of cadmium accumulated via seawater as well as the non-negligible level of cadmium accumulated into the shells is relevant to the management of Cd levels in this species and the refinement of detoxification processes in order to comply with authorized Cd levels.

Heterotrophy in tropical scleractinian corals.

The dual character of corals, that they are both auto- and heterotrophs, was recognized early in the twentieth Century. It is generally accepted that the symbiotic association between corals and their endosymbiotic algae (called zooxanthellae) is fundamental to the development of coral reefs in oligotrophic tropical oceans because zooxanthellae transfer the major part of their photosynthates to the coral host (autotrophic nutrition). However, numerous studies have confirmed that many species of corals are also active heterotrophs, ingesting organisms ranging from bacteria to mesozooplankton. Heterotrophy accounts for between 0 and 66% of the fixed carbon incorporated into coral skeletons and can meet from 15 to 35% of daily metabolic requirements in healthy corals and up to 100% in bleached corals. Apart from this carbon input, feeding is likely to be important to most scleractinian corals, since nitrogen, phosphorus, and other nutrients that cannot be supplied from photosynthesis by the coral's symbiotic algae must come from zooplankton capture, particulate matter or dissolved compounds. A recent study showed that during bleaching events some coral species, by increasing their feeding rates, are able to maintain and restore energy reserves. This review assesses the importance and effects of heterotrophy in tropical scleractinian corals. We first provide background information on the different food sources (from dissolved organic matter to meso- and macrozooplankton). We then consider the nutritional inputs of feeding. Finally, we review feeding effects on the different physiological parameters of corals (tissue composition, photosynthesis and skeletal growth).

Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata.

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.