Fanny Houlbrèque

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.

Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata

This work investigated the effect of light and feeding on tissue composition as well as on rates of photosynthesis and calcification in the zooxanthellae (zoox) scleractinian coral, Stylophora pistillata. Microcolonies were maintained at three different light levels (80, 200, 300 μmol m−2 s−1) and subjected to two feeding regimes (starved and fed) over 9 weeks. Corals were fed both natural plankton and Artemia salina nauplii four times a weeks and samplings were made after 2, 5, and 9 weeks. Results confirmed that feeding enhances coral growth rate and increases both the dark and light calcification rates. These rates were 50–75% higher in fed corals (FC; 60±20 and 200±40 nmol Ca2+ cm−2 h−1 for dark and light calcification, respectively) compared to control corals (CC; 30±9 and 124±23 nmol Ca2+ cm−2 h−1). The dark calcification rates, however, were four times lower than the rates of light calcification (independent of trophic status). After 5 weeks, chlorophyll a (chl-a) concentrations were four to seven times higher in fed corals (7–21 μg cm−2) than in control corals (2–5 μg cm−2). The amount of protein was also significantly higher in fed corals (2.11–2.50 mg cm−2) than in control corals (1.08–1.52 mg cm−2). Rates of photosynthesis in fed corals were 2–10 times higher (1.24±0.75 μmol O2 h−1 cm−2) than those measured in control corals (0.20±0.08 μmol O2 h−1 cm−2).

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

SUMMARY 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 14C-aspartic acid and 45Ca, 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 c2 concentrations were 3–4 times higher in fed corals (2.1±0.3 μg 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 (Pgmax= 570±60 nmol O2 cm–2 h–1 and Ik=403±27 μmol 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 Ca2+ 2 h–1 g–1 dry skeletal mass) compared to SC (1560±217 and 225±35 nmol Ca2+ 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.

Vital effects in coral skeletal composition display strict three-dimensional control

Biological control over coral skeletal composition is poorly understood but critically important to paleoenvironmental reconstructions. We present microanalytical measurements of trace-element abundances as well as oxygen and carbon isotopic compositions of individual skeletal components in the zooxanthellate coral Colpophyllia sp. Our data show that centers of calcification (COC) have higher trace element concentrations and distinctly lighter isotopic compositions than the fibrous components of the skeleton. These observations necessitate that COC and the fibrous skeleton are precipitated by different mechanisms, which are controlled by specialized domains of the calicoblastic cell-layer. Biological processes control the composition of the skeleton even at the ultrastructure level.

Biological forcing controls the chemistry of reef‐building coral skeleton

[1] We present analyses of major elements C and Ca and trace elements N, S, Mg and Sr in a Porites sp. exoskeleton with a spatial resolution better than similar to 150 nm. Trace element variations are evaluated directly against the ultrastructure of the skeleton and are ascribed to dynamic biological forcing. Individual growth layers in the bulk fibrous aragonite skeleton form on sub-daily timescales. Magnesium concentration variations are dramatically correlated with the growth layers, but are uncorrelated with Sr concentration variations. Observed (sub) seasonal relationships between water temperature and skeletal trace-element chemistry are secondary, mediated by sensitive biological processes to which classical thermodynamic formalism does not apply.

Strontium-86 labeling experiments show spatially heterogeneous skeletal formation in the scleractinian coral Porites porites

abundances of 86 Sr. The distribution of 86 Sr in the skeleton was imaged with the NanoSIMS ion microprobe with a spatial resolution of 200 nm and combined with images of the skeletal ultra-structure. Importantly, the distribution of the 86 Sr label in the P. porites skeleton was found to be strongly heterogeneous. This constrains the physical dimensions of the hypothetical Extracellular Calcifying Fluid (ECF) reservoir at the surface of the growing skeleton, which is implicit in most geochemical models for coral biomineralization. These new experimental capabilities allow for a much more detailed view of the growth dynamics for a wide range of marine organisms that

Nickel and ocean warming affect scleractinian coral growth

The sensitivity of corals and their Symbiodinium to warming has been extensively documented; however very few studies considered that anthropogenic inputs such as metal pollution have already an impact on many fringing reefs. Thus, today, nickel releases are common in coastal ecosystems. In this study, two major reef-building species Acropora muricata and Pocillopora damicornis were exposed in situ to ambient and moderate nickel concentrations on a short-term period (1h) using benthic chamber experiments. Simultaneously, we tested in laboratory conditions the combined effects of a chronic exposure (8weeks) to moderate nickel concentrations and ocean warming on A. muricata. The in situ experiment highlighted that nickel enrichment, at ambient temperature, stimulated by 27 to 47% the calcification rates of both species but not their photosynthetic performances. In contrast, an exposure to higher nickel concentration, in combination with elevated temperature simulated in aquaria, severely depressed by 30% the growth of A. muricata.

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.

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

Environmental conditions are known to influence corals and their associated communities of microorganisms. However, our insights into the impacts of seasonal changes in ultraviolet radiation (UVR) on both coral physiology and microbiome remain very limited. To address this challenge, we maintained the coral Acropora muricata shaded from UVR or under ambient UVR levels during two contrasting seasons, i.e. summer and winter, and assessed the impact of UVR on the coral holobiont at each season. To this end, we analysed the physiology (e.g. calcification, protein content, photosynthesis-related parameters) and coral microbiota composition, as well as the abundance and composition of the microbial communities and organic matter contents of the surrounding seawater. Our results show major seasonal effects on coral phenotype: (1) a lower host biomass and photosynthesizing, but fast calcifying phenotype in summer, and (2) a higher host biomass and photosynthesizing, but slow calcifying phenotype in winter. UVR had only a significant impact on Symbiodinium functioning. Specifically, high UVR levels reduced photosynthesis efficiency in summer, but an increase in chlorophyll a content may have compensated for this effect. The coral microbiota, which was variable but generally dominated by Endozoicomonas, was not affected by UVR, but its composition differed between seasons. In contrast, UVR had a major, but differential impact on the seawater microbial communities at both seasons. Particularly in summer, bacteria from the Alteromonadaceae were significantly more abundant (15-fold; up to 75%) in seawater under ambient UVR levels. Overall, our study suggests that UVR has only a limited impact on coral holobiont composition and functioning, despite major fluctuations in the surrounding seawater microbiome; seasonal changes in the holobiont are thus mostly driven by other environmental factors.

Enhancement of coral calcification via the interplay of nickel and urease

Corals are the main reef builders through the formation of calcium carbonate skeletons. In recent decades, coral calcification has however been impacted by many global (climate change) and local stressors (such as destructive fishing practices and changes in water quality). In this particular context, it is crucial to identify and characterize the various factors that promote coral calcification. We thus performed the first investigation of the effect of nickel and urea enrichment on the calcification rates of three coral species. These two factors may indeed interact with calcification through the activity of urease, which catalyzes the hydrolysis of urea to produce inorganic carbon and ammonia that are involved in the calcification process. Experiments were performed with the asymbiotic coral Dendrophyllia arbuscula and, to further assess if urea and/or nickel has an indirect link with calcification through photosynthesis, results were compared with those obtained with two symbiotic corals, Acropora muricata and Pocillopora damicornis, for which we also measured photosynthetic rates. Ambient and enriched nickel (0.12 and 3.50 μg L-1) combined with ambient and enriched urea concentrations (0.26 and 5.52 μmol L-1) were tested during 4 weeks in aquaria. We demonstrate in the study that a nickel enrichment alone or combined with a urea enrichment strongly stimulated urea uptake rates of the three tested species. In addition, this enhancement of urea uptake and hydrolysis significantly increased the long-term calcification rates (i.e. growth) of the three coral species investigated, inducing a 1.49-fold to 1.64-fold increase, respectively for D. arbuscula and P. damicornis. Since calcification was greatly enhanced by nickel in the asymbiotic coral species - i.e. in absence of photosynthesis - we concluded that the effect of increased urease activity on calcification was mainly direct. According to our results, it can be assumed that corals in some fringing reefs, benefiting from seawater enriched in nickel may have advantages and might be able to use urea more effectively as a carbon and nitrogen source. It can also be suggested that urea, for which hotspots are regularly measured in reef waters may alleviate the negative consequences of thermal stress on corals.