OMICS Approaches to Assess Dinoflagellate Responses to Chemical Stressors.

Dinoflagellates are important primary producers known to form Harmful Algae Blooms (HABs). In water, nutrient availability, pH, salinity and anthropogenic contamination constitute chemical stressors for them. The emergence of OMICs approaches propelled our understanding of dinoflagellates' responses to stressors. However, in dinoflagellates, these approaches are still biased, as transcriptomic approaches are largely conducted compared to proteomic and metabolomic approaches. Furthermore, integrated OMICs approaches are just emerging. Here, we report recent contributions of the different OMICs approaches to the investigation of dinoflagellates' responses to chemical stressors and discuss the current challenges we need to face to push studies further despite the lack of genomic resources available for dinoflagellates.

Seascape genomics reveals candidate molecular targets of heat stress adaptation in three coral species.

Anomalous heat waves are causing a major decline of hard corals around the world and threatening the persistence of coral reefs. There are, however, reefs that have been exposed to recurrent thermal stress over the years and whose corals appear to have been tolerant against heat. One of the mechanisms that could explain this phenomenon is local adaptation, but the underlying molecular mechanisms are poorly known. In this work, we applied a seascape genomics approach to study heat stress adaptation in three coral species of New Caledonia (southwestern Pacific) and to uncover the molecular actors potentially involved. We used remote sensing data to characterize the environmental trends across the reef system, and sampled corals living at the most contrasted sites. These samples underwent next generation sequencing to reveal single nucleotide polymorphisms (SNPs), frequencies of which were associated with heat stress gradients. As these SNPs might underpin an adaptive role, we characterized the functional roles of the genes located in their genomic region. In each of the studied species, we found heat stress-associated SNPs located in proximity of genes involved in pathways well known to contribute to the cellular responses against heat, such as protein folding, oxidative stress homeostasis, inflammatory and apoptotic pathways, and DNA damage-repair. In some cases, the same candidate molecular targets of heat stress adaptation recurred among species. Together, these results underline the relevance and the power of the seascape genomics approach for the discovery of adaptive traits that could allow corals to persist across wider thermal ranges.

Coral cover surveys corroborate predictions on reef adaptive potential to thermal stress.

As anomalous heat waves are causing the widespread decline of coral reefs worldwide, there is an urgent need to identify coral populations tolerant to thermal stress. Heat stress adaptive potential is the degree of tolerance expected from evolutionary processes and, for a given reef, depends on the arrival of propagules from reefs exposed to recurrent thermal stress. For this reason, assessing spatial patterns of thermal adaptation and reef connectivity is of paramount importance to inform conservation strategies. In this work, we applied a seascape genomics framework to characterize the spatial patterns of thermal adaptation and connectivity for coral reefs of New Caledonia (Southern Pacific). In this approach, remote sensing of seascape conditions was combined with genomic data from three coral species. For every reef of the region, we computed a probability of heat stress adaptation, and two indices forecasting inbound and outbound connectivity. We then compared our indicators to field survey data, and observed that decrease of coral cover after heat stress was lower at reefs predicted with high probability of adaptation and inbound connectivity. Last, we discussed how these indicators can be used to inform local conservation strategies and preserve the adaptive potential of New Caledonian reefs.

Seascape genomics as a new tool to empower coral reef conservation strategies: An example on north-western Pacific Acropora digitifera.

Coral reefs are suffering a major decline due to the environmental constraints imposed by climate change. Over the last 20 years, three major coral bleaching events occurred in concomitance with anomalous heatwaves, provoking a severe loss of coral cover worldwide. The conservation strategies for preserving reefs, as they are implemented now, cannot cope with global climatic shifts. Consequently, researchers are advocating for preservation networks to be set-up to reinforce coral adaptive potential. However, the main obstacle to this implementation is that studies on coral adaption are usually hard to generalize at the scale of a reef system. Here, we study the relationships between genotype frequencies and environmental characteristics of the sea (seascape genomics), in combination with connectivity analysis, to investigate the adaptive potential of a flagship coral species of the Ryukyu Archipelago (Japan). By associating genotype frequencies with descriptors of historical environmental conditions, we discovered six genomic regions hosting polymorphisms that might promote resistance against heat stress. Remarkably, annotations of genes in these regions were consistent with molecular roles associated with heat responses. Furthermore, we combined information on genetic and spatial distances between reefs to predict connectivity at a regional scale. The combination of these results portrayed the adaptive potential of this population: we were able to identify reefs carrying potential heat stress adapted genotypes and to understand how they disperse to neighbouring reefs. This information was summarized by objective, quantifiable and mappable indices covering the whole region, which can be extremely useful for future prioritization of reefs in conservation planning. This framework is transferable to any coral species on any reef system and therefore represents a valuable tool for empowering preservation efforts dedicated to the protection of coral reefs in warming oceans.

Dimethylsulfoniopropionate concentration in coral reef invertebrates varies according to species assemblages.

Dimethylsulfoniopropionate (DMSP) is a key compound in the marine sulfur cycle, and is produced in large quantities in coral reefs. In addition to Symbiodiniaceae, corals and associated bacteria have recently been shown to play a role in DMSP metabolism. Numerous ecological studies have focused on DMSP concentrations in corals, which led to the hypothesis that increases in DMSP levels might be a general response to stress. Here we used multiple species assemblages of three common Indo-Pacific holobionts, the scleractinian corals Pocillopora damicornis and Acropora cytherea, and the giant clam Tridacna maxima and examined the DMSP concentrations associated with each species within different assemblages and thermal conditions. Results showed that the concentration of DMSP in A. cytherea and T. maxima is modulated according to the complexity of species assemblages. To determine the potential importance of symbiotic dinoflagellates in DMSP production, we then explored the relative abundance of Symbiodiniaceae clades in relation to DMSP levels using metabarcoding, and found no significant correlation between these factors. Finally, this study also revealed the existence of homologs involved in DMSP production in giant clams, suggesting for the first time that, like corals, they may also contribute to DMSP production. Taken together, our results demonstrated that corals and giant clams play important roles in the sulfur cycle. Because DMSP production varies in response to specific species-environment interactions, this study offers new perspectives for future global sulfur cycling research.

Metabarcoding reveals distinct microbiotypes in the giant clam Tridacna maxima.

BACKGROUND: Giant clams and scleractinian (reef-building) corals are keystone species of coral reef ecosystems. The basis of their ecological success is a complex and fine-tuned symbiotic relationship with microbes. While the effect of environmental change on the composition of the coral microbiome has been heavily studied, we know very little about the composition and sensitivity of the microbiome associated with clams. Here, we explore the influence of increasing temperature on the microbial community (bacteria and dinoflagellates from the family Symbiodiniaceae) harbored by giant clams, maintained either in isolation or exposed to other reef species. We created artificial benthic assemblages using two coral species (Pocillopora damicornis and Acropora cytherea) and one giant clam species (Tridacna maxima) and studied the microbial community in the latter using metagenomics. RESULTS: Our results led to three major conclusions. First, the health status of giant clams depended on the composition of the benthic species assemblages. Second, we discovered distinct microbiotypes in the studied T. maxima population, one of which was disproportionately dominated by Vibrionaceae and directly linked to clam mortality. Third, neither the increase in water temperature nor the composition of the benthic assemblage had a significant effect on the composition of the Symbiodiniaceae and bacterial communities of T. maxima. CONCLUSIONS: Altogether, our results suggest that at least three microbiotypes naturally exist in the studied clam populations, regardless of water temperature. These microbiotypes plausibly provide similar functions to the clam host via alternate molecular pathways as well as microbiotype-specific functions. This redundancy in functions among microbiotypes together with their specificities provides hope that giant clam populations can tolerate some levels of environmental variation such as increased temperature. Importantly, the composition of the benthic assemblage could make clams susceptible to infections by Vibrionaceae, especially when water temperature increases. Video abstract.

A RID-like putative cytosine methyltransferase homologue controls sexual development in the fungus Podospora anserina.

DNA methyltransferases are ubiquitous enzymes conserved in bacteria, plants and opisthokonta. These enzymes, which methylate cytosines, are involved in numerous biological processes, notably development. In mammals and higher plants, methylation patterns established and maintained by the cytosine DNA methyltransferases (DMTs) are essential to zygotic development. In fungi, some members of an extensively conserved fungal-specific DNA methyltransferase class are both mediators of the Repeat Induced Point mutation (RIP) genome defense system and key players of sexual reproduction. Yet, no DNA methyltransferase activity of these purified RID (RIP deficient) proteins could be detected in vitro. These observations led us to explore how RID-like DNA methyltransferase encoding genes would play a role during sexual development of fungi showing very little genomic DNA methylation, if any. To do so, we used the model ascomycete fungus Podospora anserina. We identified the PaRid gene, encoding a RID-like DNA methyltransferase and constructed knocked-out ΔPaRid defective mutants. Crosses involving P. anserina ΔPaRid mutants are sterile. Our results show that, although gametes are readily formed and fertilization occurs in a ΔPaRid background, sexual development is blocked just before the individualization of the dikaryotic cells leading to meiocytes. Complementation of ΔPaRid mutants with ectopic alleles of PaRid, including GFP-tagged, point-mutated and chimeric alleles, demonstrated that the catalytic motif of the putative PaRid methyltransferase is essential to ensure proper sexual development and that the expression of PaRid is spatially and temporally restricted. A transcriptomic analysis performed on mutant crosses revealed an overlap of the PaRid-controlled genetic network with the well-known mating-types gene developmental pathway common to an important group of fungi, the Pezizomycotina.

Unique quantitative Symbiodiniaceae signature of coral colonies revealed through spatio-temporal survey in Moorea.

One of the mechanisms of rapid adaptation or acclimatization to environmental changes in corals is through the dynamics of the composition of their associated endosymbiotic Symbiodiniaceae community. The various species of these dinoflagellates are characterized by different biological properties, some of which can confer stress tolerance to the coral host. Compelling evidence indicates that the corals' Symbiodiniaceae community can change via shuffling and/or switching but the ecological relevance and the governance of these processes remain elusive. Using a qPCR approach to follow the dynamics of Symbiodiniaceae genera in tagged colonies of three coral species over a 10-18 month period, we detected putative genus-level switching of algal symbionts, with coral species-specific rates of occurrence. However, the dynamics of the corals' Symbiodiniaceae community composition was not driven by environmental parameters. On the contrary, putative shuffling event were observed in two coral species during anomalous seawater temperatures and nutrient concentrations. Most notably, our results reveal that a suit of permanent Symbiodiniaceae genera is maintained in each colony in a specific range of quantities, giving a unique 'Symbiodiniaceae signature' to the host. This individual signature, together with sporadic symbiont switching may account for the intra-specific differences in resistance and resilience observed during environmental anomalies.

Towards an in-depth characterization of Symbiodiniaceae in tropical giant clams via metabarcoding of pooled multi-gene amplicons.

High-throughput sequencing is revolutionizing our ability to comprehensively characterize free-living and symbiotic Symbiodiniaceae, a diverse dinoflagellate group that plays a critical role in coral reef ecosystems. Most studies however, focus on a single marker for metabarcoding Symbiodiniaceae, potentially missing important ecological traits that a combination of markers may capture. In this proof-of-concept study, we used a small set of symbiotic giant clam (Tridacna maxima) samples obtained from nine French Polynesian locations and tested a dual-index sequence library preparation method that pools and simultaneously sequences multiple Symbiodiniaceae gene amplicons per sample for in-depth biodiversity assessments. The rationale for this approach was to allow the metabarcoding of multiple genes without extra costs associated with additional single amplicon dual indexing and library preparations. Our results showed that the technique effectively recovered very similar proportions of sequence reads and dominant Symbiodiniaceae clades among the three pooled gene amplicons investigated per sample, and captured varying levels of phylogenetic resolution enabling a more comprehensive assessment of the diversity present. The pooled Symbiodiniaceae multi-gene metabarcoding approach described here is readily scalable, offering considerable analytical cost savings while providing sufficient phylogenetic information and sequence coverage.

Differential effects of coral-giant clam assemblages on biofouling formation.

To prevent the settlement and/or the growth of fouling organisms (i.e. bacteria, fungi or microalgae), benthic sessile species have developed various defense mechanisms among which the production of chemical molecules. While studies have mostly focused on the release of chemical compounds by single species, there exist limited data on multi-species assemblages. We used an integrative approach to explore the potential interactive effects of distinct assemblages of two corals species and one giant clam species on biofouling appearance and composition. Remarkably, we found distinct biofouling communities suggesting the importance of benthic sessile assemblages in biofouling control. Moreover, the assemblage of 3 species led to an inhibition of biofouling, likely through a complex of secondary metabolites. Our results highlight that through their different effect on their near environment, species assemblages might be of upmost importance for their survival and therefore, should now be taken into account for sustainable management of coral reefs.

Detection of Human Enteric Viruses in French Polynesian Wastewaters, Environmental Waters and Giant Clams.

Lack of wastewater treatment efficiency causes receiving seawaters and bivalve molluscan shellfish to become contaminated, which can lead to public health issues. Six wastewater samples, five seawater samples and three batches of giant clams from Tahiti (French Polynesia) were investigated for the presence of enteric viruses, but also if present, for the diversity, infectivity and integrity of human adenoviruses (HAdV). Enteroviruses (EV), sapoviruses (SaV) and human polyomaviruses (HPyV) were detected in all wastewater samples. In decreasing frequency, noroviruses (NoV) GII and HAdV, rotaviruses (RoV), astroviruses (AsV), NoV GI and finally hepatitis E viruses (HEV) were also observed. Nine types of infectious HAdV were identified. HPyV and EV were found in 80% of seawater samples, NoV GII in 60%, HAdV and SaV in 40% and AsV and RoV in 20%. NoV GI and HEV were not detected in seawater. Intact and infectious HAdV-41 were detected in one of the two seawater samples that gave a positive qPCR result. Hepatitis A viruses were never detected in any water types. Analysis of transcriptomic data from giant clams revealed homologues of fucosyltransferases (FUT genes) involved in ligand biosynthesis that strongly bind to certain NoV strains, supporting the giant clams ability to bioaccumulate NoV. This was confirmed by the presence of NoV GII in one of the three batches of giant clams placed in a contaminated marine area. Overall, all sample types were positive for at least one type of virus, some of which were infectious and therefore likely to cause public health concerns.

Exposure to the environmentally-persistent insecticide chlordecone induces detoxification genes and causes polyp bail-out in the coral P. damicornis.

Marine ecosystems are both stressed and threatened by pesticides that are used on land. Nevertheless, research on the impact of pesticides on coral reefs and the underlying mechanisms is still in its infancy. The insecticide chlordecone is a persistent organic pollutant with carcinogenic effects in rats and mice. Chlordecone has been detected in diverse marine organisms in the Caribbean, but unexpectedly, also in French Polynesia. We combined transcriptomic and morphologic analyses of analyses the response of the coral Pocillopora damicornis to chlordecone stress. We compared chlordecone stress with thermal stress to determine a chlordecone-specific response. We found eight transcripts related to the P450-1A or P450-3A families that were specifically overexpressed in response to chlordecone. There was also sequential overexpression of transcripts involved in apoptosis and degradation of cellular matrix proteins. Finally, we report the first observation of chlordecone-induced P. damicornis polyp bail-out. Altogether, these results strongly suggest that apoptosis and expression of genes belonging to the cathepsin family are sequentially regulated processes leading to coenosarc dissociation and loss.

On the occurrence of intracolonial genotypic variability in highly clonal populations of the hydrocoral Millepora platyphylla at Moorea (French Polynesia).

Intracolonial genotypic variability is described in many colonial organisms and arises from mosaicism (somatic mutation) and/or chimerism (allogenic fusion). Both processes provide an additional source of genotypic variation in natural populations and raise questions on the biological significance of colonies having more than one genotype. Using fifteen microsatellite markers, we screened for potential genetic heterogeneity within Millepora platyphylla colonies, a hydrocoral species known for its extensive morphological plasticity among reef habitats. We aimed to determine whether mosaicism and chimerism were related to specific reef habitats and/or colony morphologies. Our results show that intracolonial genotypic variability was common (31.4%) in M. platyphylla at Moorea, French Polynesia, with important variations in its frequency among habitats (0-60%), while no effect of morphology was observed. Mosaicism seemed responsible for most of the genetic heterogeneity (87.5%), while chimerism was rarer. Some mosaics were shared among fire coral clones indicating that mutations could be spread via colony fragmentation. Further, the genotypic variability among clones suggests that colonies produced asexually through fragmentation have the potential to accumulate their own mutations over time. Such mutation dynamics might have important implications for the adaptive potential of long-lived reef-builder populations that are predominantly sustained through asexual reproduction.

Genetic diversity and differentiation in reef-building Millepora species, as revealed by cross-species amplification of fifteen novel microsatellite loci.

Quantifying the genetic diversity in natural populations is crucial to address ecological and evolutionary questions. Despite recent advances in whole-genome sequencing, microsatellite markers have remained one of the most powerful tools for a myriad of population genetic approaches. Here, we used the 454 sequencing technique to develop microsatellite loci in the fire coral Millepora platyphylla, an important reef-builder of Indo-Pacific reefs. We tested the cross-species amplification of these loci in five other species of the genus Millepora and analysed its success in correlation with the genetic distances between species using mitochondrial 16S sequences. We succeeded in discovering fifteen microsatellite loci in our target species M. platyphylla, among which twelve were polymorphic with 2-13 alleles and a mean observed heterozygosity of 0.411. Cross-species amplification in the five other Millepora species revealed a high probability of amplification success (71%) and polymorphism (59%) of the loci. Our results show no evidence of decreased heterozygosity with increasing genetic distance. However, only one locus enabled measures of genetic diversity in the Caribbean species M. complanata due to high proportions of null alleles for most of the microsatellites. This result indicates that our novel markers may only be useful for the Indo-Pacific species of Millepora. Measures of genetic diversity revealed significant linkage disequilibrium, moderate levels of observed heterozygosity (0.323-0.496) and heterozygote deficiencies for the Indo-Pacific species. The accessibility to new polymorphic microsatellite markers for hydrozoan Millepora species creates new opportunities for future research on processes driving the complexity of their colonisation success on many Indo-Pacific reefs.

An updated assessment of Symbiodinium spp. that associate with common scleractinian corals from Moorea (French Polynesia) reveals high diversity among background symbionts and a novel finding of clade B.

The adaptative bleaching hypothesis (ABH) states that, depending on the symbiotic flexibility of coral hosts (i.e., the ability of corals to "switch" or "shuffle" their algal symbionts), coral bleaching can lead to a change in the composition of their associated Symbiodinium community and, thus, contribute to the coral's overall survival. In order to determine the flexibility of corals, molecular tools are required to provide accurate species delineations and to detect low levels of coral-associated Symbiodinium. Here, we used highly sensitive quantitative (real-time) PCR (qPCR) technology to analyse five common coral species from Moorea (French Polynesia), previously screened using only traditional molecular methods, to assess the presence of low-abundance (background) Symbiodinium spp. Similar to other studies, each coral species exhibited a strong specificity to a particular clade, irrespective of the environment. In addition, however, each of the five species harboured at least one additional Symbiodinium clade, among clades A-D, at background levels. Unexpectedly, and for the first time in French Polynesia, clade B was detected as a coral symbiont. These results increase the number of known coral-Symbiodinium associations from corals found in French Polynesia, and likely indicate an underestimation of the ability of the corals in this region to associate with and/or "shuffle" different Symbiodinium clades. Altogether our data suggest that corals from French Polynesia may favor a trade-off between optimizing symbioses with a specific Symbiodinium clade(s), maintaining associations with particular background clades that may play a role in the ability of corals to respond to environmental change.

Changes in fatty acid composition in the giant clam Tridacna maxima in response to thermal stress.

Temperature can modify membrane fluidity and thus affects cellular functions and physiological activities. This study examines lipid remodelling in the marine symbiotic organism, Tridacna maxima, during a time series of induced thermal stress, with an emphasis on the morphology of their symbiont Symbiodinium First, we show that the French Polynesian giant clams harbour an important proportion of saturated fatty acids (SFA), which reflects their tropical location. Second, in contrast to most marine organisms, the total lipid content in giant clams remained constant under stress, though some changes in their composition were shown. Third, the stress-induced changes in fatty acid (FA) diversity were accompanied by an upregulation of genes involved in lipids and ROS pathways. Finally, our microscopic analysis revealed that for the giant clam's symbiont, Symbiodinium, thermal stress led to two sequential cell death processes. Our data suggests that the degradation of Symbiodinium cells could provide an additional source of energy to T maxima in response to heat stress.

Symbiodinium clades A and D differentially predispose Acropora cytherea to disease and Vibrio spp. colonization.

Coral disease outbreaks have increased over the last three decades, but their causal agents remain mostly unclear (e.g., bacteria, viruses, fungi, protists). This study details a 14-month-long survey of coral colonies in which observations of the development of disease was observed in nearly half of the sampled colonies. A bimonthly qPCR method was used to quantitatively and qualitatively evaluate Symbiodinium assemblages of tagged colonies, and to detect the presence of Vibrio spp. Firstly, our data showed that predisposition to disease development in general, and, more specifically, infection by Vibrio spp. in Acropora cytherea depended on which clades of Symbiodinium were harbored. In both cases, harboring clade D rather than A was beneficial to the coral host. Secondly, the detection of Vibrio spp. in only colonies that developed disease strongly suggests opportunistic traits of the bacteria. Finally, even if sporadic cases of switching and probably shuffling were observed, this long-term survey does not suggest specific-clade recruitment in response to stressors. Altogether, our results demonstrate that the fitness of the coral holobiont depends on its initial consortium of Symbiodinium, which is distinct among colonies, rather than a temporary adaptation achieved through acquiring different Symbiodinium clades.

Dinoflagellate diversity among nudibranchs and sponges from French Polynesia: insights into associations and transfer.

Symbioses with the dinoflagellate Symbiodinium are widespread among marine invertebrates and protists, especially in nutritionally demanding habitats, such as tropical coral reefs, where they play a major role in ecosystem survival. Moreover, apart from corals and sea anemones, many of the Symbiodinium species and clades involved in these partnerships remain to be characterized. This study provides new insights into nudibranch and sponge associations with Symbiodinium by sequencing regions of the Symbiodinium 28S rDNA and the host mitochondrial COI oxidase. Specimens were sampled between 2011 and 2013 from locations around the islands of Moorea and Tahiti, French Polynesia. Our results revealed that some of the sponges and nudibranchs harbored typical Symbiodinium from clade B or C while others harbored new, undescribed Symbiodinium-like dinoflagellates. A detailed analysis of the different life stages of the nudibranch Phestilla lugubris and of its specific coral prey, Porites rus, suggests a prey-predator horizontal transfer of the symbiont and its vertical inheritance from the parent to the eggs.

The founding charter of the Genomic Observatories Network.

The co-authors of this paper hereby state their intention to work together to launch the Genomic Observatories Network (GOs Network) for which this document will serve as its Founding Charter. We define a Genomic Observatory as an ecosystem and/or site subject to long-term scientific research, including (but not limited to) the sustained study of genomic biodiversity from single-celled microbes to multicellular organisms.An international group of 64 scientists first published the call for a global network of Genomic Observatories in January 2012. The vision for such a network was expanded in a subsequent paper and developed over a series of meetings in Bremen (Germany), Shenzhen (China), Moorea (French Polynesia), Oxford (UK), Pacific Grove (California, USA), Washington (DC, USA), and London (UK). While this community-building process continues, here we express our mutual intent to establish the GOs Network formally, and to describe our shared vision for its future. The views expressed here are ours alone as individual scientists, and do not necessarily represent those of the institutions with which we are affiliated.

Spatial and temporal variations in stable carbon (δ(13)C) and nitrogen (δ(15)N) isotopic composition of symbiotic scleractinian corals.

Tropical scleractinian corals are considered autotrophic as they rely mainly on photosynthesis-derived nutrients transferred from their photosymbionts. Corals are also able to capture and ingest suspended particulate organic matter, so heterotrophy can be an important supplementary trophic pathway to optimize coral fitness. The aim of this in situ study was to elucidate the trophic status of 10 coral species under contrasted environmental conditions in a French Polynesian lagoon. Carbon (δ(13)C) and nitrogen (δ(15)N) isotopic compositions of coral host tissues and photosymbionts were determined at 3 different fringing reefs during wet and dry seasons. Our results highlighted spatial variability in stable isotopic compositions of both coral host tissues and photosymbionts. Samples from the site with higher level of suspended particulate matter were (13)C-depleted and (15)N-enriched relative to corals and photosymbionts from less turbid sites. However, differences in both δ(13)C and δ(15)N between coral host tissues and their photosymbionts (Δ(host-photosymbionts 13)C and Δ(host-photosymbionts 15)N) were small (0.27 ± 0.76‰ and 1.40 ± 0.90‰, respectively) and similar at all sites, thus indicating no general increases in the heterotrophic pathway. Depleted δ(13)C and enriched δ(15)N values of coral host tissues measured at the most turbid site were explained by changes in isotopic composition of the inorganic nutrients taken up by photosymbionts and also by changes in rate of isotopic fractionation with environmental conditions. Our results also highlighted a lack of significant temporal variations in δ(13)C and δ(15)N values of coral host and photosymbiont tissues and in Δ(host-photosymbionts 13)C and Δ(host-photosymbionts 15)N values. This temporal stability indicated that corals remained principally autotrophic even during the wet season when photosymbiont densities were lower and the concentrations of phytoplankton were higher. Increased coral heterotrophy with higher food availability thus appears to be species-specific.