A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes.

Apicomplexa is a group of obligate intracellular parasites that includes the causative agents of human diseases such as malaria and toxoplasmosis. Apicomplexans evolved from free-living phototrophic ancestors, but how this transition to parasitism occurred remains unknown. One potential clue lies in coral reefs, of which environmental DNA surveys have uncovered several lineages of uncharacterized basally branching apicomplexans1,2. Reef-building corals have a well-studied symbiotic relationship with photosynthetic Symbiodiniaceae dinoflagellates (for example, Symbiodinium3), but the identification of other key microbial symbionts of corals has proven to be challenging4,5. Here we use community surveys, genomics and microscopy analyses to identify an apicomplexan lineage-which we informally name 'corallicolids'-that was found at a high prevalence (over 80% of samples, 70% of genera) across all major groups of corals. Corallicolids were the second most abundant coral-associated microeukaryotes after the Symbiodiniaceae, and are therefore core members of the coral microbiome. In situ fluorescence and electron microscopy confirmed that corallicolids live intracellularly within the tissues of the coral gastric cavity, and that they possess apicomplexan ultrastructural features. We sequenced the genome of the corallicolid plastid, which lacked all genes for photosystem proteins; this indicates that corallicolids probably contain a non-photosynthetic plastid (an apicoplast6). However, the corallicolid plastid differs from all other known apicoplasts because it retains the four ancestral genes that are involved in chlorophyll biosynthesis. Corallicolids thus share characteristics with both their parasitic and their free-living relatives, which suggests that they are evolutionary intermediates and implies the existence of a unique biochemistry during the transition from phototrophy to parasitism.

Assisted gene flow using cryopreserved sperm in critically endangered coral.

Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao-Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.

Coral larval settlement induction using tissue-associated and exuded coralline algae metabolites and the identification of putative chemical cues.

Reef-building crustose coralline algae (CCA) are known to facilitate the settlement and metamorphosis of scleractinian coral larvae. In recent decades, CCA coverage has fallen globally and degrading environmental conditions continue to reduce coral survivorship, spurring new restoration interventions to rebuild coral reef health. In this study, naturally produced chemical compounds (metabolites) were collected from two pantropical CCA genera to isolate and classify those that induce coral settlement. In experiments using four ecologically important Caribbean coral species, we demonstrate the applicability of extracted, CCA-derived metabolites to improve larval settlement success in coral breeding and restoration efforts. Tissue-associated CCA metabolites induced settlement of one coral species, Orbicella faveolata, while metabolites exuded by CCA (exometabolites) induced settlement of three species: Acropora palmata, Colpophyllia natans and Orbicella faveolata. In a follow-up experiment, CCA exometabolites fractionated and preserved using two different extraction resins induced the same level of larval settlement as the unfractionated positive control exometabolites. The fractionated CCA exometabolite pools were characterized using liquid chromatography tandem mass spectrometry, yielding 145 distinct molecular subnetworks that were statistically defined as CCA-derived and could be classified into 10 broad chemical classes. Identifying these compounds can reveal their natural prevalence in coral reef habitats and facilitate the development of new applications to enhance larval settlement and the survival of coral juveniles.

A multiomic analysis of in situ coral-turf algal interactions.

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

Taxonomy of the Apicomplexan Symbionts of Coral, including Corallicolida ord. nov., Reassignment of the Genus Gemmocystis, and Description of New Species Corallicola aquarius gen. nov. sp. nov. and Anthozoaphila gnarlus gen. nov. sp. nov.

Corals (Metazoa; Cnidaria; Anthozoa) have recently been shown to play host to a widespread and diverse group of intracellular symbionts of the phylum Apicomplexa. These symbionts, colloquially called "corallicolids", are mostly known through molecular analyses, and no formal taxonomy has been proposed. Another apicomplexan, Gemmocystis cylindrus (described from the coral Dendrogyra cylindrus), may be related to corallicolids, but lacks molecular data. Here, we isolate and describe motile trophozoite (feeding) corallicolids cells using microscopic (light, SEM, and TEM) and molecular phylogenetic analysis to provide the basis for a formal description. Phylogenetic analyses using nuclear and plastid rRNA operons, and three mitochondrial protein sequences derived from single cell transcriptomes, all confirm that these organisms fall into a discrete deep-branching clade within the Apicomplexa not closely related to any known species or major subgroup. As a result, we assign this clade to a new order, Corallicolida ord. nov., and family, Corallicolidae fam. nov. We describe a type species, Corallicola aquarius gen. nov. sp. nov. from its Rhodactis sp. host, and also describe a second species, Anthozoaphila gnarlus gen. nov. sp. nov., from the coral host Madracis mirabilis. Finally, we propose reassigning the incertae sedis taxon G. cylindrus from the order Agamococcidiorida to the Corallicolida, based on similarities in morphology and host localization to that of the corallicolids.

Implications of 2D versus 3D surveys to measure the abundance and composition of benthic coral reef communities.

A paramount challenge in coral reef ecology is to estimate the abundance and composition of the communities residing in such complex ecosystems. Traditional 2D projected surface cover estimates neglect the 3D structure of reefs and reef organisms, overlook communities residing in cryptic reef habitats (e.g., overhangs, cavities), and thus may fail to represent biomass estimates needed to assess trophic ecology and reef function. Here, we surveyed the 3D surface cover, biovolume, and biomass (i.e., ash-free dry weight) of all major benthic taxa on 12 coral reef stations on the island of Curaçao (Southern Caribbean) using structure-from-motion photogrammetry, coral point counts, in situ measurements, and elemental analysis. We then compared our 3D benthic community estimates to corresponding estimates of traditional 2D projected surface cover to explore the differences in benthic community composition using different metrics. Overall, 2D cover was dominated (52 ± 2%, mean ± SE) by non-calcifying phototrophs (macroalgae, turf algae, benthic cyanobacterial mats), but their contribution to total reef biomass was minor (3.2 ± 0.6%). In contrast, coral cover (32 ± 2%) more closely resembled coral biomass (27 ± 6%). The relative contribution of erect organisms, such as gorgonians and massive sponges, to 2D cover was twofold and 11-fold lower, respectively, than their contribution to reef biomass. Cryptic surface area (3.3 ± 0.2 m2 m-2 planar reef) comprised half of the total reef substrate, rendering two thirds of coralline algae and almost all encrusting sponges (99.8%) undetected in traditional assessments. Yet, encrusting sponges dominated reef biomass (35 ± 18%). Based on our quantification of exposed and cryptic reef communities using different metrics, we suggest adjustments to current monitoring approaches and highlight ramifications for evaluating the ecological contributions of different taxa to overall reef function. To this end, our metric conversions can complement other benthic assessments to generate non-invasive estimates of the biovolume, biomass, and elemental composition (i.e., standing stocks of organic carbon and nitrogen) of Caribbean coral reef communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00338-021-02118-6.

Meta-mass shift chemical profiling of metabolomes from coral reefs.

Untargeted metabolomics of environmental samples routinely detects thousands of small molecules, the vast majority of which cannot be identified. Meta-mass shift chemical (MeMSChem) profiling was developed to identify mass differences between related molecules using molecular networks. This approach illuminates metabolome-wide relationships between molecules and the putative chemical groups that differentiate them (e.g., H2, CH2, COCH2). MeMSChem profiling was used to analyze a publicly available metabolomic dataset of coral, algal, and fungal mat holobionts (i.e., the host and its associated microbes and viruses) sampled from some of Earth's most remote and pristine coral reefs. Each type of holobiont had distinct mass shift profiles, even when the analysis was restricted to molecules found in all samples. This result suggests that holobionts modify the same molecules in different ways and offers insights into the generation of molecular diversity. Three genera of stony corals had distinct patterns of molecular relatedness despite their high degree of taxonomic relatedness. MeMSChem profiles also partially differentiated between individuals, suggesting that every coral reef holobiont is a potential source of novel chemical diversity.

Validation of a universal set of primers to study animal-associated microeukaryotic communities.

The application of metabarcoding to study animal-associated microeukaryotes has been restricted because the universal barcode used to study microeukaryotic ecology and distribution in the environment, the Small Subunit of the Ribosomal RNA gene (18S rRNA), is also present in the host. As a result, when host-associated microbial eukaryotes are analysed by metabarcoding, the reads tend to be dominated by host sequences. We have done an in silico validation against the SILVA 18S rRNA database of a non-metazoan primer set (primers that are biased against the metazoan 18S rRNA) that recovers only 2.6% of all the metazoan sequences, while recovering most of the other eukaryotes (80.4%). Among metazoans, the non-metazoan primers are predicted to amplify 74% of Porifera sequences, 4% of Ctenophora, and 15% of Cnidaria, while amplifying almost no sequences within Bilateria. In vivo, these non-metazoan primers reduce significantly the animal signal from coral and human samples, and when compared against universal primers provide at worst a 2-fold decrease in the number of metazoan reads and at best a 2800-fold decrease. This easy, inexpensive, and near-universal method for the study of animal-associated microeukaryotes diversity will contribute to a better understanding of the microbiome.

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host.

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

High Prevalence and Endemism of Trypanosomatids on a Small Caribbean Island.

We describe the monoxenous trypanosomatids parasitizing true bugs and flies on the island of Curaçao. Out of 248 examined true bugs belonging to 17 species, 93 individuals were found to be infected (overall 38% prevalence) by at least one trypanosomatid species (referred to as typing units; TUs). Out of 80 flies, six were infected. All detected trypanosomatids were compared based on their 18S rRNA sequences with TUs parasitizing bugs and flies described from mainland South America, allowing us to assess their diversity and distribution. Besides Leptomonas pyrrhocoris and Leptomonas seymouri, two known species of the subfamily Leishmaniinae, our analysis revealed six new TUs falling into the groups 'jaculum', Blastocrithidia and Herpetomonas. Moreover, two new members of the genus Phytomonas and three new TUs belonging to the monophyletic group designated as 'new clade II' sensu Mol. Phylogenet. Evol, 69, 255 (2013) were isolated. The detected trypanosomatids were characterized by moderate diversity (13 TUs) species richness. Out of nine and four TUs from the heteropteran and dipteran hosts, respectively, 11 TUs have not been encountered before. Although a sampling bias may partially affect the comparison between trypanosomatid communities on Curaçao and the mainland, the high proportion of unique TUs from the former location suggests that the prominent role of islands in increasing the global diversity of macroscopic organisms may also extend to their protistan parasites.

Costs and benefits of maternally inherited algal symbionts in coral larvae.

Many marine invertebrates provide their offspring with symbionts. Yet the consequences of maternally inherited symbionts on larval fitness remain largely unexplored. In the stony coral Favia fragum (Esper 1797), mothers produce larvae with highly variable amounts of endosymbiotic algae, and we examined the implications of this variation in symbiont density on the performance of F. fragum larvae under different environmental scenarios. High symbiont densities prolonged the period that larvae actively swam and searched for suitable settlement habitats. Thermal stress reduced survival and settlement success in F. fragum larvae, whereby larvae with high symbiont densities suffered more from non-lethal stress and were five times more likely to die compared with larvae with low symbiont densities. These results show that maternally inherited algal symbionts can be either beneficial or harmful to coral larvae depending on the environmental conditions at hand, and suggest that F. fragum mothers use a bet-hedging strategy to minimize risks associated with spatio-temporal variability in their offspring's environment.

Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors.

Holobionts are species-specific associations between macro- and microorganisms. On coral reefs, the benthic coverage of coral and algal holobionts varies due to natural and anthropogenic forcings. Different benthic macroorganisms are predicted to have specific microbiomes. In contrast, local environmental factors are predicted to select for specific metabolic pathways in microbes. To reconcile these two predictions, we hypothesized that adaptation of microbiomes to local conditions is facilitated by the horizontal transfer of genes responsible for specific metabolic capabilities. To test this hypothesis, microbial metagenomes were sequenced from 22 coral reefs at 11 Line Islands in the central Pacific that together span a wide range of biogeochemical and anthropogenic influences. Consistent with our hypothesis, the percent cover of major benthic functional groups significantly correlated with particular microbial taxa. Reefs with higher coral cover had a coral microbiome with higher abundances of Alphaproteobacteria (such as Rhodobacterales and Sphingomonadales), whereas microbiomes of algae-dominated reefs had higher abundances of Gammaproteobacteria (such as Alteromonadales, Pseudomonadales, and Vibrionales), Betaproteobacteria, and Bacteriodetes. In contrast to taxa, geography was the strongest predictor of microbial community metabolism. Microbial communities on reefs with higher nutrient availability (e.g., equatorial upwelling zones) were enriched in genes involved in nutrient-related metabolisms (e.g., nitrate and nitrite ammonification, Ton/Tol transport, etc.). On reefs further from the equator, microbes had more genes encoding chlorophyll biosynthesis and photosystems I/II. These results support the hypothesis that core microbiomes are determined by holobiont macroorganisms, and that those core taxa adapt to local conditions by selecting for advantageous metabolic genes.

Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence.

Holobionts are assemblages of microbial symbionts and their macrobial host. As extant representatives of some of the oldest macro-organisms, corals and algae are important for understanding how holobionts develop and interact with one another. Using untargeted metabolomics, we show that non-self interactions altered the coral metabolome more than self-interactions (i.e. different or same genus, respectively). Platelet activating factor (PAF) and Lyso-PAF, central inflammatory modulators in mammals, were major lipid components of the coral holobionts. When corals were damaged during competitive interactions with algae, PAF increased along with expression of the gene encoding Lyso-PAF acetyltransferase; the protein responsible for converting Lyso-PAF to PAF. This shows that self and non-self recognition among some of the oldest extant holobionts involve bioactive lipids identical to those in highly derived taxa like humans. This further strengthens the hypothesis that major players of the immune response evolved during the pre-Cambrian.

Mass spectral similarity for untargeted metabolomics data analysis of complex mixtures.

While in nucleotide sequencing, the analysis of DNA from complex mixtures of organisms is common, this is not yet true for mass spectrometric data analysis of complex mixtures. The comparative analyses of mass spectrometry data of microbial communities at the molecular level is difficult to perform, especially in the context of a host. The challenge does not lie in generating the mass spectrometry data, rather much of the difficulty falls in the realm of how to derive relevant information from this data. The informatics based techniques to visualize and organize datasets are well established for metagenome sequencing; however, due to the scarcity of informatics strategies in mass spectrometry, it is currently difficult to cross correlate two very different mass spectrometry data sets from microbial communities and their hosts. We highlight that molecular networking can be used as an organizational tool of tandem mass spectrometry data, automated database search for rapid identification of metabolites, and as a workflow to manage and compare mass spectrometry data from complex mixtures of organisms. To demonstrate this platform, we show data analysis from hard corals and a human lung associated with cystic fibrosis.

Reproductive natural history and successful juvenile propagation of the threatened Caribbean pillar coral Dendrogyra cylindrus.

BACKGROUND: The Caribbean pillar coral Dendrogyra cylindrus was recently listed as a threatened species under the United States Endangered Species Act. One of the major threats to this species is its low, virtually undetectable recruitment rate. To our knowledge, sexually-produced recruits have never been found in over 30 years of surveys of Caribbean reefs. Until recently, the reproductive behavior of D. cylindrus was uncharacterized, limiting efforts to study its early life history, identify population bottlenecks, and conduct outplanting projects with sexually-produced offspring. In Curaçao, we observed the spawning behavior of this species over three years and five lunar cycles. We collected gametes from spawning individuals on three occasions and attempted to rear larvae and primary polyp settlers. RESULTS: Here we describe successful fertilization methods for D. cylindrus and we document rapid embryonic development. We describe the successful propagation of embryos to the swimming larvae stage, the first settlement of larvae in the laboratory, and the survival of primary polyp settlers for over seven months. We show that spawning times are highly predictable from year to year relative to the lunar cycle and local sunset times. We use colony-level data to confirm that males begin spawning before females. We also provide the first reports of split-spawning across months in this species. CONCLUSIONS: Together, our findings of consistent spawning times, split-spawning, rapid embryonic development, and remarkable robustness of larvae and settlers now enable expanded research on the early life history and settlement ecology of D. cylindrus. This will help biologists to identify the population bottlenecks in nature that underlie low recruitment rates. Further, the settlement of D. cylindrus larvae in the laboratory now makes out-planting for restoration more feasible. Asynchronous spawning times and rapid embryonic development may have important consequences for population biology, connectivity, and management, by affecting fertilization dynamics and larval dispersal distances. We argue that a precautionary approach to conservation is warranted, given this species' peculiar life history traits and still-unresolved population structure. Overall, the natural history and husbandry contributions presented here should facilitate accelerated research and conservation of this threatened coral.

Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2-60 m) on a Caribbean reef.

BACKGROUND: Scleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef. RESULTS: The five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution ("shallow": A. humilis / A. agaricites and "deep": A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between "shallow" and "deep" host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes. CONCLUSIONS: Our findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths.

Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species.

When juveniles must tolerate harsh environments early in life, the disproportionate success of certain phenotypes across multiple early life stages will dramatically influence adult community composition and dynamics. In many species, large offspring have a higher tolerance for stressful environments than do smaller conspecifics (parental effects). However, we have a poor understanding of whether the benefits of increased parental investment carry over after juveniles escape harsh environments or progress to later life stages (latent effects). To investigate whether parental effects and latent effects interactively influence offspring success, we determined the degree to which latent effects of harsh abiotic conditions are mediated by offspring size in two stony coral species. Larvae of both species were sorted by size class and exposed to relatively high-temperature or low-salinity conditions. Survivorship was quantified for six days in these stressful environments, after which surviving larvae were placed in ambient conditions and evaluated for their ability to settle and metamorphose. We subsequently assessed long-term post-settlement survival of one species in its natural environment. Following existing theory, we expected that, within and between species, larger offspring would have a higher tolerance for harsh environmental conditions than smaller offspring. We found that large size did enhance offspring performance in each species. However, large offspring size within a species did not reduce the proportional, negative latent effects of harsh larval environments. Furthermore, the coral species that produces larger offspring was more, not less, prone to negative latent effects. We conclude that, within species, large offspring size does not increase resistance to latent effects. Comparing between species, we conclude that larger offspring size does not inherently confer greater robustness, and we instead propose that other life history characteristics such as larval duration better predict the tolerance of offspring to harsh and variable abiotic conditions. Additionally, when considering how stressful environments influence offspring performance, studies that only evaluate direct effects may miss crucial downstream (latent) effects on juveniles that have significant consequences for long-term population dynamics.

Survival and dispersal of turf algae and macroalgae consumed by herbivorous coral reef fishes.

The mechanisms by which algae disperse across space on coral reefs are poorly known. We investigated the ability of four common Caribbean herbivorous fish species to disperse viable algal fragments through consumption of macroalgae and subsequent defecation. Fragments of all major algal taxa (Phaeophyta, Rhodophyta, and Chlorophyta) were found in 98.7 % of the fecal droppings of all fish species; however, the ability to survive gut passage and reattach to a substrate differed between algal taxa. While survival and reattachment approached zero for Phaeophyta and Chlorophyta, 76.4 % of the fragments belonging to the group Rhodophyta (mostly species in the order Gelidiaceae) survived gut passage, and were able to grow and reattach to the substrate by forming new rhizoids. Our results thus show that Gelidid algal species are dispersed by swimming herbivores. While the relative contribution of this mechanism to overall algal dispersal and recruitment in a wider ecological context remains unknown, our findings illustrate a previously undescribed mechanism of algal dispersal on coral reefs which is analogous to the dispersal of terrestrial plants, plant fragments, and seeds via herbivore ingestion and defecation.

Non-native coral species dominate the fouling community on a semi-submersible platform in the southern Caribbean.

A coral community was examined on a semi-submersible platform that was moored at the leeward side of Curaçao, in the southern Caribbean, from August 2016 until August 2017. This community included several non-native or cryptogenic species. Among them were two scleractinian corals (Tubastraea coccinea and T. tagusensis) and two octocorals (Chromonephthea sp. and an unidentified Nephtheidae sp.). This is the first reported presence of T. tagusensis in the southern Caribbean, and the genus Chromonephthea in the Caribbean region. An ascidian, Perophora cf. regina, is also reported from the southern Caribbean for the first time, as well as a coral-associated vermetid gastropod, Petaloconchus sp., first recorded in the Caribbean in 2014. Lack of biofouling management could potentially harm indigenous marine fauna through the introduction of non-native species. Therefore monitoring communities associated with semi-submersible platforms is essential to track the presence and dispersal of non-native, potentially invasive species.

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae.

Competition between reef-building corals and benthic algae is of key importance for reef dynamics. These interactions occur on many spatial scales, ranging from chemical to regional. Using microprobes, 16S rDNA pyrosequencing and underwater surveys, we examined the interactions between the reef-building coral Montastraea annularis and four types of benthic algae. The macroalgae Dictyota bartayresiana and Halimeda opuntia, as well as a mixed consortium of turf algae, caused hypoxia on the adjacent coral tissue. Turf algae were also associated with major shifts in the bacterial communities at the interaction zones, including more pathogens and virulence genes. In contrast to turf algae, interactions with crustose coralline algae (CCA) and M. annularis did not appear to be antagonistic at any scale. These zones were not hypoxic, the microbes were not pathogen-like and the abundance of coral-CCA interactions was positively correlated with per cent coral cover. We propose a model in which fleshy algae (i.e. some species of turf and fleshy macroalgae) alter benthic competition dynamics by stimulating bacterial respiration and promoting invasion of virulent bacteria on corals. This gives fleshy algae a competitive advantage over corals when human activities, such as overfishing and eutrophication, remove controls on algal abundance. Together, these results demonstrate the intricate connections and mechanisms that structure coral reefs.