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Competition for limited space is an important driver of benthic community structure on coral reefs. Studies of coral-algae and coral-sponge interactions often show competitive dominance of algae and sponges over corals, but little is known about the outcomes when these groups compete in a multispecies context. Multispecies competition is increasingly common on Caribbean coral reefs as environmental degradation drives loss of reef-building corals and proliferation of alternative organisms such as algae and sponges. New methods are needed to understand multispecies competition, whose outcomes can differ widely from pairwise competition and range from coexistence to exclusion. In this study, we used 3D photogrammetry and image analyses to compare pairwise and multispecies competition on reefs in the US Virgin Islands. Sponges (Desmapsamma anchorata, Aplysina cauliformis) and macroalgae (Lobophora variegata) were attached to coral (Porites astreoides) and arranged to simulate multispecies (coral-sponge-algae) and pairwise (coral-sponge, coral-algae) competition. Photogrammetric 3D models were produced to measure surface area change of coral and sponges, and photographs were analyzed to measure sponge-coral, algae-coral, and algae-sponge overgrowth. Coral lost more surface area and was overgrown more rapidly by the spongeD. anchoratain multispecies treatments, when the sponge was also in contact with algae. Algae contact may confer a competitive advantage to the spongeD. anchorata,but not toA. cauliformis, underscoring the species-specificity of these interactions. This first application of photogrammetry to study competition showed meaningful losses of living coral that, combined with significant overgrowths by competitors detected from image analyses, exposed a novel outcome of multispecies competition.

Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (, We investigated the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. The microbiomes of Cliona delitrix were structured by the interplay between geographic, environmental, and host factors. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.

Many studies have evaluated the impacts of hurricanes on coral communities, but far less is known about impacts, recovery, and resilience of sponge communities to these extreme events. In September 2017, St. Thomas, U.S. Virgin Islands, was impacted by two Category 5 hurricanes within 2 weeks: Hurricanes Irma and Maria. Such extreme events occurring in such rapid succession are virtually unprecedented. Pre-hurricane (2015, 2016) surveys of permanent transects at six sites around St. Thomas were compared with those at 10 weeks post-hurricanes (December 2017) to evaluate storm impacts on sponges and on benthic coral reef constituents. These surveys also established a baseline for evaluating future recovery. Percent cover of sponges declined by 24.9% post-hurricanes. In contrast, sponge density increased by 43.9% from 2015 to 2016 and declined slightly after the hurricanes. Overall sponge volume did not vary over time, and whereas sponge diversity was similar in 2015 and 2016, it increased post-hurricanes. Sponge morphologies were differentially affected by the hurricanes; the proportion of upright sponges declined by 36.9%, while there was a 24.4% increase in encrusting sponges. Coral and macroalgal cover did not change significantly over the sampling period, while percent cover of epilithic algae increased and non-living substrata decreased from 2015 to 2016 but did not change further post-hurricanes. At all sites, recruitment and/or regrowth of sponges was observed within 10 weeks post-hurricanes, indicating potential resilience in Caribbean sponge communities. Whether these sponge communities return to pre-hurricane conditions and how long that will take remains to be seen.

Disease outbreaks have caused significant declines of keystone coral species. While forecasting disease outbreaks based on environmental factors has progressed, we still lack a comparative understanding of susceptibility among coral species that would help predict disease impacts on coral communities. The present study compared the phenotypic and microbial responses of seven Caribbean coral species with diverse life-history strategies after exposure to white plague disease. Disease incidence and lesion progression rates were evaluated over a seven-day exposure. Coral microbiomes were sampled after lesion appearance or at the end of the experiment if no disease signs appeared. A spectrum of disease susceptibility was observed among the coral species that corresponded to microbial dysbiosis. This dysbiosis promotes greater disease susceptiblity in coral perhaps through different tolerant thresholds for change in the microbiome. The different disease susceptibility can affect coral’s ecological function and ultimately shape reef ecosystems., MacKnight et al. compared the phenotypic and microbial responses of seven Caribbean coral species with diverse life-history strategies after exposure to white plague disease. The different species exhibited a spectrum of disease susceptibility and associated mortality that corresponded with their tolerances to microbial change, indicating that coral disease and microbial dysbiosis may ultimately shape reef ecosystems.

The recent increase in abundance of coral-excavating sponges is a threat to the health of coral reefs. However, the distribution and growth of these sponges are poorly documented on high latitude reefs where corals live in marginal environmental conditions. In this study, we characterize the current trends of space occupation of Cliona delitrix on high latitude reefs (26°N) in southeast Florida. C. delitrix densities were significantly higher on the deepest habitat of this reef tract (the outer reef) in response to a higher availability of coral substratum. Sponge growth rates increased with depth, and in relation to presence of tunicates and absence of macroalgae living in the sponge–coral interaction band. Conversely, coral tissue loss was similar between habitats, regardless of the fouling organisms present in the band between sponge and coral. On high latitude reefs, C. delitrix preferred massive scleractinian coral species as substratum, similar to tropical reefs, but its inclination for specific coral species varied. The outer reef sites (deepest habitat) are most vulnerable to C. delitrix colonization. Reef habitats with higher coral densities and more available dead coral may continue to suffer the greatest levels of sponge bioerosion.

As coral cover has declined on Caribbean reefs, space has become occupied by other benthic taxa, including sponges, which may affect the recruitment of new corals, thereby affecting the ability of reefs to recover to coral-dominated states. Sponges may inhibit coral recruitment by pre-empting potential recruitment space, overgrowing recruits, or through allelopathy. This study examined coral recruitment across six coral reef sites surrounding St. Thomas, US Virgin Islands, and the impact of one species of sponge and the sponge community as a whole on coral recruitment. To test the effect of a single species of sponge on coral recruitment, fragments of living or non-living Aplysina cauliformis were attached to terracotta recruitment tiles and deployed at all six sites, along with unoccupied tiles as controls. At two of the sites, a community-level experiment consisted of deploying recruitment tiles in 1 m2 plots that were either cleared of the entire sponge community or control plots where no sponges were removed. Recruitment rates showed a consistent difference among sites over multiple years and experiments. Results of the species-specific experiment showed that the proximity of live or dead A. cauliformis did not affect coral recruitment. However, results of the community-level experiment found greater coral recruitment rates in plots cleared of sponges, suggesting that the presence of the sponge community negatively affected coral recruitment. This study is one of the first to experimentally test and find a significant impact of sponges on coral recruitment, and highlights the need for additional research in this area.

Siderastrea siderea is one of the most abundant corals at high latitude shallow sites along the Florida Reef Tract (25°–27°N). This species is able to tolerate wide seawater temperature fluctuations and sedimentation stress, but its reproductive status at high latitudes and under marginal environmental conditions is poorly understood. The objectives of this study were to evaluate the reproductive potential of S. siderea along a latitudinal gradient (25°–27°N) and to determine if sexual maturity occurs in small (

Some excavating sponges are strong competitors for space on coral reefs, able to kill live coral tissue and to overgrow entire coral colonies. Stony corals with excavating sponges can die or become dislodged. To date no restoration efforts to eliminate excavating sponges from live corals have been considered. In this study we examined the effect and remedial potential of removal of the excavating sponge, Cliona delitrix, by monitoring tissue loss of the stony coral Montastrea cavernosa. Thirty-three corals colonized by the sponge were used: 11 as controls, and 22 as treatments in which sponges were removed using hammer and chisel. After sponge removal, resultant cavities in the coral skeletons were filled with common cement or epoxy. Standardized photos of each coral were taken immediately after sponge removal, and at 6 and 12 months afterwards. Results were similar between fill materials and showed a reduction in coral tissue loss in colonies where the sponge was removed. This study demonstrates that eliminating the bioeroding sponge enables potential recovery in affected stony corals after a year. However, 36% of experimental corals showed renewed presence of C. delitrix on the colony surface within a year after removal, demonstrating the extraordinary ability of this sponge to colonize corals. Although the technique used in this study is applicable to enhance modern coral restoration practices by slowing tissue loss, this method is costly, elaborate, and not suitable at a reef-wide scale. Further restoration alternatives and long-term measures to prevent over-colonization of corals by excavating sponges are encouraged.

Changes in coral-sponge interactions can alter reef accretion/erosion balance and are important to predict trends on current algal-dominated Caribbean reefs. Although sponge abundance is increasing on some coral reefs, we lack information on how shifts from corals to bioeroding sponges occur, and how environmental factors such as anomalous seawater temperatures and consequent coral bleaching and mortality influence these shifts. A state transition model (Markov chain) was developed to evaluate the response of coral excavating sponges (Cliona delitrix Pang 1973) after coral bleaching events. To understand possible outcomes of the sponge-coral interaction and build the descriptive model, sponge-corals were monitored in San Andres Island, Colombia (2004-2011) and Fort Lauderdale, Florida (2012-2013). To run the model and determine possible shifts from corals to excavating sponges, 217 coral colonies were monitored over 10 years (2000-2010) in Fort Lauderdale, Florida, and validated with data from 2011 to 2015. To compare and test its scalability, the model was also run with 271 coral colonies monitored in St. Croix, U.S. Virgin Islands over 11 years (2004-2011), and validated with data from 2012-2015. Projections and sensitivity analyses confirmed coral recruitment to be key for coral persistence. Excavating sponge abundance increased in both Fort Lauderdale and St. Croix reefs after a regional mass bleaching event in 2005. The increase was more drastic in St. Croix than in Fort Lauderdale, where 25% of the healthy corals that deteriorated were overtaken by excavating sponges. Projections over 100 years suggested successive events of moderate coral mortality could shift algae-coral dominated reefs into algae-sponge dominated. The success of excavating sponges depended of the intensity of coral bleaching and consequent coral mortality. Thus, the proportion of Cliona delitrix excavating sponges is a sensitive indicator for the intensity and frequency of recent disturbance on Caribbean coral reefs. This article is protected by copyright. All rights reserved.

Thomas, Torsten ... et al.-- 12 pages, 10 figures, additional information https://dx.doi.org/10.1038/ncomms11870, Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host–microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world’s oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions, T.T. and N.S.W. were funded through Australian Research Council Future Fellowships FT140100197 and FT120100480, respectively. S.L.L. and P.M.E. were funded by the Spanish Government project MARSYMBIOMICS CTM2013-43287-P. R.C. was funded by the Portuguese Foundation for Science and Technology through the Investigator Grant IF/01076/2014 and the project UID/Multi/04326/2013. C.G.E. and R.W.T. were supported by grants from the US National Science Foundation (DEB-0829986 and DEB-1208340). A.C.-F. was supported by the UNESCO L’Oréal Fellowship for Young Women in Science. U.H. and L.M.S. received funding from the EU- FP7 Program (KBBE.2012.3.2-01; grant no. 311932; SeaBioTech). J.M.M. was supported by the French Laboratory of Excellence Project ‘TULIP’ (ANR-10-LABX-41; ANR-11-IDEX-002-02) and by a Region Midi-Pyrénées Project (CNRS 121090)

The Caribbean encrusting and excavating sponges Cliona aprica, C. caribbaea, C. delitrix and C. tenuis (Porifera, Hadromerida, Clionaidae), aggresively undermine and displace live coral tissue. At San Andrés island and Islas del Rosario (Colombian Caribbean), in all 145 observed cases of direct contact of the sponges C. aprica, C. caribbaea and C. tenuis with 17 coral species, corals showed unhealthy signs in their tissue. It was also noticed that the surface of these sponges is colonized by few organisms and that they are rarely preyed upon. To establish the possible use of chemical substances by these sponges in competition for space with corals (allelopathy), as inhibitors of larval settlement (antifouling), and as feeding deterrents against generalist fish (antipredatory), the activity of crude organic extracts was experimentally evaluated. Extracts were prepared in methanol and 1:2 metanol:dichloromethane and incorporated in experimental media at the natural concentration within the sponges. Using an unpublished method being developed by J. Pawlik (University of North Caroline at Wilmington) and M. Ilan (Tel Aviv University), PhytagelTM disks with crude extracts of each of the four sponge species, placed on the coral Montastrea cavernosa, produced a greater degree of polyp mortality than control gels without extract. Gels with extracts of the sponges C. aprica and C. caribbaea + C. tenuis, served in Petri dishes and used as substratum in the field, inhibited significantly the settlement of fouling organisms, in comparison to control gels. In laboratory trials, wheat flour pellets with extracts C. delitrix and C. caribbaea + C. tenuis were significantly rejected by the omnivore reef damselfish, Stegastes partitus, whereas pellets with extract of C. aprica did not deter feeding. These results suggest that substances present in the crude organic extracts of these sponges may be responsible in part for their ability to compete for reef substrata and to defend themselves from potential aggressors.

The Caribbean sponge Cliona delitrix is among the strongest reef space competitors; it is able to overpower entire coral heads by undermining coral polyps. It has become abundant in reefs exposed to organic pollution, such as San Andres Island, Colombia, SW Caribbean. Forty-four sponge-colonized coral colonies were followed-up for 13 months to establish the circumstances and the speed at which this sponge advances laterally into live coral tissue and the coral tissue retreats. Cliona delitrix presence and abundance was recorded at seven stations to interpret current reef space and coral species colonization trends. The spread of C. delitrix on a coral colony was preceded by a band of dead coral a few millimeters to several centimeters wide. However, the sponge was directly responsible for coral death only when live coral tissue was within about 2 cm distance; coral death became sponge advance-independent at greater distances, being indirectly dependent on other conditions that tend to accelerate its retreat. Cliona delitrix advanced fastest into recently killed clean coral calices; however, sponge spread slowed down when these became colonized by algae. The lateral advance of C. delitrix was slower than other Cliona spp. encrusting excavating sponges, probably owing to the greater depth of its excavation into the substratum. Cliona delitrix prefers elevated portions of massive corals, apparently settling on recently dead areas. It currently inhabits 6–9% of colonies in reefs bordering San Andres. It was found more frequently in Siderastrea siderea (the most abundant local massive coral), which is apparently more susceptible to tissue mortality than other corals. Current massive coral mortality caused by C. delitrix could initially change the relative proportions of coral species and in the long-term favor foliose and branching corals.

The Caribbean encrusting and excavating sponge Cliona tenuis successfully competes for space with reef corals by undermining, killing, and displacing live coral tissue at rates of up to 20 cm per year. The crude extract from this sponge, along with the more polar partitions, kills coral tissue and lowers the photosynthetic potential of coral zooxanthellae. We used a bioassay-guided fractionation of the extract to identify the compound(s) responsible. The crude extract, the aqueous partition, and compound 1, herein named clionapyrrolidine A [(-)-(5S)-2-imino-1-methylpyrrolidine-5-carboxylic acid], when incorporated into gels at close to natural volumetric concentrations, killed coral tissue when brought into forced contact with live coral for periods of 1-4 days. This is the first report of a pure chemical produced by a sponge that kills coral tissue upon direct contact. The results are consistent with the localized coral death that occurs when C. tenuis-colonized coral fragments are thrown forcibly against live coral during storms. However, healed C. tenuis fragments placed directly onto live coral were killed readily by coral defenses, and fragments placed in close proximity to coral did not have any effect on the adjacent coral tissue. Solutions of clionapyrrolidine A in sea water were only slightly toxic against live coral. Hence, the coral death naturally brought about by C. tenuis when undermining live coral does not occur through external release of allelochemicals; below-polyp mechanisms must be explored further. N-acetylhomoagmatine (2), originally isolated from Cliona celata from the Northeastern Atlantic, was also assayed for comparison purposes because of its structural similarity to siphonodictidine, a toxic compound produced by a coral excavating sponge of the genus Aka. The lack of activity of N-acetylhomoagmatine at close to natural concentrations seems to indicate that the guanidine moiety, which is also present in siphonodictidine, is not a sufficiently strong structural motif for activity against corals.

14 páginas, 2 tablas, 9 figuras, Cliona delitrix is one of the most abundant and destructive coral-excavating sponges on Caribbean reefs. However, basic aspects of its reproductive biology, which largely determine the species propagation potential, remain unknown. A 2-year study (October 2009 to September 2011) was conducted to determine the reproductive cycle and gametogenesis of a C. delitrix population located in a shallow reef in Florida, USA. Mesohyl tissue collected from randomly chosen and tagged sponge individuals was sampled one to several times a month, and analysed by light and transmission electron microscopy (TEM). Cliona delitrix is oviparous and gonochoric, except for a few simultaneous hermaphroditic individuals. The C. delitrix reproductive cycle in Florida is from April to December, and is triggered by an increase in seawater temperature to 258C. Oogenesis and spermatogenesis were asynchronous among individuals; with different cohorts of oocytes co-occurring in females, and spermatic cysts in males. Granulose cells acted as nurse cells, contributing to the growth and maturation of both female and male gametes. Spawning of gametes was not always synchronized with full moon phase. Unlike most other oviparous sponges, the reproductive cycle of C. delitrix is versatile and includes multiple spawning events during the summer of each year. This characteristic maximizes sponge propagation on coral reefs during the warmer months of the year, particularly when thermal stress induces coral mortality. This aspect, combined with its success on polluted areas, make C. delitrix a suitable bioindicator of coral reef health., This work was funded through the UNESCO-L’Oréal Fellowship for Young Women in Science, the PhD scholarship program from Colombian Science and Technology Department (COLCIENCIAS), Billfish Tournament Scholarship, the Broward Women Association Scholarship, and the President’s Faculty Research and Development Grant to JVL and AC-F by Nova Southeastern University.

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species-specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida-Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida-Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change.

Background: Demosponges are challenging for phylogenetic systematics because of their plastic and relatively simple morphologies and many deep divergences between major clades. To improve understanding of the phylogenetic relationships within Demospongiae, we sequenced and analyzed seven nuclear housekeeping genes involved in a variety of cellular functions from a diverse group of sponges. Methodology/Principal Findings: We generated data from each of the four sponge classes (i.e., Calcarea, Demospongiae, Hexactinellida, and Homoscleromorpha), but focused on family-level relationships within demosponges. With data for 21 newly sampled families, our Maximum Likelihood and Bayesian-based approaches recovered previously phylogenetically defined taxa: Keratosa p , Myxospongiae p , Spongillida p , Haploscleromorpha p (the marine haplosclerids) and Democlavia p .W e found conflicting results concerning the relationships of Keratosa p and Myxospongiae p to the remaining demosponges, but our results strongly supported a clade of Haploscleromorpha p +Spongillida p +Democlavia p . In contrast to hypotheses based on mitochondrial genome and ribosomal data, nuclear housekeeping gene data suggested that freshwater sponges (Spongillida p ) are sister to Haploscleromorpha p rather than part of Democlavia p . Within Keratosa p , we found equivocal results as to the monophyly of Dictyoceratida. Within Myxospongiae p , Chondrosida and Verongida were monophyletic. A wellsupported clade within Democlavia p , Tetractinellida p , composed of all sampled members of Astrophorina and Spirophorina (including the only lithistid in our analysis), was consistently revealed as the sister group to all other members of Democlavia p . Within Tetractinellida p , we did not recover monophyletic Astrophorina or Spirophorina. Our results also reaffirmed the monophyly of order Poecilosclerida (excluding Desmacellidae and Raspailiidae), and polyphyly of Hadromerida and Halichondrida. Conclusions/Significance: These results, using an independent nuclear gene set, confirmed many hypotheses based on ribosomal and/or mitochondrial genes, and they also identified clades with low statistical support or clades that conflicted with traditional morphological classification. Our results will serve as a basis for future exploration of these outstanding questions using more taxon- and gene-rich datasets.

It is known that the encrusting and excavating Caribbean sponge Cliona delitrix may increase its abundance near sources of sewage. To ascertain whether its current conspicuousness in leeward reefs of San Andrés Island (SW Caribbean, Colombia) is related to organic pollution from local raw sewage discharges, quantitative data on density and cover of this sponge and other benthic components was obtained from belt and line transects at seven stations along the shallow (5-10 m deep) terrace. Coral mucus was sampled to quantify Escherichia coli bacteria, as an approximate indicator of sewage plume influence on benthic biota. A negative multiplicative regression between amount of E. coli in coral mucus and distance from the main raw sewage outlet demonstrated the domestic-wastes origin of the bacteria. Whereas significant E. coli counts occurred only up to 1-2 km from sewage sources, overall sewage influence may extend further as moderate C. delitrix abundances occurred throughout the West shallow terrace of San Andrés, apparently associated to the overall nutrient enrichment from sewage. C. delitrix abundances were lower in the Southwest, farthest from sewage influence, and generally increased towards sewage sources, but decreased near the main sewage outlet. Close to sewage sources, any positive effect on the sponge brought about by the increase in suspended organic matter is probably outweighed by the negative effect that excessive sedimentation has on the sponge itself, and on the quantity and quality of substratum available for settlement.