Lionfish that live in mesophotic reef environments (30 to 150 m depth) are potentially undermining invasive species management efforts on shallower reefs. Understanding the behavior of lionfish in these deeper habitats is critical to characterizing the impacts of mesophotic lionfish on their home reefs as well as on adjacent shallow reefs. In this study, we combined long term monitoring and acoustic telemetry data to characterize the density and behavior of lionfish on mesophotic reefs in the United States Virgin Islands (USVI). Across 10 years of monitoring, significantly higher densities of lionfish were observed on mesophotic reefs as compared to nearshore and offshore reefs in the USVI. We tagged lionfish at two mesophotic reef sites in the territory and found that most of them were resident to the mesophotic areas and had comparable home range sizes to those reported on adjacent shallow coral reefs. We found that a majority of fish displayed crepuscular diel activity patterns, but some individuals had unusually high activity during daytime periods as compared to previous studies of the species. There was variability within the crepuscular activity pattern, with some individuals being more active in the morning and others in the evening crepuscular periods. The persistence of lionfish in mesophotic reef habitats in the USVI suggests that they could be impacting these environments, and future studies and management efforts should focus on identifying, quantifying, and mitigating those effects.

The function and stability of mesophotic coral ecosystems (MCEs) have been extensively studied in recent years. These deep reefs are characterized by local physical processes, particularly the steep gradient in irradiance with increasing depth, and their impact on trophic resources. Mesophotic reefs exhibit distinct zonation patterns that segregate shallow reef biodiversity from ecologically unique deeper communities of endemic species. While mesophotic reefs are hypothesized as relatively stable refuges from anthropogenic stressors and a potential seed bank for degraded shallow reefs, these are site-specific features, if they occur at all. Mesophotic reefs are now known to be susceptible to many of the same stressors that are degrading shallow reefs, suggesting that they require their own specific conservation and management strategies.

In warm oligotrophic waters, photosymbiotic coral can flourish across a wide depth range (0–170+ m), extending to depths where light attenuates to ~0.1% of surface values. Conventional wisdom has long assumed that mixotrophic corals must increasingly rely on heterotrophy as the ambient light available to drive photosynthesis decreases with depth. However, evidence challenging this traditional dogma has been accumulating in recent years. Although some evidence suggests that some depth-generalist coral species likely increase their reliance on heterotrophy with increasing depth, there is growing evidence that other species do not. Analysis of bulk stable isotopes (δ13C and δ15N) applied to photosymbiotic corals has been used in several ways to infer their trophic ecology and their relative dependence on symbiont photosynthesis versus heterotrophic feeding. However, metrics based on bulk tissue δ13C and δ15N values are subject to considerable uncertainty due to the multiple factors that can affect their values independent of trophic ecology. These competing factors can be quite challenging to disentangle and have led to inconsistent results and conclusions regarding trends in coral heterotrophy with depth. The evidence to date suggests no uniform trophic pattern with increasing depth or decreasing light. Different corals appear to function differently, which is not surprising given their phylogenetic diversity.

Coral reefs are globally important ecosystems with high species diversity at both the macro and micro scales. In recent years, coral reefs have been heavily impacted by anthropogenic and natural stressors, including emerging diseases. Many of these diseases have been identified in reef-building corals, but other invertebrate taxa, such as soft corals, are increasingly at risk. This study focuses on a hybrid species complex within soft corals of the genus Sinularia , which dominate the shallow reefs of Guam, and the broader Indo-Pacific. These soft corals exhibit varying levels of disease susceptibility to Sinularia tissue loss disease (STLD), a chronic wasting disease. In the current study, we used next-generation amplicon sequencing of prokaryotic and eukaryotic communities within these soft corals to characterize their microbiomes, and develop a better understanding of the etiology of STLD. There were differences in specific ASVs across the microbiomes of healthy colonies of Sinularia maxima, Sinularia polydactyla and their hybrid ( S. maxima x S. polydactyla) . There was also a decline in the relative abundance of putatively beneficial symbionts (Symbiodinaceae and Endozoicomonas ) in STLD-affected soft corals, but no consistent shifts towards a specific microbial community associated with STLD. The soft coral microbiomes also contained a high relative abundance of ASVs typically associated with terrestrial runoff. Our results suggest that the STLD phenotype may be due to a combination of factors, including infection by a yet unknown etiologic agent, shifts in putatively beneficial symbionts, and anthropogenic impacts on this shallow nearshore reef.

Mesophotic coral reefs are estimated to represent up to 80% of the total areal coverage for coral reefs worldwide. Quantifying mesophotic coral reef community structure and function, at multiple spatial and temporal scales, and the ability to monitor these attributes repeatedly and accurately, is an ecological priority. Recent discussions on the relative merits of remotely operated vehicles and autonomous underwater vehicles (ROVs and AUVs, respectively) versus the use of technical divers using quadrats or photoquadrats to obtain quantitative imagery undervalues the distinct and important complimentary roles that both approaches bring to the study of mesophotic coral reefs. However, all platforms must adhere to fundamental photogrammetry principles to accomplish the goal of accurate and repeatable surveys of coral reefs. Here we show that quantifying the projected surface area of sponge populations for a tropical coral reef on Puerto Rico using ROV imagery, not originally collected for ecological characterizations, requires specific screening guidelines to ensure the images are orthogonal and processed to obtain orthorectified images for the quantification of benthic communities. This is required to minimize multiple sources of error that could confound quantitative estimates of percent cover, biomass, and/or abundance of benthic taxa on shallow and mesophotic coral reefs using plot, or plotless, designs.

Fundamental to holobiont biology is recognising how variation in microbial composition and function relates to host phenotypic variation. Sponges often exhibit considerable phenotypic plasticity and also harbour dense microbial communities that function to protect and nourish hosts. One of the most prominent sponge genera on Caribbean coral reefs is Agelas. Using a comprehensive set of morphological (growth form, spicule), chemical and molecular data on 13 recognised species of Agelas in the Caribbean basin, we were able to define only five species (=clades) and found that many morphospecies designations were incongruent with phylogenomic and population genetic analyses. Microbial communities were also strongly differentiated between phylogenetic species, showing little evidence of cryptic divergence and relatively low correlation with morphospecies assignment. Metagenomic analyses also showed strong correspondence to phylogenetic species, and to a lesser extent, geographical and morphological characters. Surprisingly, the variation in secondary metabolites produced by sponge holobionts was explained by geography and morphospecies assignment, in addition to phylogenetic species, and covaried significantly with a subset of microbial symbionts. Spicule characteristics were highly plastic, under greater impact from geographical location than phylogeny. Our results suggest that while phenotypic plasticity is rampant in Agelas, morphological differences within phylogenetic species affect functionally important ecological traits, including the composition of the symbiotic microbial communities and metabolomic profiles.

On Caribbean coral reefs, sponges are important members of the benthic community and have an important role in consuming particulate organic matter (POM) and dissolved organic matter (DOM), with the subsequent production of detritus that is then shunted into a process now referred to as the "sponge-loop." An emergent species of sponge commonly found on Caribbean coral reefs, Agelas tubulata, increases in size and growth rate from shallow (< 30 m) to mesophotic depths (30-150 m) on Grand Cayman Island. A. tubulata depends largely on heterotrophy across shallow to mesophotic depths and has been shown to utilize detritus on shallow reefs. However, detritus production by A. tubulata on shallow and mesophotic coral reefs has not been previously reported. Here we show, using flow cytometry, that sponge detritus includes a previously unquantified component, phytodetritus. Sponge phytodetritus production was shown experimentally to be greater in sponges from mesophotic depths compared to sponges from shallow coral reefs. Additionally, the size range of this phytodetritus corresponds to the size range of autotrophic picoplankton, primarily prochlorophytes, known to be an important food source for filter-feeding sponges. Given the known lability of phytodetritus, compared to other more recalcitrant components of the detrital pool, its role in the food web of mesophotic communities combined with the increased availability of live POM, may be an underappreciated component of mesophotic community carbon and nitrogen flow.

Sponges in the genus Agelas produce a diversity of bromopyrrole alkaloid secondary metabolites, some of which are known to inhibit predators and pathogens. Selective pressures on sponges to produce chemical defenses vary in time and space, often resulting in differences in the production of secondary metabolites. To characterize intraspecific variation in these compounds, we generated metabolomic profiles of the Caribbean sponge A. tubulata across spatial gradients, including multiple sites in Belize and Grand Cayman, and depths ranging from 15 to 61 m in Grand Cayman. Samples were also analyzed from a reciprocal transplant experiment across shallow (22 m) to mesophotic (61 m) reefs. We found quantitative, but not qualitative, differences in metabolite profiles across sites and depths, with 9 metabolites contributing to that variation. In addition, transplanting sponges across depths resulted in significant changes in concentrations of the metabolite sceptrin. Sponge extracts exhibited antibacterial activity against a panel of marine and human pathogens. Multiple regression analyses showed that different metabolites were associated with antibacterial activity against different pathogens. The strongest compound-specific relationship was a negative effect of oroidin on the growth of Serratia marcescens, and purified oroidin was found to inhibit S. marcescens growth in a dose-dependent manner. Overall, A. tubulata exhibits intraspecific variability in the production of antibacterial secondary metabolites across sites and depths that signals selective responses to its environment. Given the current increase in sponge densities, and incidence of disease on coral reefs, these data have implications for disease resistance and resilience of sponges in the Anthropocene.

Studies on the trophic ecology of scleractinian corals often include stable isotope analyses of tissue and symbiont carbon and nitrogen. These approaches have provided critical insights into the trophic sources and sinks that are essential to understanding larger-scale carbon and nitrogen budgets on coral reefs. While stable isotopes have identified most shallow water (<30 m) corals as mixotrophic, with variable dependencies on autotrophic versus heterotrophic resources, corals in the mesophotic zone (~30–150 m) transition to heterotrophy with increasing depth because of decreased photosynthetic productivity. Recently, these interpretations of the stable isotope data to distinguish between autotrophy and heterotrophy have been criticized because they are confounded by increased nutrients, reverse translocation of photosynthate, and changes in irradiance that do not influence photosynthate translocation. Here we critically examine the studies that support these criticisms and show that they are contextually not relevant to interpreting the transition to heterotrophy in corals from shallow to mesophotic depths. Additionally, new data and a re-analysis of previously published data show that additional information (e.g., skeletal isotopic analysis) improves the interpretation of bulk stable isotope data in determining when a transition from primary dependence on autotrophy to heterotrophy occurs in scleractinian corals.

Mesophotic coral reef ecosystems (MCEs) are characterized by gradients in irradiance, temperature and trophic resources. As depth increases on Caribbean mesophotic reefs, particulate organic matter increases while dissolved organic matter decreases, and the increase in particulate organic matter is directly related to the increase in sponge abundances and growth rates on MCEs. To further understand the trophic ecology of sponges, changes in microbiome composition and function, stable isotopic composition and proximate biochemical composition of 4 Caribbean reef sponges (Amphimedon compressa, Agelas tubulata, Plakortis angulospiculatus and Xestospongia muta) were quantified along a shallow to mesophotic depth gradient on Grand Cayman Island. Increases in δ15N for all sponges were observed as depth increased, indicating an increasing reliance on heterotrophic food resources. Species-specific changes in symbiotic microbial community composition were also observed as depth increased, and the predicted functional genes associated with nitrogen and carbon cycling showed species-specific changes between depths. Regardless of species-specific changes in microbiome community structure or function, or whether sponges were classified as high microbial or low microbial abundance, sponges increased their consumption of particulate organic matter with increasing depth into the lower mesophotic zone.

Sponges are increasingly recognized as an ecologically important taxon on coral reefs, representing significant biomass and biodiversity where sponges have replaced scleractinian corals. Most sponge species can be divided into two symbiotic states based on symbiont community structure and abundance (i.e., the microbiome), and are characterized as high microbial abundance (HMA) or low microbial abundance (LMA) sponges. Across the Caribbean, sponge species of the HMA or LMA symbiotic states differ in metabolic capacity, as well as their trophic ecology. A metagenetic analysis of symbiont 16 S rRNA and metagenomes showed that HMA sponge microbiomes are more functionally diverse than LMA microbiomes, offer greater metabolic functional capacity and redundancy, and encode for the biosynthesis of secondary metabolites. Stable isotope analyses showed that HMA and LMA sponges primarily consume dissolved organic matter (DOM) derived from external autotrophic sources, or live particulate organic matter (POM) in the form of bacterioplankton, respectively, resulting in a low degree of resource competition between these symbiont states. As many coral reefs have undergone phase shifts from coral- to macroalgal-dominated reefs, the role of DOM, and the potential for future declines in POM due to decreased picoplankton productivity, may result in an increased abundance of chemically defended HMA sponges on tropical coral reefs.

Symbiotic microbial communities of sponges serve critical functions that have shaped the evolution of reef ecosystems since their origins. Symbiont abundance varies tremendously among sponges, with many species classified as either low microbial abundance (LMA) or high microbial abundance (HMA), but the evolutionary dynamics of these symbiotic states remain unknown. This study examines the LMA/HMA dichotomy across an exhaustive sampling of Caribbean sponge biodiversity and predicts that the LMA symbiotic state is the ancestral state among sponges. Conversely, HMA symbioses, consisting of more specialized microorganisms, have evolved multiple times by recruiting similar assemblages, mostly since the rise of scleractinian-dominated reefs. Additionally, HMA symbioses show stronger signals of phylosymbiosis and cophylogeny, consistent with stronger co-evolutionary interaction in these complex holobionts. These results indicate that HMA holobionts are characterized by increased endemism, metabolic dependence and chemical defences. The selective forces driving these patterns may include the concurrent increase in dissolved organic matter in reef ecosystems or the diversification of spongivorous fishes.

Sponges are a crucial component of Caribbean coral reef ecosystem structure and function. In the Caribbean, many sponges show a predictable increase in percent cover or abundance as depth increases from shallow (< 30 m) to mesophotic (30-150 m) depths. Given that sponge abundances are predicted to increase in the Caribbean as coral cover declines, understanding ecological factors that control their distribution is critical. Here we assess if sponge cover increases as depth increases into the mesophotic zone for three common Caribbean reef sponges, Xestospongia muta, Agelas tubulata, and Plakortis angulospiculatus, and use stable isotope analyses to determine whether shifts in trophic resource utilization along a shallow to mesophotic gradient occurred. Ecological surveys show that all target sponges significantly increase in percent cover as depth increases. Using bulk stable isotope analysis, we show that as depth increases there are increases in the delta C-13 and delta N-15 values, reflecting that all sponges consumed more heterotrophic picoplankton, with low C:N ratios in the mesophotic zone. However, compound-specific isotope analysis of amino acids (CSIA-AA) shows that there are species-specific increases in delta C-13(AA) and delta N-15(AA) values. Xestospongia muta and P. angulospiculatus showed a reduced reliance on photoautotrophic resources as depth increased, while A. tubulata appears to rely on heterotrophy at all depths. The delta C-13(AA) and delta N-15(AA) values of these sponges also reflect species-specific patterns of host utilization of both POM and dissolved organic matter (DOM), its subsequent re-synthesis, and translocation, by their microbiomes.

Abstract While the effects of irradiance on coral productivity are well known, corals along a shallow to mesophotic depth gradient (10–100 m) experience incident irradiances determined by the optical properties of the water column, coral morphology, and reef topography. Modeling of productivity (i.e., carbon fixation) using empirical data shows that hemispherical colonies photosynthetically fix significantly greater amounts of carbon across all depths, and throughout the day, compared with plating and branching morphologies. In addition, topography (i.e., substrate angle) further influences the rate of productivity of corals but does not change the hierarchy of coral morphologies relative to productivity. The differences in primary productivity for different coral morphologies are not, however, entirely consistent with the known ecological distributions of these coral morphotypes in the mesophotic zone as plating corals often become the dominant morphotype with increasing depth. Other colony‐specific features such as skeletal scattering of light, Symbiodiniaceae species, package effect, or tissue thickness contribute to the variability in the ecological distributions of morphotypes over the depth gradient and are captured in the metric known as the minimum quantum requirements. Coral morphology is a strong proximate cause for the observed differences in productivity, with secondary effects of reef topography on incident irradiances, and subsequently the community structure of mesophotic corals.

AbstractOn Caribbean coral reefs, sponges are important members of the benthic community and play multiple roles in ecosystem structure and function. They have an important role in benthic‐pelagic coupling, consuming particulate organic matter (POM) and dissolved organic matter (DOM) and in turn providing food in the form of sponge biomass or the release of detritus for a variety of coral reef organisms. Throughout the Caribbean, sponges show consistent increases in their abundance and growth rates as depth increases into the mesophotic zone (30–150 m). This has been hypothesized to be driven by bottom‐up forces, particularly the increased supply of nitrogen‐rich POM in mesophotic coral reef ecosystems (MCEs). Here, we tested the hypothesis that the sponge, Agelas tubulata, exhibits increased growth rates on MCEs relative to shallow reefs on Grand Cayman Island and that this is driven by bottom‐up forcing. We observed increased growth rates in mesophotic A. tubulata, compared with shallow conspecifics, despite variability in feeding on both POM and DOM. Mesophotic sponges, however, were consistently exposed to greater amounts of POM, which was seasonally variable unlike DOM. Changes in stable isotopic signatures, and higher feeding rates with increasing depth, were consistent with increasing rates of growth in sponges as depth increases. These observations support the hypothesis that mesophotic sponges have higher growth rates due to increased POM availability and consumption over time. The results of this study illustrate the crucial role that bottom‐up forcing has in the structuring of sponge communities on both shallow and mesophotic Caribbean coral reefs and the importance of POM as a source of nitrogen in sponge diets.

There is a critical need to quantify and monitor mesophotic coral reef community structure and function at multiple spatial and temporal scales. Because accessing these habitats is costly in terms of infrastructure and effort, often for a modest return in data, many investigators collect digital imagery using transect techniques from unmanned platforms. Specifically, remotely operated vehicles and autonomous underwater vehicles are used because they operate at deeper depths for extensive periods of time, can carry an array of oceanographic and imaging instruments, and can collect and archive extensive amounts of video and still imagery. However, substrate angle, camera angle, and vehicle position above the benthos creates varying degrees of error in the imagery due to parallax and geometric distortion. Photogrammetry conducted on 2D photographs from uncorrected 3D imagery can over- or under-estimate the percent cover, biomass estimates, and abundance of the benthic groups of interest. Here we illustrate these errors and emphasize the requirement for post-processing of imagery to ensure that these data can be used for valid quantitative ecological descriptions of mesophotic benthic communities in the future.

Mesophotic coral reefs, generally defined as deep reefs between 30 and 150 m, are found worldwide and are largely structured by changes in the underwater light field. Additionally, it is increasingly understood that reef-to-reef variability in topography, combined with quantitative and qualitative changes in the underwater light field with increasing depth, significantly influence the observed changes in coral distribution and abundance. Here, we take a modeling approach to examine the effects of the inherent optical properties of the water column on the irradiance that corals are exposed to along a shallow to mesophotic depth gradient. In particular, the roles of reef topography including horizontal, sloping and vertical substrates are quantified, as well as the differences between mounding, plating and branching colony morphologies. Downwelling irradiance and reef topography interact such that for a water mass of similar optical properties, the irradiance reaching the benthos varies significantly with topography (i.e. substrate angle). Coral morphology, however, is also a factor; model results show that isolated hemispherical colonies consistently ‘see’ greater incident irradiances across depths, and throughout the day, compared to plating and branching morphologies. These modeled geometric-based differences in the incident irradiances on different coral morphologies are not, however, consistent with actual depth-dependent distributions of these coral morphotypes, where plating morphologies dominate as you go deeper. Other factors, such as the cost of calcification, arguably contribute to these differences, but irradiance-driven patterns are a strong proximate cause for the observed differences in mesophotic communities on sloping versus vertical reef substrates.

Sponges are a diverse phylum of sessile filter-feeding invertebrates that are abundant on Caribbean reefs and provide essential ecological services, including nutrient cycling, reef stabilization, habitat, and food for a variety of fishes and invertebrates. As prominent members of the benthic community, and thus potential food resources, factors determining the biochemical and energetic content of sponges will affect their trophic contributions to coral reef ecosystems. In order to evaluate the influence of geographic variation on biochemical composition and energetic content in the tissue of sponges, we collected several common and widespread species (Agelas conifera, Agelas tubulata, Amphimedon compressa, Aplysina cauliformis, Niphates amorpha, Niphates erecta, and Xestospongia muta) from multiple shallow reefs in four countries across the Caribbean Basin, including Belize, Curacao, Grand Cayman, and St. Croix, U.S. Virgin Islands. In addition, we correlated inherent species-level traits, including the production of antipredator chemical defenses and the relative abundance of microbial symbionts, with biochemical and energetic content. We found that energetic content was higher in sponges with antipredator chemical defenses, and was significantly correlated with the concentration of chemical extracts from these sponges. We also noted that sponges with high microbial abundance contained significantly more soluble protein than sponges with low microbial abundance. Finally, both biochemical and energetic content varied significantly among sponges from different locations; sponges from Grand Cayman had the highest lipid and energetic content, whereas sponges from Belize had the highest carbohydrate content but lowest energetic content. Despite similar environmental conditions at these sites, our results demonstrate that biochemical and energetic content of sponges exhibits geographic variability, with potential implications for the trophic ecology of sponges throughout the Caribbean Basin.

Foundation species (FS) regulate ecological processes within communities often facilitating biodiversity and habitat complexity. Typically FS are dominant structure-forming taxa; but less dominant taxa having disproportionate ecological impacts to the community can also be FS. Mesophotic coral ecosystems (MCEs) are deep coral reef (∼30–150 m) communities, often dominated by emergent sponges in the Caribbean Basin. Despite the potential competitive advantage of sponges on MCEs, gorgonians are also common constituents of these reefs. Data from the Bahamas demonstrate increased biodiversity and densities of sponges on mesophotic reefs with gorgonians relative to reefs without these species. Drawing upon fifteen years of field surveys at five sites in the Caribbean Basin we assessed in situ interactions between gorgonians and sponges to quantify outcomes consistent with competition (i.e., tissue necrosis and overgrowth). Gorgonians were effective competitors against a variety of sponges, and two allelochemicals produced by Ellisella elongata were mechanistically important in interactions with Agelas clathrodes. We also examined invertebrate recruitment patterns near gorgonians to assess their role in facilitating MCE biodiversity. Our results indicate that live gorgonians, Antillogorgia bipinnata and E. elongata, facilitate biodiverse recruitment into MCEs, indicating that this process is governed by more than passive hydrodynamics. Collectively, these data indicate that these gorgonians exhibit both positive and negative ecological interactions (i.e., facilitation and competition, respectively) with sponges, and other taxa. Thus, these gorgonians are FS of MCE communities within the Caribbean Basin that display several traits contributing to the ecological structure of these understudied communities.