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Biotic interactions have critical effects on the structure of ecological communities, and the variation in the strength of these interactions over space and time contributes to biogeographic variation in communities. Predation shapes community composition in a variety of habitats, although there have been comparatively few experimental studies of these effects across latitudinal scales. We tested the impact of predator exclusion on the development of epifaunal communities across 3 sites (Florida [USA], Belize, and Panama) in seagrass habitats dominated by Thalassia testudinum using caged and uncaged settlement panels. We found that predators altered composition and slowed development of epifaunal communities. The nature and magnitude of these effects, however, were complex, site-dependent, and tightly coupled to community development. Fast-growing, soft-bodied species dominated space when predators were excluded, while more resistant calcifying species were dominant in communities exposed to predators. In Panama, non-native ascidians dominated communities in cages, while ascidians were consumed when exposed to predators, indicating the importance of biotic resistance at that site. Predators also reduced the abundance of associated small mobile fauna, and the positive correlation between mobile faunal abundances and sessile biomass in our study suggests a potential indirect effect of predator-mediated habitat modification. Overall, prey characteristics were important in explaining the site-specific effects of predators on communities, indicating that taxonomic resolution can influence the results of multi-regional studies examining the mechanisms affecting community structure.

14 pages, 3 figures, 2 tables.-- This is Smithsonian Marine Station contribution #1138, In 2011, the Indian River Lagoon, a biodiverse estuary in eastern Florida (USA), experienced an intense microalgal bloom with disastrous ecological consequences. The bloom included a mix of microalgae with unresolved taxonomy and lasted for 7 months with a maximum concentration of 130 μg chlorophyll a L. In 2012, brown tide Aureoumbra lagunensis also bloomed in portions of this estuary, with reoccurrences in 2016 and 2018. To identify and understand the role of grazer pressure (top-down control) on bloom formation, we coupled DNA sequencing with bivalve feeding assays using three microalgae isolated from the 2011 bloom and maintained in culture. Feeding experiments were conducted on widely distributed bivalve species in the lagoon, including eastern oysters (Crassostrea virginica), hooked mussels (Ischadium recurvum), charru mussels (Mytella charruana), green mussels (Perna viridis), Atlantic rangia (Rangia cuneata), and hard clams (Mercenaria mercenaria), which were exposed to 3 × 10 cells mL of five species of microalgae consisting of A. lagunensis and the three species clarified herein, the picocyanobacteria Crocosphaera sp. and ‘Synechococcus’ sp., and the picochlorophyte Picochlorum sp., as well as Nannochloropsis oculata used as a control. To ensure clearance rates were indicative of consumption and assimilation, the microalgae were isotopically (N) labeled prior to feeding experiments. Clearance rates differed among bivalve and microalgal species, but enriched N values in bivalve tissue suggest that algal bloom species were assimilated by the bivalves. These results expand our understanding of the important ecosystem services that healthy, biodiverse filter feeder communities provide, We thank St. Johns River Water Management District (Contract 27799) and the Florida Fish and Wildlife Conservation Commission (FWC Agreement No. 13051) for funding the project, With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI)

Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ13C and δ15N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ13C and δ15N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ15N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ13C and δ15N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts.

Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.

Microplastics (MP) are now considered ubiquitous across global aquatic environments. The ingestion of MP by fish and other marine vertebrates is well studied, but the ingestion of MP by marine invertebrates is not. Sponges (Phylum Porifera) are particularly understudied when it comes to MP ingestion, even though they are widely distributed across benthic habitats, can process large volumes of seawater, and can retain small particles within their water filtration systems. This study examines the presence of potential MP (PMP) in wild marine sponges and seawater collected in Bocas del Toro, Panamá. Subsurface seawater and tissue from six common Caribbean sponge species was collected in Saigon Bay, a heavily impacted, shallow-water coral reef. Seawater samples were filtered onto glass fiber filters to retain any PMP present and sponge tissue was digested with bleach, heated and filtered. Filters were examined using fluorescence microscopy to quantify PMP. An average of 107 ± 25 PMP L–1 was detected in seawater from Saigon Bay with particles ranging in size between 10 μm and ~3,000 μm. The number of PMP found in sponge tissue ranged between 6 ± 4 and 169 ± 71 PMP g–1 of dry tissue. Most particles found in sponge samples were very small (10–20 μm), but fibers greater than 5,000 μm were detected. Our results indicate that PMP exists within the tissues of the sponges we studied, but future studies should confirm the presence of MP in sponges using chemical analysis. Most importantly, the discrepancy between low levels of PMP in our sponge samples and high levels in the surrounding seawater highlights the potential for sponges to resist and/or egest MP. Finally, we provide a critical evaluation of our methods to improve their use in future MP work with benthic marine organisms.

The chemical ecology and chemical defenses of sponges have been investigated for decades; consequently, sponges are among the best understood marine organisms in terms of their chemical ecology, from the level of molecules to ecosystems. Thousands of natural products have been isolated and characterized from sponges, and although relatively few of these compounds have been studied for their ecological functions, some are known to serve as chemical defenses against predators, microorganisms, fouling organisms, and other competitors. Sponges are hosts to an exceptional diversity of microorganisms, with almost 40 microbial phyla found in these associations to date. Microbial community composition and abundance are highly variable across host taxa, with a continuum from diverse assemblages of many microbial taxa to those that are dominated by a single microbial group. Microbial communities expand the nutritional repertoire of their hosts by providing access to inorganic and dissolved sources of nutrients. Not only does this continuum of microorganism–sponge associations lead to divergent nutritional characteristics in sponges, these associated microorganisms and symbionts have long been suspected, and are now known, to biosynthesize some of the natural products found in sponges. Modern “omics” tools provide ways to study these sponge–microbe associations that would have been difficult even a decade ago. Metabolomics facilitate comparisons of sponge compounds produced within and among taxa, and metagenomics and metatranscriptomics provide tools to understand the biology of host–microbe associations and the biosynthesis of ecologically relevant natural products. These combinations of ecological, microbiological, metabolomic and genomics tools, and techniques provide unprecedented opportunities to advance sponge biology and chemical ecology across many marine ecosystems.

Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate sponges. In this study, using sponge specimens collected from Guam, the Solomon Islands, the Florida Keys, and Puerto Rico, we queried whether the presence of bromotyrosine alkaloids potentiates metabolomic and microbiome conservation among geographically distant and phylogenetically different marine sponges. A multi-omic characterization of sponge holobionts revealed vastly different metabolomic and microbiome architectures among different bromotyrosine alkaloid-harboring sponges. However, we find statistically significant correlations between the microbiomes and metabolomes, signifying that the microbiome plays an important role in shaping the overall metabolome, even in low-microbial-abundance sponges. Molecules mined from the polar metabolomes of these sponges revealed conservation of biosynthetic logic between bromotyrosine alkaloids and brominated pyrrole-imidazole alkaloids, another class of marine sponge-derived natural products. In light of prior findings postulating the sponge host itself to be the biosynthetic source of bromotyrosine alkaloids, our data now set the stage for investigating the causal relationships that dictate the microbiome-metabolome interconnectedness for marine sponges in which the microbiome may not contribute to natural product biogenesis. IMPORTANCE Our work demonstrates that phylogenetically and geographically distant sponges with very different microbiomes can harbor natural product chemical classes that are united in their core chemical structures and biosynthetic logic. Furthermore, we show that independent of geographical dispersion, natural product chemistry, and microbial abundance, overall sponge metabolomes tightly correlate with their microbiomes.

Marine sponges and their associated symbionts produce a structurally diverse and complex set of natural products including alkaloids, terpenoids, peptides, lipids, and steroids. A single sponge with its symbionts can produce all of the above-mentioned classes of molecules and their analogs. Most approaches to evaluating sponge chemical diversity have focused on major metabolites that can be isolated and characterized; therefore, a comprehensive evaluation of intra- (within a molecular family; analogs) and inter-chemical diversity within a single sponge remains incomplete. We use a combination of metabolomics tools, including a supervised approach via manual library search and literature search, and an unsupervised approach via molecular networking and MS2LDA analysis to describe the intra and inter-chemical diversity present in Smenospongia aurea. Furthermore, we use imaging mass spectrometry to link this chemical diversity to either the sponge or the associated cyanobacteria. Using these approaches, we identify seven more molecular features that represent analogs of four previously known peptide/polyketide smenamides and assign the biosynthesis of these molecules to the symbiotic cyanobacteria by imaging mass spectrometry. We extend this analysis to a wide diversity of molecular classes including indole alkaloids and meroterpenes.

Potentiometric redox measurements were made in subnanoliter droplets of solutions using an optically transparent nanoporous gold electrode strategically mounted on the stage of an inverted microscope. Nanoporous gold was prepared via dealloying gold leaf with concentrated nitric acid and was chemisorbed to a standard microscope coverslip with (3-mercaptopropyl)trimethoxysilane. The gold surface was further modified with 1-hexanethiol to optimize hydrophobicity of the surface to allow for redox measurements to be made in nanoscopic volumes. Time traces of the open-circuit potential (OCP) were used to construct Nernst plots to evaluate the applicability of the droplet-based potentiometric redox measurement system. Two poised one-electron transfer systems (potassium ferricyanide/ferrocyanide and ferrous/ferric ammonium sulfate) yielded Nernstian slopes of -58.5 and -60.3 mV, respectively, with regression coefficients greater than 0.99. The y-intercepts of the two agreed well to the formal potential of the two standard oxidation-reduction potential (ORP) calibrants, ZoBell's and Light's solution. The benzoquinone and hydroquinone redox couple was examined as a representative two-electron redox system; a Nernst slope of -30.8 mV was obtained. Additionally, two unpoised systems (potassium ferricyanide and ascorbic acid) were studied to evaluate the system under conditions where only one form of the redox couple is present in appreciable concentrations. Again, slopes near the Nernstian values of -59 and -29 mV, respectively, were obtained. All experiments were carried out using solution volumes between 280 and 1400 pL with injection volumes between 8 and 100 pL. The miniscule volumes allowed for extremely rapid mixing (305 ms) as well. The small volumes and rapid mixing along with the high accuracy and sensitivity of these measurements lend support to the use of this approach in applications where time is a factor and only small volumes are available for testing.

The success of many sessile invertebrates in marine benthic communities is linked to their ability to efficiently remove suspended organic matter from the surrounding water column. To investigate the diet of the barnacle Amphibalanus eburneus, a dominant suspension feeder within the Indian River Lagoon (IRL) of central Florida, we compared the stable isotopes ratios (δ13C and δ15N) of barnacle tissue to those of particulate organic matter (POM). Collections were carried out quarterly for a year from 29 permanent sites and at sites impacted by an Aureoumbra lagunensis bloom. δ13C and δ15N values of Amphibalanus eburneus varied across sites, but δ15N was more stable over time. There was a range of δ15N values of Amphibalanus eburneus tissue from 6.0‰ to 10.5‰ across sites. Because land-based sources such as sewage are generally enriched in 15N, this suggests a continuum of anthropogenic influence across sites in the IRL. Over 70% of the variation in δ15N values of Amphibalanus eburneus across sites was driven by the δ15N values of POM, supporting a generalist feeding strategy on available sources of suspended organic matter. The dominance of this generalist consumer in the IRL may be linked to its ability to consume spatially and temporally variable food resources derived from natural and anthropogenic sources, as well as Aureoumbra lagunensis cells. Generalist consumers such as Amphibalanus eburneus serve an important ecological role in this ecosystem and act as a sentinel species and recorder of local, site-specific isotopic baselines.

Photosymbionts play an important role in the ecology and evolution of diverse host species within the marine environment. Although sponge-photosymbiont interactions have been well described from geographically disparate sites worldwide, our understanding of these interactions from shallow water systems within French Polynesia is limited. We surveyed diverse habitats around the north coast of Moorea, French Polynesia and screened sponges for the presence of photosymbionts. Overall sponge abundance and diversity were low, with Lendenfeldia chondrodeswas the only species that supported a high abundance of photosymbionts and was also the only species found in exposed, illuminated habitats. Interestingly,L. chondrodeswas found at three distinct sites, with a massive, fan-shaped growth form at two of the lagoon sites and a thin, encrusting growth form within a bay site. These two growth forms differed in their photosymbiont abundance, with massive individuals ofL. chondrodeshaving higher photosymbiont abundance than encrusting individuals from the bay. We present evidence that some sponges from French Polynesia support abundant photosymbiont communities and provide initial support for the role of these communities in host ecology.

Sponges are efficient filter feeders, removing significant portions of particulate and dissolved organic matter (POM, DOM) from the water column. While the assimilation and respiration of POM and DOM by sponges and their abundant microbial symbiont communities have received much attention, there is virtually no information on the impact of sponge holobiont metabolism on the composition of DOM at a molecular-level. We applied untargeted and targeted metabolomics techniques to characterize DOM in seawater samples prior to entering the sponge (inhalant reef water), in samples exiting the sponge (exhalent seawater), and in samples collected just outside the reef area (off reef seawater). Samples were collected from two sponge species,Ircinia campanaandSpheciospongia vesparium, on a near-shore hard bottom reef in the Florida Keys. Metabolic profiles generated from untargeted metabolomics analysis indicated that many more compounds were enhanced in the exhalent samples than in the inhalant samples. Targeted metabolomics analysis revealed differences in diversity and concentration of metabolites between exhalent and off reef seawater. For example, most of the nucleosides were enriched in the exhalent seawater, while the aromatic amino acids, caffeine and the nucleoside xanthosine were elevated in the off reef water samples. Although the metabolic profile of the exhalent seawater was unique, the impact of sponge metabolism on the overall reef DOM profile was spatially limited in our study. There were also no significant differences in the metabolic profiles of exhalent water between the two sponge species, potentially indicating that there is a characteristic DOM profile in the exhalent seawater of Caribbean sponges. Additional work is needed to determine whether the impact of sponge DOM is greater in habitats with higher sponge cover and diversity. This work provides the first insight into the molecular-level impact of sponge holobiont metabolism on reef DOM and establishes a foundation for future experimental studies addressing the influence of sponge-derived DOM on chemical and ecological processes in coral reef ecosystems.

BackgroundSaba Bank Atoll, Netherlands Antilles, is one of the three largest atolls on Earth and provides habitat for an extensive coral reef community. To improve our knowledge of this vast marine resource, a survey of biodiversity at Saba Bank included a multi-disciplinary team that sampled fishes, mollusks, crustaceans, macroalgae, and sponges.Methodology/Principal FindingsA single member of the dive team conducted surveys of sponge biodiversity during eight dives at six locations, at depths ranging from 15 to 30 m. This preliminary assessment documented the presence of 45 species pooled across multiple locations. Rarefaction analysis estimated that only 48 to 84% of species diversity was sampled by this limited effort, clearly indicating a need for additional surveys. An analysis of historical collections from Saba and Saba Bank revealed an additional 36 species, yielding a total of 81 sponge species recorded from this area.Conclusions/SignificanceThis observed species composition is similar to that found on widespread Caribbean reefs, indicating that the sponge fauna of Saba Bank is broadly representative of the Caribbean as a whole. A robust population of the giant barrel sponge, Xestospongia muta, appeared healthy with none of the signs of disease or bleaching reported from other Caribbean reefs; however, more recent reports of anchor chain damage to these sponges suggests that human activities can have dramatic impacts on these communities. Opportunities to protect this extremely large habitat should be pursued, as Saba Bank may serve as a significant reservoir of sponge species diversity.