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Tropical coral reef ecosystems are changing rapidly to an alternative state in which sponges are the dominant living habitat, with giant barrel sponges (GBSs, Xestospongia spp.) representing the largest biomass. Unlike other benthic reef organisms, GBSs are ecosystem engineers that pump large volumes of seawater, disrupting the benthic boundary layer and directing flow away from the reef surface and into the water column. The morphology and size of GBSs have made them particularly good experimental subjects to study the hydraulics of sponge pumping and the transformation that occurs as seawater is processed by the sponge holobiont (sponge cells and microbial symbionts). This Review is part of a series marking the 100th birthday of The Company of Biologists, which was founded by marine biologist George Parker Bidder III, who primarily worked on sponges. The Review provides an integrative assessment of research on GBSs with comparisons with what is known about other marine sponges. Recent discoveries suggest that ancient lineages of morphologically indistinguishable GBSs are responding to environmental changes over sub-decadal time periods to rapidly populate reefs stripped of coral cover by climate change. If GBSs remain robust to rising seawater temperatures, they will become the greatest source of habitat complexity on reefs of the future, so knowledge of their biology and physiology will be important to our understanding of these ecosystems. 

With the decline of reef-building corals, other organisms are taking over Caribbean reefs, including sponges and benthic cyanobacterial mats (BCM). Sponges take up dissolved organic matter (DOM), but the sources and chemical characteristics of DOM taken up by sponges are unknown. One likely DOM source is benthic autotrophs, including BCM, which are prolific producers of DOM. We tested the hypothesis that sponges take up BCM-derived DOM using laboratory experiments in which seawater samples were collected before and after sequential incubations of BCM and small individuals of the giant barrel sponge Xestospongia muta. The concentration of DOC and relative abundance of individual features in the high resolution mass spectra using untargeted metabolomics were determined for each sample. There was a significant increase in DOC after BCM incubations, followed by a significant decrease after sponge incubations. These changes were mirrored in single feature relative abundances, with 2101 out of 3667 features significantly enriched during BCM incubations, and 54% of these (1142) depleted during sponge incubations. Among BCM-enriched and sponge-depleted features, many were halogenated, some were known BCM-derived secondary metabolites (e.g., carriebowmide, barbamide), and others matched unidentified sponge-depleted features from seawater samples collected on the reef. To our knowledge, this is the first report that sponges take up BCM exudates, including some that were detectable in reef DOM, revealing a path of molecules from source to sink through their environment. The BCM exudates taken up by sponges may be used as a food source or incorporated into sponge secondary metabolites for holobiont maintenance or chemical defenses. 

Coral reefs are biodiverse ecosystems that rely on trophodynamic transfers from primary producers to consumers through the detrital pathway. The sponge loop hypothesis proposes that sponges consume dissolved organic carbon (DOC) and produce large quantities of detritus on coral reefs, with this turn-over approaching the daily gross primary production of the reef ecosystem. In this study, we collected samples of detritus in the epilithic algal matrix (EAM) and samples from potential sources of detritus over two seasons from the forereef at Carrie Bow Cay, Belize. We chose this location to maximize the likelihood of finding support for the sponge loop hypothesis because Caribbean reefs have higher sponge abundances than other tropical reefs worldwide and the Mesoamerican barrier reef is an archetypal coral reef ecosystem. We used stable isotope analyses and eDNA metabarcoding to determine the composition of the detritus. We determined that the EAM detritus was derived from a variety of benthic and pelagic sources, with primary producers (micro- and macroalgae) as major contributors and metazoans (Arthropoda, Porifera, Cnidaria, Mollusca) as minor contributors. None of the sponge species that reportedly produce detritus were present in EAM detritus. The cnidarian signature in EAM detritus was dominated by octocorals, with a scarcity of hard corals. The composition of detritus also varied seasonally. The negligible contribution of sponges to reef detritus contrasts with the detrital pathway originally proposed in the sponge loop hypothesis. The findings indicate a mix of pelagic and benthic sources in the calmer summer and primarily benthic sources in the more turbulent spring.