Sponge Loop Research Articles

Looking for the sponge loop: analyses of detritus on a Caribbean forereef using stable isotope and eDNA metabarcoding techniques.

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.

Sponge organic matter recycling: Reduced detritus production under extreme environmental conditions

Sponges are a key component of coral reef ecosystems and play an important role in carbon and nutrient cycles. Many sponges are known to consume dissolved organic carbon and transform this into detritus, which moves through detrital food chains and eventually to higher trophic levels via what is known as the sponge loop. Despite the importance of this loop, little is known about how these cycles will be impacted by future environmental conditions. During two years (2018 and 2020), we measured the organic carbon, nutrient recycling, and photosynthetic activity of the massive HMA, photosymbiotic sponge Rhabdastrella globostellata at the natural laboratory of Bouraké in New Caledonia, where the physical and chemical composition of seawater regularly change according to the tide. We found that while sponges experienced acidification and low dissolved oxygen at low tide in both sampling years, a change in organic carbon recycling whereby sponges stopped producing detritus (i.e., the sponge loop) was only found when sponges also experienced higher temperature in 2020. Our findings provide new insights into how important trophic pathways may be affected by changing ocean conditions.

Ecological succession of the sponge cryptofauna in Hawaiian reefs add new insights to detritus production by pioneering species

Successional theory proposes that fast growing and well dispersed opportunistic species are the first to occupy available space. However, these pioneering species have relatively short life cycles and are eventually outcompeted by species that tend to be longer-lived and have lower dispersal capabilities. Using Autonomous Reef Monitoring Structures (ARMS) as standardized habitats, we examine the assembly and stages of ecological succession among sponge species with distinctive life history traits and physiologies found on cryptic coral reef habitats of Kāneʻohe Bay, Hawaiʻi. Sponge recruitment was monitored bimonthly over 2 years on ARMS deployed within a natural coral reef habitat resembling the surrounding climax community and on ARMS placed in unestablished mesocosms receiving unfiltered seawater directly from the natural reef deployment site. Fast growing haplosclerid and calcareous sponges initially recruited to and dominated the mesocosm ARMS. In contrast, only slow growing long-lived species initially recruited to the reef ARMS, suggesting that despite available space, the stage of ecological succession in the surrounding habitat influences sponge community development in uninhabited space. Sponge composition and diversity between early summer and winter months within mesocosm ARMS shifted significantly as the initially recruited short-lived calcareous and haplosclerid species initially recruit and then died off. The particulate organic carbon contribution of dead sponge tissue from this high degree of competition-free community turnover suggests a possible new component to the sponge loop hypothesis which remains to be tested among these pioneering species. This source of detritus could be significant in early community development of young coastal habitats but less so on established coral reefs where the community is dominated by long-lived colonial sponges.

A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.

The potential roles of sponges in integrated mariculture

AbstractThis mini‐review evaluates the use of marine sponges in integrated culture systems, two decades after the idea was first proposed. It was predicted that the concept would provide a double benefit: sponges would grow faster under higher organic loadings, and filtration by sponges would improve water quality. It is promising that the growth of some commercially interesting sponges is indeed faster in organically enriched areas. The applicability of sponges as filters for undesired microorganisms has been confirmed in laboratory studies. However, upscaled farming studies need to be done to demonstrate the value of sponges for in situ bioremediation of sewage discharge or waste produced by fish cages. In addition, a new idea is presented – the use of sponges as an engine to convert dissolved organic matter (DOM) into particulate organic matter (POM) that can be consumed by deposit feeders through a chain of processes termed the sponge loop. A theoretical design of an integrated culture with seaweeds (Gracilaria sp.), sponges (Halisarca caerulea) and sea cucumbers (Apostichopus japonica) shows that 37% of the part of the primary production that is excreted by the seaweeds as DOM can be directly recovered in sponge biomass and a subsequent 12% in sea cucumber biomass after mediation (conversion of DOM to POM) by sponges. Hence, the total recovery of DOM into (sponge and sea cucumber) biomass within this IMTA is 49%.

Single-cell visualization indicates direct role of sponge host in uptake of dissolved organic matter

Marine sponges are set to become more abundant in many near-future oligotrophic environments, where they play crucial roles in nutrient cycling. Of high importance is their mass turnover of dissolved organic matter (DOM), a heterogeneous mixture that constitutes the largest fraction of organic matter in the ocean and is recycled primarily by bacterial mediation. Little is known, however, about the mechanism that enables sponges to incorporate large quantities of DOM in their nutrition, unlike most other invertebrates. Here, we examine the cellular capacity for direct processing of DOM, and the fate of the processed matter, inside a dinoflagellate-hosting bioeroding sponge that is prominent on Indo-Pacific coral reefs. Integrating transmission electron microscopy with nanoscale secondary ion mass spectrometry, we track 15N- and 13C-enriched DOM over time at the individual cell level of an intact sponge holobiont. We show initial high enrichment in the filter-feeding cells of the sponge, providing visual evidence of their capacity to process DOM through pinocytosis without mediation of resident bacteria. Subsequent enrichment of the endosymbiotic dinoflagellates also suggests sharing of host nitrogenous wastes. Our results shed light on the physiological mechanism behind the ecologically important ability of sponges to cycle DOM via the recently described sponge loop.

Depth‐dependent detritus production in the sponge, Halisarca caerulea

AbstractSponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge‐loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (< 30 m) cryptic species. However, support for this hypothesis at mesophotic depths (∼ 30–150 m) is lacking. Here, we examined detritus production, a prerequisite of the sponge loop pathway, in a reciprocal transplant experiment, using Halisarca caerulea from water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples of H. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes in Oxyphotobacteria, Acidimicrobiia, Nitrososphaeria, Nitrospira, Deltaproteobacteria, and Dadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

Marine Sponges as Chloroflexi Hot Spots: Genomic Insights and High-Resolution Visualization of an Abundant and Diverse Symbiotic Clade.

Members of the widespread bacterial phylum Chloroflexi can dominate high-microbial-abundance (HMA) sponge microbiomes. In the Sponge Microbiome Project, Chloroflexi sequences amounted to 20 to 30% of the total microbiome of certain HMA sponge genera with the classes/clades SAR202, Caldilineae, and Anaerolineae being the most prominent. We performed metagenomic and single-cell genomic analyses to elucidate the functional gene repertoire of Chloroflexi symbionts of Aplysina aerophoba. Eighteen draft genomes were reconstructed and placed into phylogenetic context of which six were investigated in detail. Common genomic features of Chloroflexi sponge symbionts were related to central energy and carbon converting pathways, amino acid and fatty acid metabolism, and respiration. Clade-specific metabolic features included a massively expanded genomic repertoire for carbohydrate degradation in Anaerolineae and Caldilineae genomes, but only amino acid utilization by SAR202. While Anaerolineae and Caldilineae import cofactors and vitamins, SAR202 genomes harbor genes encoding components involved in cofactor biosynthesis. A number of features relevant to symbiosis were further identified, including CRISPR-Cas systems, eukaryote-like repeat proteins, and secondary metabolite gene clusters. Chloroflexi symbionts were visualized in the sponge extracellular matrix at ultrastructural resolution by the fluorescence in situ hybridization-correlative light and electron microscopy (FISH-CLEM) method. Carbohydrate degradation potential was reported previously for "Candidatus Poribacteria" and SAUL, typical symbionts of HMA sponges, and we propose here that HMA sponge symbionts collectively engage in degradation of dissolved organic matter, both labile and recalcitrant. Thus, sponge microbes may not only provide nutrients to the sponge host, but they may also contribute to dissolved organic matter (DOM) recycling and primary productivity in reef ecosystems via a pathway termed the sponge loop. IMPORTANCE Chloroflexi represent a widespread, yet enigmatic bacterial phylum with few cultivated members. We used metagenomic and single-cell genomic approaches to characterize the functional gene repertoire of Chloroflexi symbionts in marine sponges. The results of this study suggest clade-specific metabolic specialization and that Chloroflexi symbionts have the genomic potential for dissolved organic matter (DOM) degradation from seawater. Considering the abundance and dominance of sponges in many benthic environments, we predict that the role of sponge symbionts in biogeochemical cycles is larger than previously thought.

Climate change alterations to ecosystem dominance: how might sponge-dominated reefs function?

Anthropogenic stressors are impacting ecological systems across the world. Of particular concern are the recent rapid changes occurring in coral reef systems. With ongoing degradation from both local and global stressors, future reefs are likely to function differently from current coral-dominated ecosystems. Determining key attributes of future reef states is critical to reliably predict outcomes for ecosystem service provision. Here we explore the impacts of changing sponge dominance on coral reefs. Qualitative modelling of reef futures suggests that changing sponge dominance due to increased sponge abundance will have different outcomes for other trophic levels compared with increased sponge dominance as a result of declining coral abundance. By exploring uncertainty in the model outcomes we identify the need to (1) quantify changes in carbon flow through sponges, (2) determine the importance of food limitation for sponges, (3) assess the ubiquity of the recently described "sponge loop," (4) determine the competitive relationships between sponges and other benthic taxa, particularly algae, and (5) understand how changing dominance of other organisms alters trophic pathways and energy flows through ecosystems. Addressing these knowledge gaps will facilitate development of more complex models that assess functional attributes of sponge-dominated reef ecosystems.

Paradigm Lost: Dynamic Nutrients and Missing Detritus on Coral Reefs

Some of the fundamental drivers of reef functioning are being rewritten through progress in understanding nutrient cycling. The sponge loop, described in 2013, revealed that some cryptic sponges can convert dissolved organic carbon (DOC) into detritus. In subsequent studies, researchers proposed that sponges and seaweeds could mutually reinforce their abundance by utilizing each other's waste products, thereby helping to suppress coral recovery. We build on these ideas, including the provision of a new but related hypothesis to explain the reinforcement of coral-algal phase shifts: Detritus and DOC resulting from fleshy algae reduce light penetration and increase the stress on corals, particularly in terms of calcification. We then consider the wider ecosystem implications of nutrient cycling and arrive at some novel conclusions. In particular, we propose that the combination of higher sponge biomass, which generates detritus, with the relative paucity of detritivory should generate a surplus of detritus on Caribbean reefs compared with that of the Indo-Pacific. New studies are needed to quantify the generality of the sponge loop and to track the fate of detritus to determine whether there is a surplus in the Caribbean. Although Charles Darwin identified enigmatic aspects of the nutritional status of coral reefs, this research field continues to surprise and redefine how we view the dynamics of this complex ecosystem.

Reef sponges facilitate the transfer of coral-derived organic matter to their associated fauna via the sponge loop

The high biodiversity of coral reefs results in complex trophic webs where energy and nutrients are transferred between species through a multitude of pathways. Here, we hypothesize that reef sponges convert the dissolved organic matter released by benthic primary producers (e.g. corals) into particulate detritus that is transferred to sponge-associated detritivores via the sponge loop pathway. To test this hypothesis, we conducted stable isotope (C-13 and N-15) tracer experiments to investigate the uptake and transfer of coral-derived organic matter from the sponges Mycale fistulifera and Negombata magnifica to 2 types of detritivores commonly associated with sponges: ophiuroids (Ophiothrix savignyi and Ophiocoma scolopendrina) and polychaetes (Polydorella smurovi). Findings revealed that the organic matter naturally released by the corals was indeed readily assimilated by both sponges and rapidly released again as sponge detritus. This detritus was subsequently consumed by the detritivores, demonstrating transfer of coral-derived organic matter from sponges to their associated fauna and confirming all steps of the sponge loop. Thus, sponges provide a trophic link between corals and higher trophic levels, thereby acting as key players within reef food webs.

Differential recycling of coral and algal dissolved organic matter via the sponge loop

Summary Corals and macroalgae release large quantities of dissolved organic matter (DOM), one of the largest sources of organic matter produced on coral reefs. By rapidly taking up DOM and transforming it into particulate detritus, coral reef sponges are proposed to play a key role in transferring the energy and nutrients in DOM to higher trophic levels via the recently discovered sponge loop. DOM released by corals and algae differs in quality and composition, but the influence of these different DOM sources on recycling by the sponge loop has not been investigated. Here, we used stable isotope pulse‐chase experiments to compare the processing of naturally sourced coral‐ and algal‐derived DOM by three Red Sea coral reef sponge species: Chondrilla sacciformis, Hemimycale arabica and Mycale fistulifera. Incubation experiments were conducted to trace 13C‐ and 15N‐enriched coral‐ and algal‐derived DOM into the sponge tissue and detritus. Incorporation of 13C into specific phospholipid‐derived fatty acids (PLFAs) was used to differentiate DOM assimilation within the sponge holobiont (i.e. the sponge host vs. its associated bacteria). All sponges assimilated both coral‐ and algal‐derived DOM, but incorporation rates were significantly higher for algal‐derived DOM. The two DOM sources were also processed differently by the sponge holobiont. Algal‐derived DOM was incorporated into bacteria‐specific PLFAs at a higher rate while coral‐derived DOM was more readily incorporated into sponge‐specific PLFAs. A substantial fraction of the dissolved organic carbon (C) and nitrogen (N) assimilated by the sponges was subsequently converted into and released as particulate detritus (15–24% C and 27–49% N). However, algal‐derived DOM was released as detritus at a higher rate. The higher uptake and transformation rates of algal‐ compared with coral‐derived DOM suggest that reef community phase shifts from coral to algal dominance may stimulate DOM cycling through the sponge loop with potential consequences for coral reef biogeochemical cycles and food webs.

Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems.

Shallow warm-water and deep-sea cold-water corals engineer the coral reef framework and fertilize reef communities by releasing coral mucus, a source of reef dissolved organic matter (DOM). By transforming DOM into particulate detritus, sponges play a key role in transferring the energy and nutrients in DOM to higher trophic levels on Caribbean reefs via the so-called sponge loop. Coral mucus may be a major DOM source for the sponge loop, but mucus uptake by sponges has not been demonstrated. Here we used laboratory stable isotope tracer experiments to show the transfer of coral mucus into the bulk tissue and phospholipid fatty acids of the warm-water sponge Mycale fistulifera and cold-water sponge Hymedesmia coriacea, demonstrating a direct trophic link between corals and reef sponges. Furthermore, 21–40% of the mucus carbon and 32–39% of the nitrogen assimilated by the sponges was subsequently released as detritus, confirming a sponge loop on Red Sea warm-water and north Atlantic cold-water coral reefs. The presence of a sponge loop in two vastly different reef environments suggests it is a ubiquitous feature of reef ecosystems contributing to the high biogeochemical cycling that may enable coral reefs to thrive in nutrient-limited (warm-water) and energy-limited (cold-water) environments.

Surviving in a Marine Desert: The Sponge Loop Retains Resources Within Coral Reefs

Ever since Darwin's early descriptions of coral reefs, scientists have debated how one of the world's most productive and diverse ecosystems can thrive in the marine equivalent of a desert. It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna. This "sponge loop" was confirmed in aquarium and in situ food web experiments, using (13)C- and (15)N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as coral reefs persist in oligotrophic seas--the reef's paradox--and has implications for reef ecosystem functioning and conservation strategies.