Consumption of dissolved organic carbon by Caribbean reef sponges

Abstract

Sponges are conspicuous and abundant within the benthic fauna on Caribbean reefs. The ability of these organisms to efficiently capture carbon from particulate sources is well known and the importance of dissolved organic carbon (DOC) uptake has been recognized for several species. We surveyed DOC ingestion by seven sponge species common to Florida Keys reefs using nondisruptive sampling methods on undisturbed individuals. Three of the seven species exhibited significant DOC removal ranging from 13% to 24% of ambient concentrations. The tested species that removed DOC host large microbial consortia within their tissues, while the converse was observed for those that did not. This divergent behavior may suggest an important role for sponge associated microbes in the utilization of DOC by these species. The feeding behaviors of individuals of Xestospongia muta were then monitored over time to investigate its respiratory consumption of particulate and DOC. The uptake rates of dissolved oxygen (DO) and organic carbon by two undisturbed individuals revealed that DOC represented 96% of removed C, and that the tested individuals removed approximately equal quantities of C and DO. This demonstrates that X. muta largely satisfies its respiration demands through DOC consumption, and that DOC likely represents the dominant C source for biomass production and cell overturn in this species. These results further illustrate the metabolic importance of DOC to sponges, and suggest that these organisms are an important pathway for remineralizing organic matter on Caribbean reefs.Hard coral cover has declined from an average nearing 50% to less than 10% on Caribbean reefs between 1977and 2001(Gardner et al. 2003. Overall, scleractinian cover on Caribbean reefs remains suppressed, with most reefs exhibiting less than 20% total cover (Green et al. 2008;Schutte

A test of the sponge-loop hypothesis for emergent Caribbean reef sponges

“…A direct relationship between DOC availability and consumption may indicate that microbes are primarily involved in DOM uptake (Middelburg 2015); however, microbes and sponge cells may also differentially assimilate different DOC fractions (Rix et al 2017), which may explain the lack of a relationship for the other 4 species considered. Finally, given lower rates of DOC uptake by emergent sponge species, and approximately equivalent dissolved oxygen demand for emergent and encrusting species (Reiswig 1974, 1981, Yahel et al 2003, de Goeij et al 2008b, Hoer et al 2018), a larger proportion of consumed DOC may be used to satisfy respiration demands by emergent species relative to encrusting species, allowing for carbon accumulation and cell turnover by the latter (see Hoer et al 2018 for discussion).…”

“…Notably, an increasing number of sponge species have been found to feed on DOC (Yahel et al 2003, de Goeij et al 2008b, Ribes et al 2012, Mueller et al 2014, McMurray et al 2016, Archer et al 2017, Hoer et al 2018, Morganti et al 2017, and a link between DOC uptake and detritus production has been established for additional cryptic sponge species (Alexander et al 2014, Rix et al 2016. While it was generally thought that sponge species with dense assemblages of symbiotic microbes -i.e.…”

“…While it was generally thought that sponge species with dense assemblages of symbiotic microbes -i.e. high microbial abundance (HMA) sponges (Gloeckner et al 2014) -derive a majority of their dietary carbon from DOC, and low microbial abundance (LMA) sponges derive it from filtering POC (Maldonado et al 2012, Hoer et al 2018, there is increasing evidence that some LMA sponges consume DOC (Mueller et al 2014, Rix et al 2016, Morganti et al 2017 and that sponge cells are directly involved in DOC uptake (de Goeij et al 2008a, Rix et al 2016. The spongeloop has been supported in recent studies of encrusting species using more ecologically-relevant DOC types, including coral-and algal-derived DOC (Rix et al 2017), and assimilation rates for these DOC types are comparable to those for diatom-derived DOC (de Goeij et al 2013).…”

“…Massive and emergent sponge species, which dominate the surface of Caribbean coral reefs (Loh & Pawlik 2014), represent a large proportion of total coral reef sponge biomass and are therefore expected to represent a substantial contribution to carbon cycling if they participate in the sponge-loop. While DOC uptake has been demonstrated for a few emergent sponge species (Yahel et al 2003, McMurray et al 2016, Archer et al 2017, Hoer et al 2018, potential detritus production has yet to be quantified for these species (but see McMurray et al 2016).…”

Reviews and syntheses: to the bottom of carbon processing at the seafloor

“…Some invertebrates have the capability to take up dissolved organic carbon and, in particular, sponges can assimilate substantial quantities and transform it into biomass (de Goeij et al, 2013;Fiore et al, 2017;Hoer et al, 2018). This sponge tissue and in particular its detritus can be consumed by benthic organisms.…”