Abiotic conditions drive significant variability in nutrient processing by a common Caribbean sponge, Ircinia felix

Abstract

Coral reefs typically occur in oligotrophic waters, where tight recycling of energy and nutrients is essential in order to support their high productivity. Sponges are efficient filter feeders that host diverse and abundant microbial communities that often contain members capable of carrying out complex nutrient transformations. Consequently, sponges often act as significant sources of bioavailable forms of nitrogen and phosphorus while acting as sinks for dissolved organic carbon (DOC). However, little attention has focused on variability of nutrient release by sponges and no studies have reported how abiotic conditions may impact sponge‐driven changes in nutrient concentrations. Here, we show that a common Caribbean sponge, Ircinia felix, is capable of being both a source and a sink for DOC, ammonium, nitrate/nitrite ( NOx−), and phosphate ( PO43−). Additionally, we show that abiotic conditions, particularly ambient nutrient availability, seem to explain a significant amount of the variability (R2 range from 0.40 to 0.65). Interestingly, as ambient nutrient concentrations increased, I. felix transitioned from acting as a source to serving as a sink for all nutrient forms measured. We also found I. felix‐associated bacteria exhibit a significantly higher abundance of predicted nitrogen metabolism, carbon fixation, and photosynthetic genes relative to ambient water and sediment. These results suggest that sponges play an important and dynamic role in biogeochemical cycling on reefs, particularly as human activities alter natural nutrient dynamics in coastal systems.

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

“…It is thought that sponges primarily consume labile, rather than refractory, forms of DOC (Yahel et al 2003, de Goeij et al 2008b, and higher rates of uptake and detritus production have been found for sponges incubated with algal-versus coral-derived DOC (Rix et al 2017). Evidence suggests that there may be a direct relationship between ambient DOC concentrations and DOC uptake, and there may be a threshold for DOC uptake (Mueller et al 2014, McMurray et al 2016, Archer et al 2017, Morganti et al 2017. Our results only support such a relationship for the HMA species Agelas tubulata, Verongula reiswigi, V. gigantea, and the LMA species Callyspongia plicifera, although additional data are needed to further examine this putative relationship for the species investigated.…”

“…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.…”

“…The DOM pool available on coral reefs is highly heterogeneous (Hansell & Carlson 2002), consisting of a mixture of refractory and labile forms that likely vary in their bioavailability to sponges (Yahel et al 2003, de Goeij et al 2008b. Additionally, both the quality (Rix et al 2017) and concentration (Mueller et al 2014, McMurray et al 2016, Archer et al 2017, Morganti et al 2017 of DOC are known to affect rates of sponge-mediated DOC flux. Even more striking is that work on the sponge-loop has thus far been limited to sponge species with thinly encrusting growth forms that typically live in reef interstices.…”

“…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).…”

Dissolved inorganic nitrogen fluxes from common Florida Bay (U.S.A.) sponges

“…These factors likely acted in concert, leading an underestimation of the ingested or produced DOM (as in Jiménez and Ribes ). Of note in this context is that sponges, including one of the species analyzed herein, I. felix , can be both sources and sinks of organic matter (e.g., Archer et al ). This continual production and consumption in the chambered water mass would obscure overall trends in behavior and could similarly stymie attempts to determine uptake or production over time.…”