Sponge waste that fuels marine oligotrophic food webs: a re‐assessment of its origin and nature

Abstract

It has recently been realized that sponges take up much of the dissolved organic matter (DOM) available in the water of reefs. The energy derived from this DOM is suggested to be invested in renewing the sponge filter cells (choano-cytes) every few hours, generating an outflow of detrital particulate organic matter (POM) that is rapidly ingested by other invertebrates. By this DOM-to-POM recycling, sponges are proposed to fuel the food web of oligotrophic marine communities, including reefs, caves and deep-sea environments. In four species studied herein by electron microscopy, the POM found in the outgoing aquiferous canals had a complex composition, with large between-species differences. It may include choanocytes (0-52%), and also mesohyl cells, such as ar-cheocytes (9-20%) and spherulous, and granular cells with inclusions (27-90%). Exocytosed vesicles also occurred. Surprisingly, to end up into the outgoing canals, the internal mesohyl cells are squeezed between the epithelial cells (endopinacocytes) of the canal wall. Mesohyl cells were also able to transfer their inclusions to the endopinacocytes, which in turn extruded their acquired vesicle loads into the canal lumen. The unanticipated abundant participation of mesohyl cells and endopinacocytes in the production of POM appears to be an ordinary process that occurs continuously in the sponges, mostly related to elimination of digestion leftovers and excretion by-products. Therefore, POM is generated by sponges irrespective of whether the primary food source is particulate (evidence from this study) or DOM (previous literature). Altogether, these results indicate that the cellular mechanisms behind the relevant organic-matter recycling carried out by sponges are more diverse than initially anticipated. The varying ratios of choanocytes/mesohyl cells in the POM across species suggest that different sponge species may impact differently the energetics of food webs of the respective oligotrophic habitats where they dominate.

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

“…Sponge detritus includes both debris resulting from cell turnover and digestive wastes (Maldonado 2016). For the few individuals with negative detrital flux, the concentration of carbon emitted was generally small; therefore, we hypothesize that, similar to conclusions reached by Kahn & Leys (2016) for work on explants of 4 cold-water sponge species, the detritus released by massive species is likely produced as waste, rather than cellular debris resulting from rapid cell turnover.…”

“…See Table 1 for full species names and sample sizes strata; yet, these species consume DOC at high rates and DOC frequently constitutes > 90% of total organic carbon uptake (de Goeij et al 2008b(de Goeij et al , 2013. Instead of growing, it is hypothesized that detritus production results from the rapid proliferation and shedding of cells, primarily choanocytes (de Goeij et al 2009, Alexander et al 2014, 2015, but may also include digestive waste products (Kahn & Leys 2016, Maldonado 2016). This process is energetically costly, and may represent 75% of the total organic carbon (DOC and POC) assimilated (Kahn & Leys 2016).…”

“…There is little information on the physical nature of spongeproduced detritus; however particles < 8 μm have been detected in excurrent seawater using flow cytometry (Yahel et al 2003, McMurray et al 2016, and Wolfrath & Barthel (1989) reported that the sponge Halichondrea panacea excreted detritus in the form of spherical fecal pellets with diameters that ranged from 10 to 55 μm when fed microspheres and unicellular algae. Examinations of detritus within the lumen of sponge excurrent canals have additionally revealed that the detritus has a complex composition and includes choanocytes, archeocytes, spherulous cells, granular cells, and exocytosed vesicles, all generally <10 μm in diameter (Maldonado 2016), and that, closer to the oscula, this detritus may occur as mucal sheets of cellular debris (Alexander et al 2014). …”

Using a thermistor flowmeter with attached video camera for monitoring sponge excurrent speed and oscular behaviour

“…Marine sponges (Porifera), and their associated microbial symbionts, perform many ecologically important functions including: creating and bioeroding substrate, coupling bentho-pelagic biogeochemical fluxes (e.g., carbon, nitrogen, silicon, and phosphorus cycling), forming intricate associations with other organisms (Bell, 2008; Maldonado, Ribes & Van Duyl, 2012), and converting dissolved organic matter to particulate organic matter for use in oligotrophic food webs (De Goeij et al, 2013; Maldonado, 2016). Furthermore, marine sponges are present in a wide variety of habitats from the polar regions to the tropics and from the shallows to the deep sea (Van Soest et al, 2016), and they are often the most abundant, macrobenthic taxa present (Flach et al, 1998; Diaz & Rützler, 2001; Heyward et al, 2010).…”

Microbiomes of the Arctic carnivorous sponges Chondrocladia grandis and Cladorhiza oxeata suggest a specific, but differential involvement of bacterial associates

“…They are a key macrobenthic component in many environments and perform important ecological functions, including the enhancement of biochemical fluxes between benthic and pelagic zones and the conversion of dissolved organic matter into particulate organic matter (Maldonado 2016). The ecological importance of marine sponges is thought to be driven in part by their ability to readily associate with microorganisms.…”