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 (choanocytes) 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 archeocytes (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 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.