Framework cavities are the largest but least explored coral reef habitat. Previous dive studies of caverns, spaces below plate corals, rubble and artificial cavities suggest that cavity-dwelling (coelobite) filter-feeders are important in the trophodynamics of reefs. Quantitative community data are lacking, however, as the bulk of the narrow crevices interlacing the reef framework are inaccessible to conventional analysis methods. Here we have developed endoscopic techniques to explore Red Sea framework crevices up to 4 m into the carbonate rock, revealing a large internal surface (2.5-7.4 m2 per projected m2 reef) dominated by encrusting filter-feeders. Sponges alone provided up to 60% of coelobite cover, outweighing epi-reefal filter-feeder biomass by two orders of magnitude. Coelobite community filtration removed more than 60% of the phytoplankton in the course of its less than 5-minute passage through the crevices, corresponding to an uptake of roughly 0.9 g carbon m-2 d-1. Mineralization of the largely allochthonous organic material is a principal source of nutrients supporting coral and algal growth. The supply of new material by coelobites may provide a key to understanding the 'coral reef paradox'-a rich ecosystem thriving in nutrient-poor water.