Sponges belonging to the genus Cliona are common inhabitants of many coral reefs, and as bioeroders, they play an important role in the carbonate cycle of the reef. Several Cliona species maintain intracellular populations of dinoflagellate zooxanthellae (i.e., Symbiodinium spp.), which also form symbioses with a variety of other invertebrates and protists (e.g., corals, molluscs, foraminifera). Unlike the case of coral symbioses, however, almost nothing is known of the metabolic interaction between sponges and their zooxanthella symbionts. To assess this interaction, we performed a tracer experiment to follow C and N in the system, performed a reciprocal transplant experiment, and measured the stable carbon isotope ratio of Cliona spp. with and without zooxanthellae to study the influence of environment on the interaction. We found strong evidence of a transfer of C from zooxanthellae to their sponge hosts but no evidence of a transfer of N from sponge to zooxanthellae. We also saw significant influences of the environment on the metabolism of the sponges. Finally, we observed significant differences in carbon metabolism of sponge species with and without symbionts. These data strongly support hypotheses of metabolic integration between zooxanthellae and their sponge host and extend our understanding of basic aspects of benthic-pelagic coupling in shallow-water marine environments.