Tracing 13C-enriched dissolved and particulate organic carbon in the bacteria- containing coral reef sponge Halisarca caerulea: Evidence for DOM feeding

Here we report on the trophodynamics of the bacteria-containing coral reef sponge Halisarca caerulea. The assimilation and respiration of the 13C-enriched substrates glucose, algal-derived dissolved and particulate organic matter (diatom-DOM and -POM), and bacteria were followed in 1and 6-h incubations. Except for glucose, all substrates were readily processed by the sponge, with assimilation being the major fate. 13C-Enrichment patterns in fatty acid biomarkers revealed that sponge dissolved organic 13C assimilation was both direct and bacteria mediated as tracer carbon was recovered both in bacteria-specific and nonbacterial fatty acid. This is the first direct evidence of DOM incorporation by sponges. The present study demonstrates that the encrusting sponge H. caerulea feeds on both DOM and POM and given their dominant coverage of the largest coral reef habitat (coral cavities) it is proposed that organic matter assimilation by cryptic reef sponges may represent an important, largely overlooked ecological function. Quantitatively significant DOM processing may not be the exclusive function of the microbial world on coral reefs; sponges transform DOM to biomass, and thus retain and store organic matter in the reef system. Sponges are common inhabitants on coral reefs and are widely acknowledged as efficient suspension feeders, preferably filtering small particles (,10 mm) like bacteria and phytoplankton from the passing water (Pile et al. 1996; Ribes et al. 1999). On the open reef sponges co-occur with benthic organisms like corals and algae, whereas in the cryptic reef framework, which forms the largest habitat on well-developed coral reefs (Ginsburg 1983), sponges dominate the cover (Vasseur 1974; Wunsch et al. 2000; Van Duyl et al. 2006). Coral cavities are sinks of bacterioand phytoplankton (Richter et al. 2001; Scheffers et al. 2004). Recently it has been demonstrated that the cryptic reef framework is a major sink of dissolved organic carbon (DOC), with DOC removal rates exceeding bacterioand phytoplankton removal rates by two orders of magnitude (De Goeij and Van Duyl 2007). Heterotrophic bacterioplankton are the dominant consumers of reactive DOC in the ocean (Harvey 2006). However, although the magnitude of eukaryote uptake of DOC is likely to be small relative to prokaryotic uptake, there is growing evidence that some eukaryotes may be directly fueled by DOC, such as flagellates (Tranvik et al. 1993), and invertebrates like bivalves (Roditi et al. 2000). Moreover, evidence is accumulating that tropical sponges are important removers of bulk DOC from the passing water (Yahel et al. 2003; De Goeij et al. 2008). Substantial bulk DOC removal was found by three common encrusting coral cavity sponges, including the sponge Halisarca caerulea, with DOC removal accounting for more than 90% of the total organic carbon removal (De Goeij et al. 2008). The uptake and 1 Corresponding author ([email protected]). Acknowledgments We thank the Caribbean Marine Biology & Ecology (CARMABI) Foundation staff (Curaçao, Netherlands Antilles) and especially Carlos Winterdaal and Brian Leysner for their hospitality and support. We thank Anna de Kluijver for her help in the field. Thanks to Lennart van IJzerloo and Ronald Rutger for technical assistance preparing isotope substrates and performing fatty acid extractions. We also thank Jack Middelburg and Carlo Heip for support of this work. Thanks to Ronnie Nøhr Glud and two anonymous reviewers for constructive comments on the manuscript. This study is financed by the Netherlands Institute for Scientific Research–Netherlands Foundation for the Advancement of Tropical Research (NWO-WOTRO) grant W84-547 and the 6th EU framework project Sustainable production, Physiology, Oceanography, Natural products, Genetics and Economics of Sponges (SPONGES) (project FP6-COOP-CT-2005-017800). Limnol. Oceanogr., 53(4), 2008, 1376–1386 E 2008, by the American Society of Limnology and Oceanography, Inc.