Physicochemical controls on ancient carbon assimilation into ecosystem biomass in shallow-water hydrothermal systems

Hydrothermal vents release substantial amounts of ancient carbon into the ocean, primarily as carbon dioxide, yet the extent to which this carbon is integrated into marine food webs remains poorly constrained. Here, we present a combination of bulk radiocarbon and stable carbon isotope measurements of particulate organic carbon from water column filters with compound-specific hydrogen and radiocarbon isotope analyses of fatty acids from surface sediments to trace carbon assimilation across benthic and pelagic realms in a low pH, shallow-water hydrothermal system off Taiwan. Isotope correlations indicate that vent-derived carbon dioxide constitutes a substantial fraction of the local microbial and faunal biomass through chemoautotrophic pathways (up to ~30%). Farther from the vents, hydrothermal carbon remains detectable and is incorporated into photoautotrophic biomass in the overlying water column. Notably, ancient carbon content in the standing stock of particulate organic carbon was higher at the lower temperature (“White”) vent, even though fluid and sulfide emissions – and thus potential energy availability – were substantially greater at the higher temperature (“Yellow”) vent. These findings show that physicochemical conditions, including pH and temperature, rather than fluid chemistry alone, control carbon assimilation patterns and ultimately limit the retention of vent-derived carbon in this shallow-water system.