Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications

Invertebrate animals that live at the bottom of aquatic ecosystems (i.e., benthic macrofauna) are important mediators between nutrients in the water column and microbes in the benthos. The presence of benthic macrofauna stimulates microbial nutrient dynamics through different types of animal-microbe interactions, which potentially affect the trophic status of aquatic ecosystems. This review contrasts three types of animal-microbe interactions in the benthos of aquatic ecosystems: (i) ecosystem engineering, (ii) grazing, and (iii) symbiosis. Their specific contributions to the turnover of fixed nitrogen (mainly nitrate and ammonium) and the emission of the greenhouse gas nitrous oxide are evaluated. Published data indicate that ecosystem engineering by sediment-burrowing macrofauna stimulates benthic nitrification and denitrification, which together allows fixed nitrogen removal. However, the release of ammonium from sediments is enhanced more strongly than the sedimentary uptake of nitrate. Ecosystem engineering by reef-building macrofauna increases nitrogen retention and ammonium concentrations in shallow aquatic ecosystems, but allows organic nitrogen removal through harvesting. Grazing by macrofauna on benthic microbes apparently has small or neutral effects on nitrogen cycling. Animal-microbe symbioses provide abundant and distinct benthic compartments for a multitude of nitrogen-cycle pathways. Recent studies reveal that ecosystem engineering, grazing, and symbioses of benthic macrofauna significantly enhance nitrous oxide emission from shallow aquatic ecosystems. The beneficial effect of benthic macrofauna on fixed nitrogen removal through coupled nitrification-denitrification can thus be offset by the concurrent release of (i) ammonium that stimulates aquatic primary production and (ii) nitrous oxide that contributes to global warming. Overall, benthic macrofauna intensifies the coupling between benthos, pelagial, and atmosphere through enhanced turnover and transport of nitrogen