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

Abstract

Abstract. 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.

Meiofauna increases bacterial denitrification in marine sediments

“…We suggest that this process was particularly important in the direct stimulation of nitrification–denitrification as increased availability of ammonium would have stimulated nitrifiers, and increased availability of nitrate and labile organic compounds would have specifically stimulated heterotrophic denitrification. Moreover, in sediments with more active irrigation by meiobenthos transport of solutes like oxygen, ammonium and nitrate is generally increased in animal burrows2627 resulting in a microhabitat where the essential substrates for nitrifying and denitrifying bacteria are more available1215.…”

“…Macrofaunal activity is generally known to enhance denitrification due to particle reworking and burrowing, ventilation and bioirrigation (refs 14, 15 and references therein) whereas, in some cases, it can negatively impact denitrification and enhance N recycling by means of DNRA stimulation16. Most studies dealing with the effects of fauna on benthic biogeochemistry have considered large animals because they are easy to manipulate in the laboratory and are expected to physically alter microbial pathways and process rates limited by diffusive supply or other constraints (for example, sediment aging, burial to strictly anoxic zones or exhaustion of energy-yielding electron acceptors)161718.…”

Direct Nitrous Oxide Emission from the Aquacultured Pacific White Shrimp (Litopenaeus vannamei)

“…For mollusks, including Mytilus edulis, significant N 2 O production also proceeds in microbial biofilms growing on the shells of the animals (40). This phenomenon can also be expected for the richly sculptured shells of oysters, which have been recognized as keystone species for coastal nitrogen management (63), but to date has not been noted for N 2 O emission, which may be a disadvantage of nitrogen removal stimulated by benthic macrofauna (39,64). The current report on N 2 O emission from L. vannamei should thus inspire further research on N 2 O production directly associated with a larger variety of aquacultured and free-living animals.…”

Application of the isotope pairing technique in sediments: Use, challenges, and new directions

“…This may stimulate D W as compared to D N (i.e. if nitrifiers have not properly established), and underestimate denitrification efficiency due to large NH 4 + efflux, while the opposite maybe be true in the natural environment (Pelegri et al ; Stief ). IPT‐based investigations into the effect of macrofauna on randomly sampled intact sediment cores in which macrofaunal communities were assessed a posteriori are scarce.…”