Regulation of nitrous oxide emission associated with benthic invertebrates

Abstract

1. A number of freshwater invertebrate species emit N 2 O, a greenhouse gas that is produced in their gut by denitrifying bacteria (direct N 2 O emission). Additionally, benthic invertebrate species may contribute to N 2 O emission from sediments by stimulating denitrification because of their bioirrigation behaviour (indirect N 2 O emission). 2. Two benthic invertebrate species were studied to determine (i) the dependence of direct N 2 O emission on the preferred diet of the animals, (ii) the regulation of direct N 2 O emission by seasonally changing factors, such as body size, temperature and NO À 3 availability and (iii) the quantitative relationship between direct and indirect N 2 O emission. 3. Larvae of the mayfly Ephemera danica, which prefer a bacteria-rich detritus diet, emitted N 2 O at rates of up to 90 pmol Ind. )1 h )1 under in situ conditions and 550 pmol Ind. )1 h )1 under laboratory conditions. In contrast, larvae of the alderfly Sialis lutaria, which prefer a bacteria-poor carnivorous diet, emitted N 2 O at invariably low rates of 0-20 pmol Ind. )1 h )1 . The N 2 O emission rate of E. danica larvae was positively correlated with seasonally changing factors (body size, temperature and NO À 3 availability). Direct N 2 O emission by E. danica larvae was limited by low temperature in winter, larval development in spring and low NO À 3 availability in summer. 4. Both E. danica and the non-emitting S. lutaria increased the total N 2 O and N 2 emission from sediment in a density-dependent manner. While N 2 O directly emitted by benthic invertebrates can be partially consumed in the sediment (E. danica), non-emitting species can still indirectly contribute to total N 2 O emission from sediment (S. lutaria).

Shell Biofilm Nitrification and Gut Denitrification Contribute to Emission of Nitrous Oxide by the Invasive Freshwater Mussel Dreissena polymorpha (Zebra Mussel)

“…First, they provide quantitative data for the contribution of shell biofilms to the overall N 2 O emission by a benthic freshwater invertebrate, hence extending earlier qualitative observations on marine invertebrates (11). Second, with a substantial part of N 2 O produced via nitrification, which can be entirely fueled by the mussels' own ammonia excretion, the data suggest that invertebrate-associated N 2 O emissions can be decoupled from environmental nitrate concentrations, one of the main drivers of gut denitrification (19,37,38); in addition, biofilm nitrification may not only directly produce N 2 O but also provide nitrate for denitrification-derived N 2 O production inside the mussel.…”

Emission of nitrous oxide and dinitrogen by diverse earthworm families from Brazil and resolution of associated denitrifying and nitrate-dissimilating taxa

“…The findings also reinforce the likelihood that the capacity of earthworms to emit nitrogenous gases is geographically widespread. Indeed, certain marine invertebrates also emit nitrogenous gases (Stief et al ., ; Heisterkamp et al ., ; Stief & Schramm, ). Current studies are focused on resolving the factors responsible for the paradoxically observed differences in the capacities of contrasting earthworms to emit nitrogenous gases.…”

Direct contribution of clams (Ruditapes philippinarum) to benthic fluxes, nitrification, denitrification and nitrous oxide emission in a farmed sediment

“…High percentage yields of N 2 O associated with isolated benthic invertebrates have generally been attributed to incomplete denitrification within the animal's digestive system (Stief et al, 2009;Heisterkamp et al, 2010;Stief and Schramm, 2010;Svenningsen et al, 2012). It is proposed that denitrifying bacteria ingested by the animals in their diet are sourced primarily from oxic environments such as surficial sediment or the water column.…”

“…It is possible however, that in fact rates associated with the clams in the core incubations were similar to those measured in the laboratory incubations, and that in the more complex and heterogeneous sediment environment there were sinks for the N 2 O produced, which moderated the N 2 O efflux to the overlying water. In a microcosm experiment, Stief and Schramm (2010) found that estimates of sediment-water column N 2 O fluxes based on rates of N 2 O production by denitrification in the gut of the mayfly (Ephemera danica) larvae were~155% of those measured in the microcosms and concluded that part of the N 2 O emitted by the animals was consumed by microbial processes in the surrounding sediment. Therefore, it is possible that part of the N 2 O emitted by the clams was also consumed by denitrifiers in the burrow wall sediments in our study.…”

“…Recently, the hard surfaces, soft tissues and digestive systems of a range of benthic infauna and epifauna have been shown to be colonised by nitrifying and/or denitrifying bacteria, or to exhibit high rates of these processes (Welsh and Castadelli, 2004;Stief et al, 2009Stief et al, , 2010Welsh et al, 2009;Heisterkamp et al, 2010Heisterkamp et al, , 2013Radax et al, 2012;Keesing et al, 2013). Thus, the presence of fauna could directly contribute to local rates of nitrification and denitrification.…”