Association of Earthworm-Denitrifier Interactions with Increased Emission of Nitrous Oxide from Soil Mesocosms Amended with Crop Residue

Abstract

Earthworm activity is known to increase emissions of nitrous oxide (N 2 O) from arable soils. Earthworm gut, casts, and burrows have exhibited higher denitrification activities than the bulk soil, implicating priming of denitrifying organisms as a possible mechanism for this effect. Furthermore, the earthworm feeding strategy may drive N 2 O emissions, as it determines access to fresh organic matter for denitrification. Here, we determined whether interactions between earthworm feeding strategy and the soil denitrifier community can predict N 2 O emissions from the soil. We set up a 90-day mesocosm experiment in which 15 N-labeled maize (Zea mays L.) was either mixed in or applied on top of the soil in the presence or absence of the epigeic earthworm Lumbricus rubellus and/or the endogeic earthworm Aporrectodea caliginosa. We measured N 2 O fluxes and tested the bulk soil for denitrification enzyme activity and the abundance of 16S rRNA and denitrifier genes nirS and nosZ through real-time quantitative PCR. Compared to the control, L. rubellus increased denitrification enzyme activity and N 2 O emissions on days 21 and 90 (day 21, P ‫؍‬ 0.034 and P ‫؍‬ 0.002, respectively; day 90, P ‫؍‬ 0.001 and P ‫؍‬ 0.007, respectively), as well as cumulative N 2 O emissions (76%; P ‫؍‬ 0.014). A. caliginosa activity led to a transient increase of N 2 O emissions on days 8 to 18 of the experiment. Abundance of nosZ was significantly increased (100%) on day 90 in the treatment mixture containing L. rubellus alone. We conclude that L. rubellus increased cumulative N 2 O emissions by affecting denitrifier community activity via incorporation of fresh residue into the soil and supplying a steady, labile carbon source.

Soil fauna diversity increases CO2 but suppresses N2O emissions from soil

“…The only soil faunal group so‐far acknowledged to have a pronounced influence on soil‐derived N 2 O emissions are earthworms (Lubbers, Van Groenigen, et al, ). These macro‐detritivores have been well studied with respect to N 2 O emissions and they can increase N 2 O emissions considerably through interacting with the microbial community (Drake & Horn, ; Nebert, Bloem, Lubbers, & Groenigen, ), by increasing the mineralization of nutrients and altering the soil structure (Lubbers, Brussaard, Otten, & Groenigen, ; Lubbers, Van Groenigen, et al, ). Other macrofauna, such as isopods and grubs, and mesofaunal groups, such as potworms, fungivorous mites and springtails, can also influence N 2 O emissions (Kuiper et al, ; Majeed et al, ; Tianxiang, Huixin, Tong, & Feng, ; Van Vliet, Beare, Coleman, & Hendrix, ).…”

Nitrification inhibitors mitigate earthworm-induced N2O emission—a mesocosm study

“…In this study, E. fetida enhanced 4.2-fold times N 2 O emissions from soil. It was found that L. rubellus increased cumulative N 2 O emissions by 76 % (Nebert et al 2011). Also, the presence of Aporrectodea turgida and Lumbricus terrestris increased the amount N 2 O produced in soil (Chen et al 2014).…”

“…The earthworm-induced N 2 O accounted for the majority of the cumulative N 2 O emission in our mesocosms (Table 1). Nebert et al (2011) reported that L. rubellus increased cumulative N 2 O emissions by affecting activity of denitrifiers through influencing substrates supply. Therefore, we concluded that N 2 O emissions from mesocosms with earthworms (E. fetida) were mitigated by NI application.…”

The soil N cycle: new insights and key challenges

“…A recent meta-analysis on the effect of earthworms on soil greenhouse gas emissions reported an average earthworm-induced increase in N 2 O emissions of 42 % (Lubbers et al, 2013). This was hypothesized to be the result of effects on the denitrifier community as well as changes in soil structure affecting gas diffusivity and anaerobicity Horn, 2006, 2007;Nebert et al, 2011). Further work on soil microbiology and soil structure is needed to determine what are the exact effects of earthworm activity on microbial producers and consumers of N 2 O and on net soil N 2 O emission.…”