Earthworm‐induced N mineralization in fertilized grassland increases both N₂O emission and crop‐N uptake

Abstract

Earthworms can increase plant nitrogen (N) availability by stimulating mineralization of organic matter. However, recent studies show that they can also cause elevated emission of the greenhouse gas nitrous oxide (N 2 O). It is unclear to what extent these two effects occur in fertilized grasslands, where earthworm densities are typically greatest. The aims of this study were therefore to (i) quantify the effects of earthworm activity on N uptake and N 2 O emissions in fertilized grasslands and (ii) link these effects to earthworm functional groups. In a 73-day factorial mesocosm experiment, combinations of Lumbricus rubellus (L r , epigeic), Aporrectodea longa (A l , anecic) and Aporrectodea caliginosa (A c , endogeic) individuals were introduced into columns with grass growing on a fertilized (250 kg N ha −1 ) loamy soil. Introduction of L r resulted in 50.8% (P < 0.001) larger N 2 O emissions and 5.4% (P = 0.032) larger grass biomass. Grass-N uptake increased from 172 to 188 kg N ha −1 in the presence of L r (P < 0.001), from 176 to 183 kg N ha −1 in the presence of A c (P = 0.001), and from 168 to 199 kg N ha −1 when all three earthworm species were present (P = 0.006). L r increased soil NH 4 + -N concentrations (P = 0.010), further indicating enhanced mineralization of N caused by earthworm activity. We conclude that the previously observed beneficial effect of earthworm presence on plant-N availability has a negative side-effect: increased emissions of the mineralized N as N 2 O.

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

“…Both earthworm species appeared to prevent N immobilization, significantly increasing mineral N pool in the bulk soil on days 21 and 90 but preventing it from accumulating in microbial biomass (see Table S3). Consistent with other studies (6,29,35), L. rubellus activity resulted in larger NH 4 ϩ pools on days 21 and 90, indicating enhanced mineralization rates. Nitrogen mineralization by L. rubellus likely resulted from incorporation of maize residue into the soil, as evidenced by an increased pool of mineralizable N on day 89 in treatments with L. rubellus (see Table S2).…”

“…For example, epigeic earthworms primarily reside in the soil-litter interface, mixing into the soil and ingesting fresh organic matter, while endogeic earthworms inhabit deeper soil layers, feeding predominantly on soil organic matter. Several studies have concluded that earthworm-mediated N 2 O emissions depend largely upon ecological feeding strategy (21,29,37).…”

Methanogenic food web in the gut contents of methane-emitting earthwormEudrilus eugeniaefrom Brazil

“…Fermentation products in the gut may serve as substrates for soil-derived denitrifiers and be trophically linked to the in vivo emission of nitrous oxide (N 2 O) and dinitrogen (N 2 ) (Karsten and Drake, 1997;Matthies et al, 1999;Depkat-Jakob et al, 2013). In this regard, earthworms can contribute to the capacity of soils to emit nitrogenous gases (Karsten and Drake, 1997;Matthies et al, 1999;Rizhiya et al, 2007;Lubbers et al, 2011), and it has been postulated that the emission of H 2 by earthworms might drive energy-dependent processes in soil such as the fixation of N 2 or carbon dioxide (CO 2 ) (Wü st et al, 2009a). Soil iron is likewise subject to anaerobic redox transformations during gut passage (Wü st et al, 2009a).…”

Effect of Earthworm Feeding Guilds on Ingested Dissimilatory Nitrate Reducers and Denitrifiers in the Alimentary Canal of the Earthworm

“…On a dry weight basis, earthworms can emit much larger amounts of N 2 O than soils (12,29,31,32,34,42,75,76). The burrowing activities and feeding habits of earthworms, as well as in situ soil conditions, can influence the emission of nitrogenous gases from soils inhabited by earthworms (3,5,34,40,42,54).…”