Interactions between residue placement and earthworm ecological strategy affect aggregate turnover and N2O dynamics in agricultural soil

Giannopoulos, G.; Pulleman, M.M.; Groenigen, J.W. van


Previous laboratory studies using epigeic and anecic earthworms have shown that earthworm activity can considerably increase nitrous oxide (N2O) emissions from crop residues in soils. However, the universality of this effect across earthworm functional groups and its underlying mechanisms remain unclear. The aims of this study were (i) to determine whether earthworms with an endogeic strategy also affect N2O emissions; (ii) to quantify possible interactions with epigeic earthworms; and (iii) to link these effects to earthworm-induced differences in selected soil properties. We initiated a 90-day 15N-tracer mesocosm study with the endogeic earthworm species Aporrectodea caliginosa (Savigny) and the epigeic species Lumbricus rubellus (Hoffmeister). 15N-labeled radish (Raphanus sativus cv. Adagio L.) residue was placed on top or incorporated into the loamy (Fluvaquent) soil. When residue was incorporated, only A. caliginosa significantly (p <0.01) increased cumulative N2O emissions from 1350 to 2223 µg N2O–N kg-1 soil, with a corresponding increase in the turnover rate of macroaggregates. When residue was applied on top, L. rubellus significantly (p <0.001) increased emissions from 524 to 929 µg N2O–N kg-1, and a significant (p <0.05) interaction between the two earthworm species increased emissions to 1397 µg N2O–N kg-1. These effects coincided with an 84% increase in incorporation of residue 15N into the microaggregate fraction by A. caliginosa (p = 0.003) and an 85% increase in incorporation into the macroaggregate fraction by L. rubellus (p = 0.018). Cumulative CO2 fluxes were only significantly increased by earthworm activity (from 473.9 to 593.6 mg CO2–C kg-1 soil; p = 0.037) in the presence of L. rubellus when residue was applied on top. We conclude that earthworm-induced N2O emissions reflect earthworm feeding strategies: epigeic earthworms can increase N2O emissions when residue is applied on top; endogeic earthworms when residue is incorporated into the soil by humans (tillage) or by other earthworm species. The effects of residue placement and earthworm addition are accompanied by changes in aggregate and SOM turnover, possibly controlling carbon, nitrogen and oxygen availability and therefore denitrification. Our results contribute to understanding the important but intricate relations between (functional) soil biodiversity and the soil greenhouse gas balance. Further research should focus on elucidating the links between the observed changes in soil aggregation and controls on denitrification, including the microbial community