Six months of L-terrestris L. activity in root-formed biopores increases nutrient availability, microbial biomass and enzyme activity

In arable fields, biopores are primarily formed by taproots, but may also be bored by earthworms. Irrespective of the pore origin, repeated use by anecic earthworms yields a wall coating that is rich in carbon, nutrients and microorganisms. However, this effect is halted by routine tillage, and it remains unclear how quickly earthworms are able to alter biopore properties in subsoil. We conducted an earthworm incubation field experiment in arable soil to test the capacity of Lumbricus terrestris to i. increase total nutrient contents including plant available P, ii. alter the microbial community and iii. increase enzyme activities in biopore walls over one vegetation period. Firstly, biopores that contained chicory roots were identified on a plot scale (4.2 x 1.5 m). After two years under fallow, roots were decomposed. We then inserted individual earthworms at 45 cm depth into a subset of these pores, afterwards refilling with topsoil. After six months, earthworms were removed and soil was opened at 45-75 cm and 75-105 cm soil depth layers. The inner pore wall (1 mm) of individual root biopores ('RBP') or root biopores modified by earthworms ('EBP') as well as the bulk soil were sampled in 6 depth intervals of 10 cm each and analyzed for total C, N, S content, plant available P, microbial biomass, phospholipid fatty acids (PLFA) and enzyme activity. Biochemical properties of bulk soil, RBP and EBP clearly differed after one vegetation period as indicated by principal component analysis. PLFA markers of fungi and protozoa were detected only in biopores. Compared with the bulk soil, total C, N, S were enriched in RBP by a factor of 2.0-3.1, plant available P by a factor of 8-10, and microbial biomass by a factor of 12-36. In EBP, all of these parameters were as in RBP or elevated even further (C, N, S: factor 1.0-1.4, plant available P: factor 1.3-1.5, microbial biomass: factor 1.5-2.0, PLFA markers of fungi: factor 2.6-4.4, PLFA markers of protozoa: factor 9.2-14.2). PLFA markers indicative of the ratio of Gram-positive to Gram-negative bacteria (G+: G-) were 5-10 fold lower in RBP than in bulk soil, the microbial metabolic quotient (qCO(2)) was 0.4-0.6 times as high. In EBP, these parameters were further reduced (ratio G+: G-: factor 0.7, qCO(2): factor 0.7-0.8). RBP were particularly characterized by high contents of 10-methyl branched fatty acid indicators of actinobacteria. Activities of enzymes involved in the C-cycle (xylanase, cellobiohydrolase, beta-glucosidase) and N-cycle (chitinase, chitotriosidase, leucine aminopeptidase) were also elevated in RBP as compared to the bulk soil (factor 1.1-3.6) and further increased in EBP (factor 1.2-3.7). All these effects were more pronounced in the 45-75 cm soil layer. We conclude that, in only six months, L. terrestris in arable fields modified ordinarily nutrient-rich biopores into 'super-hotspots' of microbial biomass, enzyme activity and nutrient availabilities. Hence, even short-term promotion of earthworm populations by agricultural management practices can increase microbial biomass and enzyme activity in biopores and its coupling to nutrient mobilization in the subsoil.