Microbial nitrogen transformations in earthworm burrows

Abstract

Earthworms play an active role in soil nitrogen cycling. Past research has shown that earthworm castings are enriched in NO₃⁻ and NH₄⁺ and show a high potential for microbial nitrification and denitrification. Little information is available on microbial populations and N transformations in the 1–2 mm thick soil lining of earthworm burrows (the drilosphere). We measured nitrifying bacterial populations, denitrifying bacterial populations, nitrification rates and denitrification rates of drilosphere and nondrilosphere soils. These measurements, in addition to measurements of NO₃⁻ concentration, NH₄⁺ concentration, soluble organic-C, pH and water content, were performed on drilosphere material from laboratory microcosms inoculated with Lumbricus terrestris L. and on drilosphere material collected from earthworm burrows in long term no-till plots. The drilosphere soil was enriched in NO₃⁻, NH₄⁺ and soluble organic C and these soils had elevated populations of nitrifying and denitrifying bacteria relative to nondrilosphere soil. Drilosphere soil also had higher nitrification and denitrification rates. We postulate that earthworm-derived C and N deposited in the drilosphere facilitates the enrichment of N-transforming bacterial populations and that the elevated N-transformation rates results in an enrichment of NO₃⁻ in the earthworm burrow. This phenomenon has the potential for increased downward NO₃⁻ transport; however, the extent to which this potential is realized is not known.

Introduction

Earthworms are dynamic members of the soil ecosystem. Earthworms ingest organic material and facilitate the redistribution of crop residues and organic matter throughout the soil profile (MacKay and Kladivko, 1985, Scheu, 1987a, Zhang and Hendrix, 1995). There have been numerous studies of the effects of earthworms on nutrient cycling. It has been observed that earthworm castings contain elevated amounts of NH₄, NO₃, Mg, K and P relative to bulk soil (Lunt and Jacobson, 1944, Parle, 1963, Gupta and Sakal, 1967, Syers et al., 1979, Tiwari et al., 1989). Studies of microbially-mediated N transformations associated with earthworm castings indicate elevated nitrification (Parle, 1963, Syers et al., 1979) and denitrification activities (Svensson et al., 1986, Elliott et al., 1990, Parkin and Berry, 1994). Daniel and Anderson (1992) reported elevated microbial respiration and bacterial counts in earthworm casts, yet no significant change in microbial biomass C.

An important result of earthworm activity is the creation of channels and pores throughout the soil volume. Earthworm burrows facilitate gas exchange and water movement. Earthworm burrows have also been implicated in the preferential flow of water and solutes (Ehlers, 1975, Zachmann et al., 1987, Edwards et al., 1988, Edwards et al., 1988, Edwards et al., 1989) and it has been reported that the walls of earthworm burrows are enriched in NO₃⁻ and labile-C (Syers and Springett, 1983) that may be transported by infiltrating water.

Despite the potential importance of earthworm burrows to the quantity and quality of infiltrating water, there have been few studies of the chemical characteristics of drilosphere (Lavelle, 1988, Binet and Trehen, 1992, Stehouwer et al., 1993, Stehouwer et al., 1994) and none investigating the nitrogen transformations and microbial populations associated with the soil lining earthworm burrows. The microenvironment associated with the walls of earthworm burrows may be substantially different from soil only a few millimeters away. Walls of the burrows of Lumbricus terrestris (L.) are smooth and cemented together with mucous secretions (Lavelle, 1988). The mucous secretions contain high concentrations of organic N and ammonium (Needham, 1957) and may serve as a substrate for fungi and bacteria (Edwards and Fletcher, 1988). Also, earthworm castings that are ejected in the burrow and subsequently pressed into the side of the burrow wall contain elevated amounts of nitrate and ammonium (Edwards and Lofty, 1980). In a study using ¹⁵N-labeled rye residue, Binet and Trehen (1992) observed that the ¹⁵N translocated from the surface applied residue was 3 times greater in the burrow wall than in the surrounding soil. These investigators also determined that most of the burrow-associated N was located in the first 2 mm of the burrow wall.

While it is clear that the soil material associated with earthworm burrows may provide a substantially different environment to soil microorganisms, we are unaware of studies conducted to ascertain the populations or activities of microorganisms responsible for major N transformations in the soil lining earthworm burrows. Our objective was to assess the populations and activities of N-transforming microbial communities the drilosphere in relation to nondrilosphere soil. These determinations were made on drilosphere material generated in laboratory microcosms by L. terrestris (L.) and in drilosphere material collected from earthworm burrows in the field.