by Robert L. Bugg
1994. Sustainable Agriculture/Technical Reviews. 6(3):11-13. Sustainable Agriculture Research and Education Program, Davis, CA.
Earthworms are increasingly recognized as indicators of agroecosystem health and as important tools for ensuring soil improvement and efficient nutrient cycling. In the past, SAREP has highlighted both historical and recent research on earthworms (see Sustainable Agriculture News 3(1): 5,11 and Components 1(4):6-9). The literature has since proliferated rapidly; here we present additional findings from more recent or underexposed research, and include observations from an ongoing demonstration project, Biologically Integrated Orchard Systems: BIOS (see Sustainable Agriculture 5(5):2).
Parmelee et al. (1990) conducted a "piggyback" study in long-term research plots at Horseshoe Bend in north-central Georgia. The long-term trial involved a sandy clay loam soil planted to a soybean-cereal rye-sorghum rotation and managed with vs. without tillage. Aporrectodea caliginosa was the dominant annelid earthworm, and Lumbricus rubellus was also present. No-till management led to a 1.42-fold increase in annelid density and biomass over those observed with conventional tillage. Detailed sampling indicated that densities of Enchytraeidae (small earthworm relatives) were higher under no-till, which contradicted earlier preliminary sampling of the same plots (Hendrix et al., 1986). When the pesticide carbofuran was used on the long-term treatments, it resulted in a 47 percent increase in particulate organic matter under the no-till regime.
Organic Matter and Nitrogen Cycling
Kretschmar and Ladd (1993) conducted a laboratory study of the decomposition of subterranean clover (Trifolium subterraneum) foliage incubated in columns of loamy sand. Clover foliage was incorporated at varying depths and soil was compacted at varying pressures. The earthworm Aporrectodea trapezoides was then added to some columns, but not to others. Results suggested that if herbage was deeply incorporated or the soil highly compacted, the earthworm alleviated the problems of decreased oxidation rates, and thereby promoted decomposition of the residues.
Ruz Jerez et al. (1988) conducted a study on organic matter breakdown and nitrification as influenced by the earthworms Lumbricus rubellus or Eisenia fetida. The study was conducted in 2-liter laboratory glass incubation chambers containing soil (fine sandy loam) and earthworms (10 per chamber). (Reviewer's note: 5 earthworms per liter corresponds to high worm densities in the field.) Dried wilted or senescing clover or grass residue was incorporated into the upper 1 cm of soil in each chamber
Following an initial amount of litter that would correspond to 700 kg dry matter (DM) per hectare, additional litter was added at a rate of 350 kg DM per hectare per week for 10 weeks thereafter. The total addition of clover or grass herbage during the 11 weeks of the study was 4,200 kg DM per hectare. (Reviewer's note: This is about the amount of organic matter that would result from one fairly close mowing of a cover crop of annual grasses, clovers, or medics in a Californian orchard.)
The researchers observed an approximately 50 percent increase in mineral nitrogen after 11 weeks' incubation with earthworms as compared to without; mineral nitrogen was 9 percent higher in chambers that were held at 22.5° C than in those that were held at 15° C. When results were pooled over both temperatures, only 0.6 percent of the clover residue remained, whereas 9 percent of the grass residue was recoverable; this difference is probably related to differences in the residue's carbon-to-nitrogen ratio as well as its palatability to earthworms. In chambers without earthworms, 11.3 percent of the clover residue remained, and 13.7 percent of the grass residue. Microbial biomes was reduced in chambers with earthworms. No information was presented comparing results obtained for Lumbricus rubellus vs. Eisenia fetida.
Test plants (ryegrass [Lolium sp.]) grown in the various treatments following incubation suggested a 25 percent increase in nitrogen uptake following incubation of herbage and soil with, as opposed to without, earthworms. The authors suggested that prior laboratory studies may have underestimated earthworm respiration rates.
Marinissen and de Ruiter (1993) assessed data on the cycling of nitrogen and organic matter from a study in the Netherlands, and from the long-term study in Horseshoe Bend, Georgia (described above under Parmelee et al., 1990). As in the Horseshoe Bend study, the dominant annelid at the Netherlands site was Aporrectodea caliginosa (constituting 92 percent of the wet biomass of annelids). Other species observed at the Netherlands site were Lumbricus rubellus (6%) and Aporrectodea rosea (296). The researchers developed projections for nitrification based on both direct and indirect effects of earthworms. Direct effects were calculated based on varying assumptions concerning production rates of dead tissue, casts, urine, and mucus. Other assumptions that were varied concerned the carbon:nitrogen ratios of the earthworms themselves and of the organic matter being processed. Indirect effects of earthworms were also evaluated, based on the possibilities that: 1) increased grazing by earthworms on microbes stimulates microbial regrowth, and 2) earthworm-induced improvement of soil structure promotes microbial activity.
Projections from the Netherlands data suggested that earthworms are directly or indirectly responsible for nitrification of from 10 to 100 kg nitrogen per hectare per year. Data from Horseshoe Bend, where earthworm densities were higher, suggested corresponding figures of from 82 to 364 kg nitrogen per hectare per year. These widely varying projections reflect a need for more precise assessment of the parameters employed in the models.
Soil Structural Changes
Lee and Foster (1991) composed a review article suggesting that earthworm burrows are important for water infiltration only when irrigation or rainfall exceeds the soil capacity for capillary uptake. Moreover, anecic earthworms (those that make deep, permanent, vertical tunnels) may block burrow entrances with soil or plant material, or position their bodies to obstruct flow down the burrows. Any of these phenomena make earthworm burrows less effective in promoting water infiltration.
Other research has indicated that earthworm casts are frequently more stable than aggregates composed of clay-organic matter complexes. The authors point out that this is not always the case, but they provided no explanation for the discrepancy.
Zhang and Schrader (1993) conducted laboratory studies on the aggregate stability of "natural," worm-induced, and pressure-induced aggregates. Worm-induced aggregates from castings and burrow linings were less stable than "natural"" aggregates, but more so than those formed by human agency through mere compression. The authors considered it unlikely that earthworms rupture mineral particles by compression, but did suggest that the chemical bonds of natural aggregates may be ruptured during ingestion by earthworms. The tensile strength (resistance to crushing) of aggregates formed by the three species of earthworms assessed was as follows: Lumbricus terrestris>Aporrectodea longa>Aporrectodea caliginosa. Tensile strength was positively correlated with organic matter content in the worm-formed aggregates.
Martin (1986) conducted a toxicological study that indicated that Aporrectodea caliginosa is as sensitive or more so to pesticides than are other agriculturally important earthworms. The author suggested that this species would be a logical choice for screening pesticides intended for use in pasture crops or crops grown in rotation with pasture.
Ma et al. (1990) assessed the effects of turfgrass fertilization with six types of nitrogenous fertilizers, including mineral ammonium sulfate, nitrochalk (ammonium nitrate with lime), sulfur-coated urea, organic-coated urea, isobutylidenediurea, and ureaformaldehyde. There were three rates of application for each of the six fertilizers, corresponding to 60, 120, and 180 kg nitrogen per hectare per year. The trial was carried out in a loamy sand soil in Haren, Netherlands, on a turf that included various annual and perennial grasses. Plots were 2.5 x 3.0 m and arrayed in a randomized complete block with two replications for each of 18 treatments.
Results suggested profound reductions caused by ammonium sulfate and by sulfur-coated urea in the endogeic earthworms Aporrectodea caliginosa caliginosa and Aporrectodea rosea. By contrast, the endogeic earthworm Aporrectodea caliginosa tuberculata and the epigeic Lumbricus rubellus showed less reduction. The observed reductions were believed by the authors to have been caused by acidification. (Reviewer’s note: Endogeic species forage below the soil surface in horizontal, branching burrows; epigeic species live in the superficial soil layers and feed on undecomposed plant litter.) Aporrectodea caliginosa tuberculata and Lumbricus rubellus have in the past been noted as tolerant of acid soils, whereas the types of worms showing reductions have been regarded as doing best near neutral pH. Nitrochalk had little effect on earthworm densities, and the other fertilizers had intermediate effects.
Collections From Merced County Almond Orchards
As part of the BIOS project in Merced County, California, seven growers collected earthworms from their orchards. These worms were identified by specialists Matthew Werner of the UC Santa Cruz Agroecology Program and Sam James of Maharishi International University, Iowa.
The endogeic earthworm Aporrectodea caliginosa was the most widely-distributed species, having been collected in all the orchards sampled. This nominal species is now regarded as a complex of three closely related species (Matthew Werner, pers. comm.). As noted in the above synopses, Aporrectodea caliginosa is frequently encountered in other farming systems. It is regarded as having agricultural importance, and diverse feeding habits, including feeding on soft tissue of plant litter at the soil surface or on dead roots below the soil surface (reviewed by Lee, 1985).
Werner noted that specimens of Aporrectodea caliginosa from three of the orchards were unpigmented, indicating a strictly subterranean existence. One of these farms also included Aporrectodea turgida and was the only orchard at which the epigeic species Lumbricus rubellus could be found. Specimens of Aporrectodea caliginosa from the remaining four farms had moderate to heavy pigmentation, suggesting at least occasional above-ground feeding, casting, or travel. On one of these farms, the endogeic species Amynthas diffringens and Microscolex dubius were also collected.
No anecic earthworms were found, nor have obvious middens been seen at any of the BIOS farms. In light of the apparent lack of anecics, Werner has suggested inoculative release of the anecic earthworms Lumbricus terrestris or Aporrectodea longa to promote more rapid litter incorporation. It is striking that three of the four species collected recently at BIOS farms (Aporrectodea caliginosa, Lumbricus rubellus, and Microscolex dubius) are renowned as "peregrine or "wandering" earthworms, because they have frequently been transported by humans to new locations (Lee, 1985).
Hendrix, R.E., R.W. Parmelee, D.A. Crossley Jr., D.C. Coleman, E.R. Odum and R.M. Groffman. 1986. Detritus food webs in conventional and no-tillage agroecosystems. Bioscience 36:374-380.
Kretzschmar, A. and J.N. Ladd. 1993. Decomposition of 14C-labelled plant material in soil: The Influence of substrate location, soil compaction and earthworm numbers. Soil Biology and Biochemistry 25:803-809.
Lee, K.E. 1985. Peregrine species of earthworms. In: Pagliai, A.M. Bonvicini and R. Omodeo (eds.) On Earthworms. Selected Symposia and Monographs, 2 Collani U.Z.I. Mucchi Editore, Modena, Italy. pp. 315-327.
Lee, K.E. and R.C. Foster. l991. Soil fauna and soil structure. Australian Journal of Soil Research 29:745-775.
Ma, Wel-Chun, L. Brussard and J.A. De Ridder. 1990. Long-term effects of nitrogenous fertilizers on grassland earthworms (Oligochaeta: Lumbricidae): Their relation to soil acidification. Agriculture, Ecosystems and Environment 30:71-80.
Marinissen, J.C.Y. and R.C. de Ruiter. 1993. Contribution of earthworms to carbon and nitrogen cycling in agro-ecosystems. Agriculture, Ecosystems and Environment 47:59-74.
Martin, N.A. 1986. Toxicity of pesticides to Allolobophora caliginosa (Oligochaeta: Lumbricidae). New Zealand Journal of Agricultural Research 29:699-706.
Parmelee, R.W., M.H. Beare, W. Cheng, P.F. Hendrix, S.J. Rider, D.A. Crossley Jr., and D.C. Coleman. 1990. Earthworms and enchytraeids in conventional and no-tillage agroecosystems: A biocide approach to assess their role in organic matter breakdown. Biology and Fertility of Soils 10:1-10.
Ruz Jerez, B.E., R.R. Bail, and R.W. Tillman. 1988. The role of earthworms in nitrogen release from herbage residues. In: Jenkinson, D.S. and K.A. Smith (eds.). Nitrogen Efficiency in Agricultural Soils. Elsevier Applied Science, New York, NY. pp. 355-370.
Zhang, H. and S. Schrader. 1993. Earthworm effects on selected physical and chemical properties of soil aggregates. Biology and Fertility of Soils 15:229-234.
For more information write to: R.L. Bugg, Information Group, SAREP. University of California, Davis, CA 95616.