Earthworm Ecology and Sustaining Agriculture
by Matthew R. Werner
Center for Agroecology and Sustainable Food Systems, University of California,
Santa Cruz, CA 95064
Reprinted from Components, vol. 1, no.4 (Fall 1990)
University of California Sustainable Agriculture Research & Education Program
Earthworms can play a variety of important roles in agroecosystems. Their feeding and burrowing activities incorporate organic residues and amendments into the soil, enhancing decomposition, humus formation, nutrient cycling, and soil structural development (Mackay and Kladivko, 1985; Kladivko et al., 1986). Earthworm burrows persist as macropores which provide low resistance channels for root growth, water infiltration, and gas exchange (Kladivko and Timmenga, 1990; Zachmann and Linden, 1989). Quality, quantity and placement of organic matter is a main determinant of earthworm abundance and activity in agricultural soils (Edwards, 1983; Lofs-Holmin, 1983), as are disturbances of the soil by tillage, cultivation, and the use of pesticides (Doran and Werner, 1990).
This article will review recent information on earthworms as it relates to the sustainability of agriculture. For further information, see Lee (1985) or Satchell (1983).
Earthworm species can be classed in one of three morpho- ecological groupings (Bouche, 1977 [summary in Lee, 1985]). Epigeic species live in organic horizons and ingest large amounts of undecomposed litter. These species produce ephemeral burrows into the mineral soil for diapause periods only. They are relatively exposed to climatic fluctuations and predator pressures, and tend to be small with rapid generation times. A common example is Eisenia foetida (redworm, manure worm) which is used in vermicomposting.
Endogeic species forage below the surface, ingest large quantities of soil with a preference towards organic rich soil, and build continuously ramifying burrows that are mostly horizontal. These species are apparently not of major importance in litter incorporation and decomposition since they feed on subsurface material. They are important in other soil formation processes including root decomposition, soil mixing, and aeration.
Species which build permanent, vertical burrows that penetrate the soil deeply were termed anecics by Bouche. These species are detritivores and come to the surface to feed on partially decomposed litter, manure, and other organic matter. The permanent burrows of anecics create a microclimatic gradient, and the earthworms can be found shallow or deep in their burrows depending on the prevailing conditions. Anecics have profound effects on organic matter decomposition, nutrient cycling, and soil formation. The most common examples are the nightcrawlers sold by fish-bait dealers consisting of Lumbricus terrestris and Aporrectodea longa.
Palatability of different types of litter to earthworms may depend on nitrogen and carbohydrate content, and the presence of polyphenolics such as tannins (Satchell, 1967). Earthworms prefer materials with a low C/N ratio, such as clovers, to grasses which have a higher C/N ratio (Ruz Jerez et al., 1988). Colonization of litter residues by microorganisms also increases palatability (Cortez et al., 1989), as does leaching of feeding inhibitors.
Benefits of Earthworms
Deep burrowing species such as L. terrestris can burrow through compacted soil and penetrate plough pans, creating channels for drainage, aeration, and root growth (Joschko et al., 1989). Recent work by Shipitalo and Protz (1989) elucidated some of the mechanisms by which earthworms enhance soil aggregation. Ingested aggregates are broken up in a liquid slurry that mixes soil with organic material and binding agents. The defecated casts become stable after drying. Stewart et al. (1988) also presented evidence that earthworms initiate the formation of stable soil aggregates in land degraded by mining.
In forest ecosystems earthworms, especially litter feeders such as L. terrestris, can consume all the litter deposited on the soil surface within a period of several weeks (Knollenberg et al., 1985) or months (Satchell, 1967). Incorporation of litter by earthworms in apple orchards can be an important mechanism for preventing outbreaks of scab fungus, spores of which are transmitted from litter to new foliage by spring rains. Raw (1962) found a high correlation between L. terrestris biomass and apple leaf litter incorporation, with over 90 percent of litter incorporated during the winter when this species was abundant. Incorporation of surface litter may be an important function of earthworms in no-tillage agroecosystems.
Introduction of earthworms to areas not previously populated has led to improvement of soil quality and productivity in New Zealand grassland (Martin, 1977), on drained Dutch polders (Van Rhee, 1977), in heathland in Ireland (Curry and Bolger 1984), and in mining spoils in the U.S. (Vimmerstedt and Finney, 1973).
Earthworm casts are sources of nutrients for plants. Lumbricids in a pasture soil produced casts that contained 73 percent of the nitrogen found in the ingested litter; indicating both the importance of earthworms in incorporating litter nitrogen into the soil and the inefficiency of nitrogen digestion by earthworms (Syers et al., 1979). Earthworms increase the amount of nitrogen mineralized from organic matter in soil. Because nitrification is enhanced in earthworm casts, the ratio of nitrate-N to ammonium-N tends to increase when earthworms are present (Ruz Jerez et al., 1988). Nitrogen-fixing bacteria are found in the gut of earthworms and in earthworm casts, and higher nitrogenase activity, meaning greater rates of N-fixation, are found in casts when compared with soil (Simek and Pizl, 1989).
Earthworms may increase levels of metabolic activity in soils, as measured by the amount of CO2 evolved, yet nematode abundance and microbial biomass may decrease (Yeates, 1981; Ruz Jerez et al., 1988). This occurs because earthworms reduce the amount of substrate available to other decomposers, and because earthworms ingest other decomposer organisms as they feed. This process would tend to accelerate nutrient cycling rates.
Management Effects on Earthworms
Earthworms are not favored by tillage, and in general the greater the intensity and frequency of disturbance, the lower the population density or biomass of earthworms (Haukka, 1988; Mackay and Kladivko 1985; Edwards, 1980; Gerard and Hay, 1979; Barnes and Ellis, 1979). Agricultural soils are generally dominated by species adapted to disturbance, low organic matter content, and a lack of surface litter. Earthworms are dependent on moderate soil moisture content, and cultivation tends to have a negative effect on earthworms by decreasing soil moisture (Zicsi, 1969). Some common agricultural lumbricids are Allolobophora chlorotica, the Aporrectodea caliginosa species complex (A. trapezoides, A. turgida, and A. tuberculata), and L. terrestris. Species common to organic rich habitats, such as E. foetida are rarely found (Lee, 1985).
Earthworm populations are usually significantly depressed in cropped fields relative to pasture or undisturbed lands. Lumbricids in a South African soil were decreased by cultivation to about one-third of original levels. Aporrectodea trapezoides was less affected than Eisenia rosea, possibly because it is able to burrow more deeply in the soil and escape the zone of disturbance (Reinecke and Visser; 1980). Gerard and Hay (1979) reported 93 earthworms per square meter in normally plowed plots, including A. caliginosa, A. chlorotica, A. longa, and L. terrestris. Earthworm abundance increased in plots that received disk cultivation, or no-till treatment Earthworm abundance doubled in no-till soybeans as compared with plowing (Mackay and Kladivko, 1985).
While a major function of tillage is to decrease bulk density of soil and increase porosity, it only increases microporosity. Macropores, which may be of physical or biological origin and which can play an important role in conducting water rapidly into the soil, are destroyed by tillage. For instance, a 67 percent decrease in the rate of infiltration after plowing a tropical forest soil was attributed to the destruction of earthworm burrows. Infiltration in an adjacent arable soil, which was initially much lower than in the forest soil, increased by 23 percent after plowing because the surface crust was broken (Aina, 1984). Infiltration increases in cropped soils when an organic mulch is added in the fall, due to the increased activities of earthworms in these soils and the production of macropores (Slater and Hopp, 1947). Soil compaction caused by agricultural traffic can also decrease earthworm populations (Bostrom, 1986).
A study in Denmark found that 200 T/ha of manure was optimal for increased earthworm abundance and biomass (Andersen, 1980). L. terrestris, A. longa, and A. caliginosa were increased by manure, while A. rosea and A. chlorotica were not influenced The Rothamsted Experiment Station plots in England which received manure for 118 years also had increased earthworm abundance, and inorganic fertilizers in this case caused decreases in earthworm populations (Edwards and Lofty, 1974). Heavy applications of inorganic fertilizers may cause immediate reductions in earthworm abundance (Edwards, 1983).
Organic mulches enhance earthworm habitat by moderating microclimate and supplying a food source. In corn plots in Pennsylvania, earthworms were most abundant in the fall in treatments that were not plowed before winter and where corn residues had been chopped and left as a mulch, regardless of whether the plots were organically or conventionally managed (Werner and Dindal, 1990).
Effects of agricultural pesticides on earthworms depend on the chemical used. Herbicides tend to have low toxicity for earthworms, but can cause population reductions by decreasing organic matter input and cover from weed plants. Fungicides and fumigants tend to be very toxic to earthworms. Application methods may have unique effects on ecological groups of soil animals. For instance, the fungicide benomyl caused reductions of field populations of earthworms. Anecics such as L. terrestriswere most susceptible to surface applications, and were less affected by incorporation of the pesticide into the soil. Because L. terrestris forms permanent burrows, it does not come into contact with subsurface soil beyond its burrow. However; endogeic species such as A. caliginosa, which continuously extend their burrows as they feed in the subsurface soil, were most susceptible when benomyl was incorporated (Edwards and Brown, 1982).
Enhancing Earthworm Populations
There are many creative ways in which a farmer can manage for earthworms. A first step might be to determine what earthworm ecotypes are present, and how abundant they are. Endogeic species are most commonly found. These are useful, but a mixed community including anecic species as well would be even more beneficial, especially for incorporation of surface matter. Direct inoculation is one possible method, but transferring blocks of soil (one cubic foot each) from an area with a large earthworm population into a farm soil might work better. It is also important to consider what species should be introduced, and this is where research specific to seasonally-dry climates in California is needed. Much of our knowledge about earthworms concerns species of one family, the Lumbricidae, which are native to moist temperate areas of Europe. The spread of these earthworms has paralleled European colonialism around the world. They are the only earthworms present in the northeastern US and Canada, where glaciation killed the native fauna. In areas that have a native earthworm fauna, lumbricids often dominate in disturbed habitats. Morphologically, lumbricids are more muscular than any other family of earthworms, suggesting a greater capacity for burrowing (Hartenstein, 1986).
The earthworm fauna in California includes some native species, lumbricid immigrants, as well as immigrants from Asia and South America. From limited personal observations, the lumbricids found in California agricultural soils tend to have small populations that are active for relatively short periods during the wet season. This may reflect agricultural management practices as well as climate effects. There may be species that are adapted to seasonally-dry climates that would flourish in California agricultural soils, if provided the proper conditions.
One management idea for introducing desired species is to set aside a small area of land on a farm to be managed exclusively as an earthworm reservoir. If needed, the soil could be limed to bring it near pH 7, fertilized, and a cover crop established and cut periodically to provide an organic mulch as food and physical cover. In this area a community of the desired species could be established and built up. From this reservoir blocks could periodically be taken and introduced into the field. Rate of spread would vary with species and conditions in the field. Lumbricus terrestris is capable of travelling at least 19 meters on the soil surface in the course of one evening foray (Mather and Christensen, 1988). This is a long term process for establishing earthworms, and would only be successful if ample organic matter was supplied to the soil where earthworms were being introduced, and if physical and chemical disturbances of the soil were minimized. Organically managed perennial crops would be ideal for this method.
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