Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae)

Summary Microbial respiration, microbial biomass and nutrient requirements of the microflora (C, N, P) were studied in the food substrate (soil taken from the upper 3 cm of the mineral soil of a beech wood on limestone), the burrow walls and the casts of the earthworm Aporrectodea caliginosa (Savigny). The passage of the soil through the gut caused an increase in soil microbial respiration of about 90% over a 4-week period. Microbial biomass was increased only in freshly deposited casts and decreased in aging faeces to a level about 10% lower than in soil. Microbial respiration of the burrow walls was only increased over a shorter period (about 2 weeks). The microflora of the soil and the burrow walls was limited by P, whereas in earthworm casts, microbial growth was limited by the amount of available C. In aging faeces the P requirement of the microflora increased and approached that of the soil. Immobilization of phosphate in earthworm casts is probably caused by mainly abiotic processes. C mineralization by soil microflora fertilized with glucose and P was limited by N, except in freshly deposited casts. Ammonium, not nitrate, was responsible for this process. N dynamics in earthworm casts are discussed.     

Influence of drying and ageing on the stabilization of earthworm (Lumbricidae) casts

The influence of drying and ageing on the stabilization of casts produced by the endoge′ic earthworm, Aporrectodea rosea, from a soil, which was hard-setting and low in organic matter, were investigated in the laboratory. Casts and uningested soil were aged-most for up to 32 days, dried for up to 21 days, or subjected to different wetting and drying cycles over 30 days. The dispersion index of aged-moist casts decreased from 0.40 to 0.25 over 32 days, while dispersion index of dried casts decreased from 0.40 to 0.01 over 21 days. The dispersion index of air-dried casts was not significantly increased by five cycles of wetting and drying. The dispersion index of dried casts was not significantly less than that of dried soil. In soils wetter than a matric potential of approximately –35kPa, stabilization of casts was probably due to a combination of cohesion of soil particles, age-hardening and growth of microorganisms. However, in soils drier than –35kPa, cementation was probably the major mechanism of stabilization. The addition of wheat straw to the soil prior to ingestion by earthworms increased dispersion from aged-moist casts, but did not influence dispersion from dried casts. The addition of wheat straw decreased the number of air-dried casts which slaked severely. The concentration of soluble carbohydrate decreased with dispersion index as casts and uningested soil were each dried. This suggested that soluble carbohydrate may have been denatured with or without being bonded to soil particles during drying. Received: 7 May 1996     

Destabilization of soil during the production of earthworm (Lumbricidae) and artificial casts

The mechanisms by which soil is destabilized in the digestive tract of endogéic earthworms were investigated with artificial casts, which were moulded with a syringe from slurries of a silty loam with or without gypsum and organic matter treatments, and compared to casts produced by Aporrectodea rosea (Lumbricidae). Both types of casts generally had the same levels of mechanical dispersion, observations of slaking, and particle size distribution when the casts were fresh, aged-moist for 30 days, or air-dried. Fresh casts were significantly more dispersive than the uningested soil despite the addition of gypsum or organic matter to the soil. However, the dispersion from aged-moist or air-dried casts was not substantially greater than that of uningested soil. Air-drying was more effective than moist-ageing in increasing the stability of casts and uningested soil. The concentration of soluble carbohydrate was greater in artificial casts produced from soil treated with sheep dung or xanthan gum, and in earthworm casts produced from soil treated with xanthan, than in the uningested soil of the same treatments. An increase in the concentration of soluble carbohydrate was related to an increase in dispersion. An attempt was made to simulate the addition of mucus to soil in the digestive tract of earthworms, by the addition of sucrose or xanthan gum to the slurry during the production of artificial casts. The addition of xanthan, but not sucrose, to the slurry increased mechanical dispersion relative to that of the uningested soil in the fresh treatment. Although the production of artificial casts destabilized soil to the same degree as earthworm casts, the artificial casts did not simulate all chemical, biochemical, and microbiological aspects of digestion. Received: 24 November 1995     

The effect of two endogeic earthworm species on zinc distribution and availability in artificial soil columns

The objective of this study was to determine the impact of earthworm bioturbation on the distribution and availability of zinc in the soil profile.Experiments were carried out with Allolobophora chlorotica and Aporrectodea caliginosa in 24 perspex columns (∅ 10 cm), filled with 20-23 cm non-polluted soil (OM 2%, clay 2.9%, pH 0.01 M CaCl₂ 6.4), that was covered by a 3-5 cm layer of aged zinc spiked soil (500 mg Zn/kg dry soil) and another 2 cm non-polluted soil on top. After 80 and 175 days, columns were sacrificed and each cm from the top down to a depth of 15 cm was sampled. Earthworm casts, placed on top of the soil, were collected. Each sample was analyzed for total and CaCl₂-exchangeable zinc concentrations.Effects of earthworm bioturbation were most pronounced after 175 days. For A. chlorotica, total and CaCl₂-exchangeable zinc concentrations in the polluted layers were lower with than without earthworms. Total zinc concentrations in the non-polluted layers were higher in columns with earthworms. Casts of A. chlorotica collected on the soil surface showed slightly higher total zinc concentrations than non-polluted soil. Casts were found throughout the whole column. For A. caliginosa there were no differences in total zinc concentration between columns with and without earthworms. CaCl₂-exchangeable zinc concentrations in the polluted layers were lower for columns with earthworms. Casts were mainly placed on top of the soil and contained total zinc concentrations intermediate between those in non-polluted and polluted soil layers.This study shows that different endogeic earthworm species have different effects on zinc distribution and availability in soils. A. chlorotica transfers soil throughout the whole column, effectively mixing it, while A. caliginosa decreases metal availability and transfers polluted soil to the soil surface.     

Variables controlling denitrification from earthworm casts and soil in permanent pastures

Summary Denitrification (using the acetylene block method) was determined in earthworm casts and soils from permanent, drained or undrained pasture plots fertilized with 0 or 200 kg N ha^-1 year^-1 as ammonium nitrate. Rates of N₂O production from soil cores were about three times higher from the fertilized than from the unfertilized plots while drainage had a relatively small effect. Denitrification rates from casts were 3–5 times higher than those from soil irrespective of the drainage treatment. Casts generally had higher NO _inf3 ^sup- , NH _inf4 ^sup+ , and moisture contents, and higher microbial respiration rates than soil. Rates of N₂O production were determined primarily by NO _inf3 ^sup- supply, secondarily by moisture; available C did not appear to limit denitrification in these pastures. Estimates of the potential contribution of casts to denitrification ranges from 10.1% of 29.3 kg ha^-1 year^-1 from the unfertilized, drained plot to 22% of 82.5 kg ha^-1 year^-1 from the fertilized undrained plot.     

Factors affecting surface casting behaviour in several species of earthworm

Summary Surface cast production was investigated for several species of earthworms, including some not normally considered to produce surface casts. In single-species culture, the amount of cast material deposited on the surface by different species varied, with Allolobophora chlorotica < Lumbricus rubellus < Aporrectodea caliginosa < Aporrectodea longa. In field communities, results indicated that a single species dominated surface casting activity. The order of species dominance was consistent with the above findings from single-species cultures, if Lumbricus terrestris was considered to be equivalent to Ap. longa.Surface casting is an essential function within earthworm communities which maintains their living space. However, it involves an energy cost and carries a risk of predation. Therefore, there are disadvantages associated with this activity. All of the species studied produced surface casts unless other, usually larger, species were present.     

Peat amendment and production of different crop plants affect earthworm populations in field soil

A field experiment was conducted to study the effects of peat amendment and crop production system on earthworms. The experiment was established on a field previously cultivated with oats and with silt as the main soil type. Perennial crops strawberry, timothy and caraway, and annual crops rye, turnip rape, buckwheat, onion and fiddleneck were cultivated with conventional methods. All the crops were grown with and without soil amendment with peat. Earthworms were sampled twice: 4 and 28 months after establishment of the experiment. In the former case part of the experimental plots were soil sampled and hand sorted for estimation of earthworms. In the latter case all experimental plots were sampled and both soil sampling and mustard extraction was carried out. Soil organic carbon and microbial biomass was measured at 14 and 28 months. Peat increased the abundance of juvenile Aporrectodea caliginosa by 74% in three growing seasons, but had no effect on adult numbers. Lumbricus terrestris numbers were not increased by peat treatment. Three season cultivation of caraway favoured both A. caliginosa and L. terrestris. An equal abundance of A. caliginosa was also found in plots cultivated with turnip rape and fiddleneck. Total earthworm and especially A. caliginosa numbers were very small in plastic-mulched strawberry beds. This was mainly attributed to repeated use of the insecticide endosulfan. With the strawberry plots omitted there was a significant correlation between soil microbial N measured at 14 months and juvenile Aporrectodea spp. and Lumbricus spp. numbers measured at 28 months. Adult earthworm numbers were not associated with either soil organic C or microbial biomass.     

Cropping history and peat amendment-induced changes in strawberry field earthworm abundance and microbial biomass

Common agricultural practices, e.g. soil tillage and organic amendment, may affect field earthworm communities considerably. However, there is little data to show how long the changes persist after a certain action. The effect of peat, commonly used in Finland to improve the horticultural soil structure, on key soil organisms is also largely unknown. Earthworm abundance and microbial biomass were studied in a strawberry field experiment (soil type silty clay) with a history of different crops (strawberry, timothy, caraway, rye, turnip rape, fiddleneck, onion and buckwheat) and peat treatments. Sampling was carried out after three years of perennial cropping of strawberry. Half of the area was peat-amended twice three years apart. The earthworm community consisted mainly of Aporrectodea caliginosa and Lumbricus terrestris. Soil peat amendment almost doubled the number of endogeic A. caliginosa, but had no effect on the anecic L. terrestris. The effect of cropping history on earthworms diminished after three years of strawberry cropping. Only the positive effect of caraway on juvenile Lumbricus spp. was detectable three years after its cropping had been finished. However, some crops had secondary effects on the earthworm distribution without significant influence on their numbers while they were grown, e.g. high numbers of A. caliginosa were recorded from soil with a history of timothy ley. The effect of strawberry cropping was contradictory: six years of continuous strawberry cropping decreased the number of the anecic L. terrestris, but during the last three years on strawberry, the proportion of L. terrestris increased from 6% to 40% in the experimental area with a concomitant great drop in the number of A. caliginosa. The role of different agricultural practices (no tillage, mulching, inter-row grass cover and pesticides) is discussed. The crop-induced changes persisted in the microbial biomass for three years (onion cropping reduced microbial biomass C), but soil amendment had no effect on microbes. The abundance of A. caliginosa was associated with soil organic C, but not with soil microbial biomass.     

Growth rates of Aporrectodea caliginosa (Oligochaetae: Lumbricidae) as influenced by soil temperature and moisture in disturbed and undisturbed soil columns

Earthworm growth is affected by fluctuations in soil temperature and moisture and hence, may be used as an indicator of earthworm activity under field conditions. There is no standard methodology for measuring earthworm growth and results obtained in the laboratory with a variety of food sources, soil quantities and container shapes cannot easily be compared or used to estimate earthworm growth in the field. The objective of this experiment was to determine growth rates of the endogeic earthworm Aporrectodea caliginosa (Savigny) over a range of temperatures (5–20 °C) and soil water potentials (−5 to−54 kPa) in disturbed and undisturbed soil columns in the laboratory. We used PVC cores (6 cm diameter, 15 cm height) containing undisturbed and disturbed soil, and 1 l cylindrical pots (11 cm diameter, 14 cm height) with disturbed soil. All containers contained about 500 g of moist soil. The growth rates of juvenile A. caliginosa were determined after 14–28 days. The instantaneous growth rate (IGR) was affected significantly by soil moisture, temperature, and the temperature×moisture interaction, ranging from −0.092 to 0.037 d⁻¹. Optimum growth conditions for A. caliginosa were at 20 °C and −5 kPa water potential, and they lost weight when the soil water potential was −54 kPa for all temperatures and also when the temperature was 5 °C for all water potentials. Growth rates were significantly greater in pots than in cores, but the growth rates of earthworms in cores with undisturbed or disturbed soil did not differ significantly. The feeding and burrowing habits of earthworms should be considered when choosing the container for growth experiments in order to improve our ability to extrapolate earthworm growth rates from the laboratory to the field.     

Nitrogen mineralization and reorganization in casts of the geophagous tropical earthworm Pontoscolex corethrurus (Glossoscolecidae)

Summary Mineral N concentrations ranged from 133.1 to 167.8 g g^-1 dry soil in fresh casts of the endogeic earthworm Pontoscolex corethrurus fed on an Amazonian Ultisol; this was approximately five times the concentration in non-ingested soil. Most of this N was in the form of NH _inf4 ^sup+ . N also accumulated in microbial biomass, which increased from a control value of 10.5–11.3 to 67.5–74.1 g g^-1 in fresh casts. During a 16-day incubation, part of the NH _inf4 ^sup+ -N was nitrified and/or transferred to the microbial biomass. Total labile N (i.e., mineral+biomas N) decreased sharply at first (ca. 50% in the first 12 h), and then more slowly. The exact fate of this N (microbial metabolites, denitrification, or volatilization) is not known. After 16 days, the overall N content of the casts was still 28% higher than that of the control soil. Incubation of the soil before ingestion by the earthworms significantly increased the production of NH _inf4 ^sup+ in casts. We calculate that in a humid tropical pasture, 50–100 kg mineral N may be produced annually in earthworm casts. Part of this N may be conserved in the compact structure of the cast where the cast is not in close contact with plant roots.     

Growth of Lumbricus terrestris and Aporrectodea caliginosa in an acid forest soil, and their effects on enchytraeid populations and soil properties

A laboratory experiment was carried out to test the hypothesis that the earthworms Lumbricus terrestris and Aporrectodea caliginosa are able to maintain their populations and reproduce in the acid forest soil of a deciduous forest where no lumbricids were found in the field. The experiment was conducted in 45-l containers in which layers of mineral subsoil, humus and organic topsoil collected from the site were established. Both species survived and at least L. terrestris reproduced during the 60 weeks’ incubation. Burrows and middens of L. terrestris were recorded and quantities of litter were consumed. The presence of lumbricids increased the organic matter content of humus, reduced the acidity of the topsoil and humus layers, and suppressed the population of the enchytraeid Cognettia sphagnetorum. A dense population of Enchytraeus albidus was found in L. terrestris middens. It is concluded that edaphic factors do not explain the absence of earthworms, but isolation from cultural landscapes and lack of opportunity to colonize the site from the surroundings is the decisive factor.     

Influence of soil ingestion by earthworms on the availability of potassium in soil: An incubation experiment

Summary An incubation experiment was conducted to study the changes that occur in the K status of soil due to earthworm activity. Samples of Tokomaru silt loam soil were inoculated with the common pasture earthworm species Aporrectodea caliginosa and incubated for 21 days. Aliquots of moist soil were analyzed for exchangeable K by leaching with neutral molar ammonium acetate at 1:50 soil solution ratio. Extraction with boiling 1 M nitric acid at 1:100 soil solution ratio for 20 min was used to determine available non-exchangeable K. The results indicated that the exchangeable K content increased significantly due to earthworm activity but nitric acid-extractable K did not change significantly. It is inferred that earthworms increase the availability of K by shifting the equilibrium among the forms of K from relatively un-available forms to more available forms in the soil chosen for the study.     

Characteristics of earthworm casts affecting herbicide sorption and movement

Various physical and chemical characteristics of earthworm casts collected from a laboratory incubation and a field experiment were examined in relation to their effect on the sorption and the movement of three ¹⁴C-labelled ionic herbicides: atrazine, 2,4-dichlorophenoxyacetic acid, and metsulforon methyl. The earthworm casts contained higher levels of fine fractions and total and soluble C. This is attributed to the grinding action of the earthworm gut and selective feeding on zones with higher organic matter and fine size fractions. The earthworm casts had a higher pH than the source soil, resulting in a higher number of surface negative charges. The earthworm casts sorbed higher amounts of herbicides than the source soil, mainly due to the increases in the amount of organic C and fine size fractions. The incrased sorption of herbicides by the casts resulted in decreased leaching.     

Influence of earthworm activity on aggregate-associated carbon and nitrogen dynamics differs with agroecosystem management

Earthworms are known to be important regulators of soil structure and soil organic matter (SOM) dynamics, however, quantifying their influence on carbon (C) and nitrogen (N) stabilization in agroecosystems remains a pertinent task. We manipulated population densities of the earthworm Aporrectodea rosea in three maize-tomato cropping systems [conventional (i.e., mineral fertilizer), organic (i.e., composted manure and legume cover crop), and an intermediate low-input system (i.e., alternating years of legume cover crop and mineral fertilizer)] to examine their influence on C and N incorporation into soil aggregates. Two treatments, no-earthworm versus the addition of five A. rosea adults, were established in paired microcosms using electro-shocking. A ¹³C and ¹⁵N labeled cover crop was incorporated into the soil of the organic and low-input systems, while ¹⁵N mineral fertilizer was applied in the conventional system. Soil samples were collected during the growing season and wet-sieved to obtain three aggregate size classes: macroaggregates (>250 μm), microaggregates (53-250 μm) and silt and clay fraction (<53 μm). Macroaggregates were further separated into coarse particulate organic matter (cPOM), microaggregates and the silt and clay fraction. Total C, ¹³C, total N and ¹⁵N were measured for all fractions and the bulk soil. Significant earthworm influences were restricted to the low-input and conventional systems on the final sampling date. In the low-input system, earthworms increased the incorporation of new C into microaggregates within macroaggregates by 35% (2.8 g m⁻² increase; P=0.03), compared to the no-earthworm treatment. Within this same cropping system, earthworms increased new N in the cPOM and the silt and clay fractions within macroaggregates, by 49% (0.21 g m⁻²; P<0.01) and 38% (0.19 g m⁻²; P=0.02), respectively. In the conventional system, earthworms appeared to decrease the incorporation of new N into free microaggregates and macroaggregates by 49% (1.38 g m⁻²; P=0.04) and 41% (0.51 g m⁻²; P=0.057), respectively. These results indicate that earthworms can play an important role in C and N dynamics and that agroecosystem management greatly influences the magnitude and direction of their effect.     

Effect of agroforestry woody species on earthworm activity and physicochemical properties of worm casts

The effects of five agroforestry woody species (Dactyladenia barteri, Gliricidia sepium, Leucaena leucocephala, Senna siamea andTreculia africana) on the surface aasting activity ofHyperiodrilus africanus were studied in an Alfisol (Oxic Paleustalf) in southwestern Nigeria. Casting activity under the woody species decreased in the following order:Dactyladenia sp. (26.4 Mg ha^-1 year^-1)>Gliricidia sp. (24.4 Mg ha^-1 year^-1)>Treculia sp. (22.9 Mg ha^-1 year^-1)>Leucaena sp. (18.6 Mg ha^-1 year^-1)>Senna sp. (18.3 Mg ha^-1 year^-1). These differences in casting activity were partly explained by microclimatic effects. Irrespective of the woody species, the worm casts were higher in clay and silt contents, bulk density, water-stable aggregates, pH, organic C, exchangeable cations, effective cation exchange capacity, and extractable P levels than the corresponding surface soils. The woody species did affect the physicochemical properties and P sorption of the worm casts. The content of water-stable aggregates of worm casts decreased in the following order:Dactyladenia sp.>Treculia sp.>Senna sp.>Leucaena sp.>Gliricidia sp. Large differences in extractable P levels were observed.Senna sp. was associated with the highest extractable P level (11.5 mg kg^-1) andTreculia sp. the lowest (4.9 mg kg^-1). P sorption was highest on worm casts underDactyladenia sp. and lowest on those underTreculia sp. Without fertilizer application, there were no significant differences in the dry weight of maize grown in the different worm casts. With NPK applications, the dry weight of maize grown in worm casts associated withTreculia sp. was significantly lower than that of maize grown in the other worm casts, mainly due to the low extractable P level. Despite a high organic C and exchangeable K status, maize grown in the worm casts still responded significantly to N and K applications. The N uptake by maize grown in worm casts associated withTreculia sp. was lower than that in the other treatments.     

Surface cast production by the earthworm Aporrectodea nocturna in a pre-alpine meadow in Switzerland

Field and laboratory experiments were carried out to describe the effects of Aporrectodea nocturna on soil characteristics in a pre-alpine meadow and to support the development of a model of cast production. In the prealpine meadow, increased cast production, first observed about 20 years ago around a newly planted hedge, was recorded to a distance of maximal 170 m from the hedge. Numbers of A. nocturna between 130 and 165 m from the hedge decreased from 164 to 16 individuals m^-2. In the same area cast production steadily decreased from about 1.5 kg m^-2 week^-1 to nil, the plant community structure changed and the microbial biomass decreased, but the root biomass and the moisture content did not change. Laboratory experiments demonstrated that high cast production was not a specific feature of the A. nocturna population nor of the soil in the meadow. Diapause of A. nocturna was terminated in the laboratory during September. A model of cast production potential by the earthworm A. nocturna was established using laboratory determinations of the relationships with body weight, temperature, and water potential. The model was shown to predict cast production in the field given the assumption that the water potential was 0 MPa. According to the model, 81% of surface cast production was by juveniles, and 19% by adults of A. nocturna.     

What happens to earthworm casts in the soil? A field study of carbon and nitrogen dynamics in Neotropical savannahs

In the Oxisols of the eastern plains of Colombia, the large native anecic earthworm Martiodrilus sp. is an abundant ecosystem engineer producing long-lasting casts and burrows. Casts deposited in the soil by this species have been estimated at several tonnes per hectare per year. The physical and chemical processes occurring in these casts have never been studied. In this study, we compared the dynamics of water content (WC), total C (C_tot), and available N (N_avail) contents, and the distribution in size of aggregates in ageing below-ground casts of this species and in the bulk soil. In a native herbaceous savannah and a sown grass/legume pasture (Brachiaria humidicola, Arachis pintoi, Desmodium ovalifolium and Stylosanthes capitata), fresh surface casts were experimentally injected into artificial burrows of 1 cm Ø and 10 cm depth and sampled at different dates during a total period of 120 days. The injection procedure used resulted in a 34% decrease in WC of the casts from the sown pasture and reduced the mean mass diameter (MMD) of the aggregates of casts from the savannah by 19%. Other properties were not significantly affected by the procedure.For injected casts in both grasslands, MMD and C_tot were stable during cast ageing while WC and N_avail were initially at levels several times higher than the bulk soil and decreased to similar bulk soil values with ageing. The C_tot was twice and one third higher in casts compared with the bulk soil in the pasture and the savannah, respectively. Overall means for cast MMD (8.3 and 7.4 mm) were twice as high as those in the bulk soil (3.8 mm) in the savannah and the pasture, respectively. However, MMD was not significantly different between the casts and the bulk soil in two occasions in the pasture. Available nitrogen (N_avail) in injected casts was initially greater than bulk soil levels, reaching maximum levels just after injection (116 and 93 mg kg⁻¹) and remained significantly greater during 1-2 weeks, in the savannah and the pasture, respectively. In conclusion, the tonnes of casts deposited in the soil profile by Martiodrilus sp. each year are likely to contribute greatly to plant nutrition and to the regulation of the soil structure. For each anecic earthworm species, the ecological impact of its below-ground casts is likely to be as important as its surface casts.