The effect of earthworms (Lumbricidae) on nitrogenase activity in soil

Summary Nitrogenase activity associated with earthworms, their faeces and activity in soil was measured by the acetylene reduction technique. A clear increase in nitrogenase activity was found in field-deposited casts of Aporrectodea caliginosa in comparison with surrounding soil, although potential nitrogenase activity was significantly higher in soil than in casts. Nitrogenase activity associated directly with earthworms (Lumbricus rubellus ) was detected, indicating the presence of active N₂-fixing bacteria on the body surface and/or in the gut. Laboratory experiments showed that nitrogenase activity in the casts of L. rubellus was higher than in unmodified soil, and that nitrogenase activity in soil was significantly increased by the burrowing and feeding activity of these worms. This paper discusses the possible causes of these earthworm effects on soil nitrogenase activity and some methodological problems of determining the nitrogenase activity.     

Effects of earthworm casts and compost on soil microbial activity and plant nutrient availability

Vermicomposting differs from conventional composting because the organic material is processed by the digestive systems of worms. The egested casts can be used to improve the fertility and physical characteristics of soil and potting media. In this study, the effects of earthworm casts (EW), conventional compost (CP) and NPK inorganic fertilizer (FT) amendments on N mineralization rates, microbial respiration, and microbial biomass were investigated in a laboratory incubation study. A bioassay with wheat (Triticum aestivium L.) was also conducted to assess the amendment effects on plant growth and nutrient uptake and to validate the nutrient release results from the incubation study. Both microbial respiration and biomass were significantly greater in the CP treatment compared to EW treatment for the initial 35 days of incubation followed by similar respiration rates and biomass to the end of the study at 70 days of incubation. Soil NO₃⁻ increased rapidly in the EW and CP treatments in the initial 30 days of incubation, attaining 290 and 400 mg N kg⁻¹ soil, respectively. Nitrate in the EW treatment then declined to 120 mg N kg⁻¹ soil by day 70, while nitrate in the CP treatment remained high. While ammonium levels decreased in the CP treatment as nitrate level increased with increasing incubation time, a low level of ammonium was maintained in the EW treatment throughout the incubation. The wheat bioassay study included two additional cast treatments (EW-N and EW2) to have treatments with higher levels of N input. Plants grown with CP or FT treatment had a lower shoot biomass and higher shoot N content than in EW-N and EW-2 treatments, and also showed symptoms of salinity stress. Ionic strength and other salinity indicators in the earthworm cast treatments were much lower than in the CP treatment, indicating a lower risk of salinity stress in casts than in compost. All cast and compost amendments significantly increased wheat P and K uptake compared to either the non-amended control or the mineral fertilizer treatment. The results show that casts are an efficient source of plant nutrients and that they are less likely to produce salinity stress in container as compared to compost and synthetic fertilizers.     

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.     

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     

Density, biomass and vertical distribution ofAporrectodea caliginosa (Savigny 1826) (Oligochaeta, Lumbricidae) in Benghazi, Libya

Studies were conducted during the period May 1993 to April 1994 on the density, biomass and vertical distribution ofAporrectodea caliginosa, a common species of earthworm found in the Benena farms in Benghazi, Libya. The soil of the farm was a clay loam, pH 7.3, and the organic matter averaged 4.2%. Maximum density and biomass ofA. caliginosa were recorded from October to December 1993 and again during March and April 1994, and minimum values were recorded from May to July 1993. A juvenile dominant population was observed during the summer. This was followed by an increase in subadults and adults during the autumn, winter and spring seasons. A positive correlation of the moisture and an inverse correlation of soil temperature on the density and biomass of these animals were discernible. A. caliginosa mainly confined their activities to the surface organic zone (0–10 cm depth) of the soil for most of the months studied.     

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     

Mechanisms of stabilization of earthworm casts and artificial casts

Summary Fresh casts were collected from the earthworm species Aporrectodea caliginosa, and artificial casts were also made. The casts were subjected to ageing, drying-rewetting, and sterilization by hexanol vapour. Clay dispersion was determined, as a measure of the lack of stability of the casts. Two soils were used, the topsoil of a recently reclaimed polder soil in the Netherlands and the topsoil from a South Australian duplex soil. For both soils the fresh worm casts had higher dispersible clay than the artificial casts. During ageing, both types of casts became more stable. There are strong indications that this was mainly due to changes on the surface of the casts. Fungi developed on the surface of 6-day-old worm casts made of Australian soil. This gave a higher stability to the casts compared to artificial casts of the same age without fungal growth. With both types of casts, hexanol inhibited fungal growth on the surface of the casts, reducing the stabilizing effect of ageing. The fungus did not develop on Dutch soil casts until after 42 days, and the development of a higher stability with age was also less marked than in the Australian soil. When the casts were subjected to a drying and rewetting cycle before analysis, they became much more stable than the casts that were analyzed wet. The drying-rewetting cycle removed most of the differences between the worm casts and the artificial casts, and also removed any effects of ageing.Dedicated to the late Prof. Dr. W. Kühnelt     

The hormone-like effect of earthworm casts on plant growth

Summary The fertilizing effect of earthworm casts depends on microbial metabolites, mainly growth regulators. The hormone-like effect of earthworm casts is discussed with reference to the literature and ad hoc experiments. When used in plant propagation, earthworm casts promote root initiation and root biomass and increase root percentage. When applied as a casing layer, earthworm casts stimulate carpophore formation in Agaricus bisporus, and N assimilation. When used in horticulture, earthworm casts have a hormone-like effect, influencing the development and precociousness of plants or inhibiting them. These effects are dependent on dose, application time and plant species. In addition, results recorded on dwarfing, stem elongation and precociousness of flowering suggest that the biological effect of earthworm casts is linked to microbial metabolites that influence plant metabolism, growth and development.     

Phosphorus fractions and dynamics in surface earthworm casts under native and improved grasslands in a Colombian savanna Oxisol

The objective of this study was to assess the effect of a native anecic species on phosphorus availability in an Oxisol characterised by a low chemical fertility. Experiments were carried out at Carimagua research station in a representative site of the isohyperthermic savannas on the Colombian Orinoco basin. One field study and two laboratory/incubation studies were performed in a natural herbaceous savanna and a Brachiaria decumbens and Pueraria phaseoloides pasture. In the laboratory, experiment pots were prepared containing soil collected from the respective field paddock's topsoil. Total P content was higher in earthworm casts than in the surrounding soil in field samples, 50% in native savanna soil and more than 100% in pasture soil. In casts produced under laboratory conditions this increase was relatively low (10-20%). Under field conditions, almost without exception, all P fractions were increased in casts relative to the original soil (corresponding to the increase in total P content), being relatively greater in the labile inorganic P fractions. In addition, samples from the natural savanna showed that pH of casts was higher (5.2) than that of soil (4.6) in both field and laboratory samples. Except in the native savanna under field conditions, the phosphatase activity was reduced in casts by 16.7 to 44%. From our results we conclude that earthworms in the field incorporate P from litter or other organic sources (i.e. undecomposed plant and root material, earthworm faeces) which is not normally measured in the analysis of bulk soil.     

Effect of earthworm casts on protein synthesis inAgaricus bisporus

Summary When earthworm casts were used as a casing, an early fructification, a greater stimulation in fruitbody formation, an increase in the carpophore protein content and in L-¹⁴C-leucine incorporation were observed inAgaricus bisporus. The protein-synthesizing capacity of the carpophore and its protein content were tested on samples collected 28 and 35 days after the casing. An increased L-¹⁴C-leucine incorporation of about 34% and an increased protein content of about 25% were recorded.     

Effect of earthworm casts on protein synthesis in radish (Raphanus sativum) and lettuce (Lactuga sativa) seedlings

Summary The protein-synthesizing capacity of 3-day-old seedlings of radish and lettuce grown in the presence of earthworm casts was investigated using L-¹⁴-C-leucine incorporation. The results showed that earthworm casts increased protein synthesis by 24% for lettuce and 32% for radish, althought no significant differences in protein content were evident.     

Changes in microbial biomass and microbial activity of pig slurry after the transit through the gut of the earthworm Eudrilus eugeniae (Kinberg, 1867)

Here we studied the effects of gut transit through the earthworm Eudrilus eugeniae, on the physicochemical, biochemical, and microbial characteristics of pig slurry, by analyzing fresh casts. The reduction in the dissolved organic C contents in casts we recorded suggests that during digestion, earthworms assimilated labile organic C preferentially, which is a limiting growth factor for them. Furthermore, both microbial biomass and activity in pig slurry were significantly decreased by earthworm gut transit. It appears that E. eugeniae is able to digest microorganisms, although the addition of glucose to the food increased respiration, indicating that growth of microorganisms in casts could be limited by depletion of labile C. Despite reduced microbial biomass and activity, the metabolic diversity of microbial communities was greater in casts than in original pig slurry. Community level physiological profiles obtained from Biolog Ecoplate data revealed that, after earthworm gut transit, the microbial communities in casts and pig slurry were clearly differentiated by their physiological profiles. The results indicate that first stage in vermicomposting of pig slurry by E. eugeniae, i.e., casting, produced changes that will influence the dynamics of the organic matter degradation by reducing forms of N and C available to microorganisms, hence restricting their growth and multiplication. Nevertheless, the reduced microflora of casts was characterized by an increased catabolic potential that might lead to thorough degradation of pig slurry.     

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.     

Relationships between casts of geophagous earthworms (Lumbricidae,Oligochaeta) and matric potential

A laboratory study was conducted to determine the effects of matric potentials between -25.4 and-2.0 kPa on the mechanical dispersion of fresh and aged casts produced by Aporrectodea caliginosa, A. rosea, and A. trapezoides. We also examined the effects on dispersion of the matric potential at which the air-dried casts were rewetted. Dispersion from subsurface casts up to 6 days old and uningested aggregates was influenced, but dispersion from fresh casts was not influenced, by the matric potential of the soil core from which the samples were collected. Dispersion from subsurface casts and uningested aggregates increased as the matric potential of the soil core increased from -25.4 to -2.0 kPa. Cast dispersion was not influenced by the earthworm species which produced the cast. Little or no clay was mechanically dispersed after the casts had been air-dried and rewetted, and the matric potential at which casts were rewetted had little influence on dispersion.     

Potential for higher rates of denitrification in earthworm casts than in the surrounding soil

Summary Earthworms (Lumbricus terrestris L.) were cultured in the laboratory and fed on lucerne (Medicago sativa L.). Denitrification rates in the surface casts and the surrounding soil were quantified using C₂H₂-inhibition of nitrous oxide reductase. The investigation also included determination of the N₂O-formation by nitrification as well as CO₂-formation as a measure of respiration. The denitrification rates of wet earthworm casts were found to be significantly higher than those occurring in wet samples from the soil. The low N₂O-formation observed seemed to be due to denitrification. Respiration was higher in casts, indicating higher oxygen demand which resulted in more anaerobic conditions. The energy supply was probably better in casts compared with the surrounding soil.     

Enhanced root nodulation of subterranean clover (Trifolium subterraneum) byRhizobium leguminosarium biovartrifolii in the presence of the earthwormAporrectodea trapezoides (Lumbricidae)

In a greenhouse study, the effect of the earthwormAporrectodea trapezoides on root nodulation in seedlings of subterranean clover (Trifolium subterraneum) was examined in the presence and absence of addedRhizobium leguminosarium biovartrifolii (strain NA 30). WhenR. trifolii NA 30 was inoculated into dung and placed on the soil surface, the total number of root nodules was five times greater (P<0.001) in the presence of earthworms than without earthworms and the number of nodules on the primary root of the plants 2–8 cm below the soil surface was 4 to 6 times greater (P<0.001) in the presence of earthworms. The additional nodulation did not affect plant growth or foliar N. When NA30 was dispersed through the soil at the beginning of the experiment, the presence of earthworms did not influence the level of root nodulation. The presence of earthworms increased root dry weight by 20–30%, plant top weight by up to 125% (P<0.001), and foliar N by 5–25% (P<0.001). Surface-applied dung increased the dry weight of plant tops (2-to 3-fold,P<0.001) but did not affect the concentration of foliar N (P<0.005).     

Rainfall effects on erosion of earthworm casts and phosphorus transfers by water runoff

 We investigated whether, under a temperate climate and in a maize crop, earthworm casts could contribute to soil erosion and further favour the exportation of phosphorus by runoff waters. Recording of casts was made in compacted (wheel-tracks) and non-compacted inter-rows, for a 2-month period in spring. To assess the rainfall impact on cast evolution, half of the observation sites were protected against rain splash by a nylon mesh placed above the soil surface. The water runoff was collected and analysed for sediment contents and phosphorus concentration. The mean annual production of surface casts was calculated to be 34 kg (dry weight) year^–1 kg^–1 earthworm (fresh weight). Synchronization between cast erosion and rainfall events was shown under natural conditions (unprotected sites). The erosion rate was 4 times greater over rainy periods than dry ones, reaching 80% of cast numbers. It appeared that not the runoff effect but the splash effect, due to the kinetics of the drops, disrupted casts. Newly formed casts disappeared first, with the erosion rate decreasing twofold for casts more than 10 days old. Cast erosion and runoff, as well as worm casting activity, were greater under compacted sites than under non-compacted sites, indicating an influence of earthworms on soil erosion from compacted soils. The total phosphorus content was similar in casts and uningested soil (0.80 mg phosphorus g^–1). Potential phosphorus losses from cast erosion was calculated to reach 25–49 mg phosphorus m^–2 per rainfall event depending on soil compaction. The amounts of particulate phosphorus recovered in water runoff after each rainfall event varied from 1 mg to 11 mg phosphorus. These results are compared and discussed. Received: 20 October 1998     

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.     

Effect of food type and placement on earthworm (Aporrectodea tuberculata) burrowing and soil turnover

Subsurface-dwelling Aporrectodea tuberculata, a common earthworm in Upper-Midwest (USA) agricultural fields, may be a significant component of agroeco-systems with regard to soil mixing and preferential transport of water and chemicals. In this study we looked at effects of food residue placement and food type on A. tuberculata burrowing and soil turnover in two-dimensional Evans box microcosms. Four food residue placements mimicked patterns induced by primary tillage and two food types, readily available and natural food sources, with no food as a control. An average earthworm population of 100 earthworms m^-2 was calculated to generate 1058 km ha^-1 of new burrows and turnover 7.9 Mg ha^-1 of soil in 1 week of activity at 20°C. Burrowing was random until food sources were encountered, at which time burrowing appeared to center around the food source.