Effects of endogeic earthworms on soil processes and plant growth in coniferous forest soil

Summary The effects of the endogeic earthworm, Aporrectodea caliginosa tuberculata (Eisen) on decomposition processes in moist coniferous forest soil were studied in the laboratory. The pH preference of this species and its effects on microbial activity, N and P mineralization, and the growth of birch seedlings were determined in separate pot experiments. Homogenized humus from a spruce stand was shown to be too acid for A. c. tuberculata. After liming, the earthworms thrived in the humus and their biomass increased (at pH above 4.8). In later experiments in which the humus was limed, the earthworms positively influenced the biological activity in humus and also increased the rate of N mineralization. A. c. tuberculata increased the growth of birch seedlings, with increases observed in stems, leaves, and roots. Neither NH ₄ ⁺ -N fertilizer nor mechanical mixing with artificial worms affected seedling growth. No plant-growth-affecting compounds (e.g., hormone-like compounds) due to the earthworms were present in the humus. The shoot: root ratio in the birch seedlings was not affected by either the earthworms or the fertilizer. The experiments revealed the impact of earthworm activity on soil processes and plant growth.     

Changes in active microbial biomass by earthworms and grass amendments in agricultural soil

The influence of the earthworm Aporrectodea caliginosa on the biomass and the proportion of active and dormant soil microorganisms after the addition of cut perennial ryegrass (Lolium perenne) to upper soil from agricultural field was studied in a microcosm experiment. During a 2-month period, soil samples were taken 1, 8, 22, 36, 50, and 64 days after cut grass addition. A substrate-induced respiration (SIR) method was used to analyse the samples for total microbial biomass and the distribution of active and dormant microbial biomass. It was found that the addition of grass increased the microbial biomass (SIR) because of an increase in the active microbial biomass. After the initially high values, the active microbial biomass decreased slowly, and at day 64, it was still higher in the grass-amended soils than in the control treatment without grass addition. After 1 day, the active microbial biomass was higher in the soil with A. caliginosa than without the earthworm. At the subsequent samplings, there were no differences in microbial biomass or the proportion of dormant vs active microorganisms between the grass-amended soils. The average from all sampling occasions of SIR was higher in earthworm-treated soil.     

Population and behavioural level responses of arable soil earthworms to boardmill sludge application

The response of earthworms to soil application of boardmill waste sludge was quantified in field and laboratory experiments. The influence of one application of 6×10⁴ tonnes ha⁻¹ of unamended sludge was tested against no application on silty-clay arable soil. After 2 years, results in stubble-cultivated soil showed a 1.7 times lower density of earthworms where sludge was added, whereas there was no difference in average earthworm fresh weight. In direct-drilled soil, there was an indication of lower average numbers of Lumbricus terrestris middens when sludge was applied. Negative impacts in the field may have been due to indirect negative effects of the sludge application. In the laboratory, habitat choice tests were undertaken with two common species from the field site using sludge-based mulch and fertiliser products. Aporrectodea caliginosa showed no discernible preference between soil and soil mixed with unamended sludge (mulch), but favoured soil over soil mixed with sludge and chicken manure (fertiliser). Tests with L. terrestris showed a similar pattern. The preference of L. terrestris for the two products was compared with that for chopped barley straw by direct observation of foraging behaviour. Differences in foraging time of L. terrestris for different feeds were not significant, but mass of straw collected was significantly greater compared with either type of sludge treatment.     

Mixing of different mineral soil layers by endogeic earthworms affects carbon and nitrogen mineralization

The effect of the endogeic earthworm species Octolasion tyrtaeum (Savigny) on decomposition of uniformly ¹⁴C-labelled lignin (lignocellulose) was studied in microcosms with upper mineral soil (Ah-horizon) from two forests on limestone, representing different stages of succession, a beech- and an ash-tree-dominated forest. Microcosms with and without lower mineral soil (Bw-horizon) were set-up; one O. tyrtaeum was added to half of them. It was hypothesised that endogeic earthworms stabilise lignin and the organic matter of the upper mineral soil by mixing with lower mineral soil of low C content. Cumulative C mineralization was increased by earthworms and by the addition of lower mineral soil. Effects of the lower mineral soil were more pronounced in the beech than in the ash forest. Cumulative mineralization of lignin was strongly increased by earthworms, but only in the beech soil (+24.6%). Earthworms predominantly colonized the upper mineral soil; mixing of the upper and lower mineral soils was low. The presence of lower mineral soil did not reduce the rates of decomposition of organic matter and lignin; however, the earthworm-mediated increase in mineralization was less pronounced in treatments with (+8.6%) than in those without (+14.1%) lower mineral soil. These results indicate that the mixing of organic matter with C-unsaturated lower mineral soil by endogeic earthworms reduced microbial decomposition of organic matter in earthworm casts.     

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.     

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.     

Changes in potassium availability and other soil properties due to soil ingestion by earthworms

An incubation experiment was conducted to study the changes that occur in potassium availability and other soil properties with ingestion of soil by earthworms. Two soils were used. Raumai soil with high non-exchangeable K and Milson soil with low non-exchangeable K were incubated with two species of earthworm, Aporrectodea caliginosa and Lumbricus rubellus, for 8 weeks. The casts and soil samples were analysed for exchangeable K, Ca, Mg, Na, and H, pH, organic C, and texture. The results indicated that in Raumai soil, the exchangeable K levels of the casts of both earthworm species were significantly higher than for the control soil, the effect being more marked for L. rubellus than for A. caliginosa. In Milson soil, the exchangeable K levels were significantly lower in the casts of both types of earthworm than in the control soil. The nitric acid-extractable K of the soil and casts was not markedly different for either soil type, but available non-exchangeable K values were significantly higher for the casts of L. rubellus from Milson soil than for the noningested Milson soil. In Raumai soil, the exchangeable Ca was higher in the casts of L. rubellus, exchangeable Mg and H were reduced, and exchangeable Na did not change markedly in the cast compared to the control soil. For Milson soil, the casts contained lower exchangeable Ca and H but higher Na and Mg than the control. The casts of both species of earthworm had significantly higher pH values for both soil types. There was no marked difference in the organic C content of the control soil and cast samples for Milson but a reduction in the casts of A. caliginosa for the Raumai soil. Finer fractions increased in the casts of both earthworm species in both soil types.     

Reproduction and growth of three deep-burrowing earthworms (Lumbricidae) in laboratory culture in order to assess production for soil restoration

Laboratory experiments were conducted to examine the growth and reproduction of three deep-burrowing lumbricids, Aporrectodea longa, Lumbricus terrestris, and Octolasion cyaneum. The reproductive output was recorded as 18.8, 38.0, and 32.3 cocoons per worm per year for A. longa, L. terrestris, and O. cyaneum, respectively. For the same species, maturity was reached at a mean mass of 3.9, 5.0 and 2.4 g, within 3 months from the hatchling stage by L. terrestris and within 4 months by the other two species. The hatching success of cocoons at 15 and 20°C was within the range of 70–80% for each species, except A. longa at the higher temperature, where a viability of 47% was recorded. Twenty percent of viable O. cyaneum cocoons produced twin hatchlings, compared with only one percent for A. longa and L. terrestris. A combination of these results suggests that a complete life-cycle for each species could be achieved within 6 months (L. terrestris and A. longa) or 7–8 months (O. cyaneum). Each species has particular life-cycle strategies that would aid survival and colonisation, under field conditions, if inoculated into restored soils.     

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.     

Growth rates,establishment, and effects on herbage yield of introduced earthworms in grassland on reclaimed cutover peat

Summary Lumbricus terrestris L. juveniles confined in nylon mesh bags grew at mean rates of 6–12 mg ind^–1 day^–1 in reclaimed peat grassland soil, while the growth rates of Aporrectodea caliginosa (Sav.) juveniles were 1.5–2.1 mg ind^–1 day^–1. Earthworm population densities exceeding 700 m² had become established within 1 year adjacent to sods transplanted from an old pasture, while microplots enclosed in nylon mesh cages had mean population densities of 318–408 earthworms m^–2 and biomass of 89–111 g m^–2 3–4 1/2 years after inoculation. Herbage yields were 25% greater in the 2nd year and 49% greater in the 3rd year in earthworm-inoculated microplots which received an annual application of cattle slurry compared with similarly fertilized, non-inoculated cages.Dedicated to the late Prof. Dr. M.S. Ghilarov     

Effect of earthworms on molybdenum-depending activities

Pot experiments performed in an alkaline, silty clay soil showed that the presence of Allolobophora caliginosa increased nitrate reductase activity in maize seedlings and nitrogen fixation in the soil, but did not affect photosynthesis and biomass of maize seedlings and oxygen consumption in the soil. The increase in molybdenum-depending activities is ascribed to the greater availability of molybdenum recorded in the presence of earthworms.     

Endogeic earthworms alter carbon translocation by fungi at the soil-litter interface

The effect of endogeic earthworms (Octolasion tyrtaeum (Savigny)) on the translocation of litter-derived carbon into the upper layer of a mineral soil by fungi was investigated in a microcosm experiment. Arable soil with and without O. tyrtaeum was incubated with ¹³C/¹⁵N-labelled rye leaves placed on plastic rings with gaze (64 μm mesh size) to avoid incorporation of leaves by earthworms. The plastic rings were positioned either on or 3 cm above the soil surface, to distinguish between biotic and chemical/physical translocation of nutrients by fungi and leaching.Contact of leaves to the soil increased ¹³C translocation, whereas presence of O. tyrtaeum reduced the incorporation of ¹³C into the mineral soil in all treatments. Although biomass of O. tyrtaeum decreased during the experiment, more ¹³C and ¹⁵N was incorporated into earthworm tissue in treatments with contact of leaves to the soil. Contact of leaves to the soil and the presence of O. tyrtaeum increased cumulative ¹³CO₂-C production by 18.2% and 14.1%, respectively.The concentration of the fungal bio-indicator ergosterol in the soil tended to be increased and that of the fungal-specific phospholipid fatty acid 18:2ω6 was significantly increased in treatments with contact of leaves to the soil. Earthworms reduced the concentration of ergosterol and 18:2ω6 in the soil by 14.0% and 43.2%, respectively. Total bacterial PLFAs in soil were also reduced in presence of O. tyrtaeum, but did not respond to the addition of the rye leaves. In addition, the bacterial community in treatments with O. tyrtaeum differed from that without earthworms and shifted towards an increased dominance of Gram-negative bacteria.The results indicate that litter-decomposing fungi translocate litter-derived carbon via their mycelial network in to the upper mineral soil. Endogeic earthworms decrease fungal biomass by grazing and disruption of fungal hyphae thereby counteracting the fungal-mediated translocation of carbon in soils.     

Earthworm effects on the use of C sources by microorganisms: Non-linear response to temperature alteration

A microcosm was used to study the effect of the endogeic earthworm Aporrectodea caliginosa (Savigny) on the use of C by microorganisms in a calcareous beech forest soil and its dependence on temperature (5–25%C). Inclusion of ¹⁴C-labelled beech leaf litter made it possible to differentiate between C use by litter-colonizing microflora and by autochthonous soil microflora. The effect of temperature on the soil microbial biomass ¹²C was confined to a significant increase at 15 and 20°C. The size of the ¹⁴C-labelled microbial biomass, in contrast, was positively correlated with temperature. The ¹²C mineralization increased exponentially with temperature. The relationship between ¹⁴C mineralization and temperature, in contrast, followed a logistic curve. Significant main effects of A. caliginosa were confined to ¹²C mineralization, reflecting an increase in ¹²CO₂–C production in the earthworm treatments. The earthworm effects on ¹²CO₂–C production and on ¹⁴C incorporation of the microflora were not linear. The effect of A. caliginosa on ¹²CO₂–C production was most pronouned at intermediate temperatures. It is concluded that temperature alterations affect the microbial use of different C sources in different ways and that the temperature effects can be significantly modified by endogeic earthworms.     

Ability of the earthworms Aporrectodea rosea and Aporrectodea trapezoides to increase plant growth and the foliar concentration of elements in wheat (Triticum aestivum cv. spear) in a sandy loam soil

In a greenhouse study, the ability of the earthworms Aporrectodea rosea and A. trapezoides to influence the foliar concentration of elements and the growth of wheat plants was assessed 27 days after sowing in a sandy loam soil. The presence of A. rosea and A. trapezoides (at densities equivalent to 314 and 471 m^-2, respectively) caused a significant increase in the shoot dry weight of wheat. The presence of A. rosea and A. trapezoides (at densities equivalent to 314 and 157 m^-2, respectively) was also associated with a significant increase in the root dry weight of wheat. The presence of A. rosea caused a significant increase in the foliar concentration of Ca, Cu, K, Mn, N, Na, and P, but did not influence the foliar concentration of Al, B, Fe, Mo, Mg, S, and Zn. The presence of A. trapezoides was associated with a significant increase in the foliar concentration of Al, Ca, Fe, K, Mn, N, and Na, but did not influence the foliar concentration of B, Cu, Mo, Mg, P, S, and Zn. These results demonstrate the potential of A. rosea and A. trapezoides to increase the growth of wheat in a sandy loam soil and suggest that the mechanism by which they increased plant growth was, in part, through increasing the availability and uptake of nutrients from this soil.     

Effects of earthworms on nitrogen mineralization

The influence of earthworms (Lumbricus terrestris and Aporrectodea tuberculata) on the rate of net N mineralization was studied, both in soil columns with intact soil structure (partly influenced by past earthworm activity) and in columns with sieved soil. Soil columns were collected from a well drained silt loam soil, and before the experiment all earthworms present were removed. Next, either new earthworms (at the rate of five earthworms per 1200 cm³, which was only slightly higher than field numbers and biomass) were added or they were left out. At five points in time, the columns were analyzed for NH ₄ ⁺ , NO ₃ ^– , and microbial biomass in separate samples from the upper and lower layers of the columns. N mineralization was estimated from these measurements. The total C and N content and the microbial biomass in the upper 5 cm of the intact soil columns was higher than in the lower layer. In the homogenized columns, the C and N content and the microbial biomass were equally divided over both layers. In all columns, the concentration of NH ₄ ⁺ was small at the start of the experiment and decreased over time. No earthworm effects on extractable NH ₄ ⁺ were observed. However, when earthworms were present, the concentration of NO ₃ ^– increased in both intact and homogenized cores. The microbial biomass content did not change significantly with time in any of the treatments. In both intact and homogenized soil, N mineralization increased when earthworms were present. Without earthworms, both type of cores mineralized comparable amounts of N, which indicates that mainly direct and indirect biological effects are responsible for the increase in mineralization in the presence of earthworms. The results of this study indicate that earthworm activity can result in considerable amounts of N being mineralized, up to 90 kg N ha^–1 year^–1, at the density used in this experiment.     

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.     

Orientation behaviour of earthworms (Lumbricidae) towards different crops

Summary In an outdoor experiment the distribution of earthworms (Lumbricus spp., Allolobophora spp.) under different plant species was studied. Earthworms avoid uncovered areas, but show different reactions under vegetation. This effect reappears in the same manner every year. A particular preference was shown for clover whereas onion was least preferred. Possible reasons for this behaviour are the extent of covering, the moisture regime and exudates of the plants. According to the results obtained the deciding factor seems to be the extent of cover whereas odorous substances are of secondary importance.Dedicated to the late Prof. Dr. M.S. Ghilarov     

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.     

Distribution of earthworms and influence of soil properties across a successional sand dune ecosystem in NW England

An investigation of earthworms across a sand dune system in NW England examined species distribution and abundance with respect to soil physico-chemical conditions and management. Replicated 0.1 m² quadrats were examined every 50 m along 700 m transects across areas of vegetation succession and samples were then taken every 10 m where earthworms were first encountered. A translocation of Aporrectodea longa assessed the ability of this species to live in soils with a high sand content and laboratory work examined growth, maturation and survival of this species in soils with increasing proportions of sand (0–100%). Nine earthworm species were found on the dunes, but none in yellow dunes where organic matter (OM) content was <1%. Dendrobaena octaedra and Lumbricus rubellus were located 300 m from the strand line in grey dunes with an OM content of 3.9%. Allolobophora chlorotica and Lumbricus castaneus occurred within a wet dune slack at 340 m (OM content 11%). In areas of human disturbance (dune car park), A. longa, Aporrectodea caliginosa and Lumbricus terrestris were present, and in soil below pine trees L. castaneus and L. rubellus were present in litter. Laboratory growth of A. longa demonstrated significant (p < 0.05) increases in growth (2–2.75 g) with 25 and 50% sand compared with 0, 75 and 100% over 24 weeks and a greater rate of maturation. Initial results show earthworm colonisation to be influenced by dune successional stage. Laboratory findings suggested A. longa could exist in higher sand content areas but experimental design needs development. The translocation was unsuccessful. Future investigations could examine soil properties more closely and undertake monitoring on site throughout the year.