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 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.     

Influence of earthworms and leaf litter on edaphic variables in sewage-sludge-treated soil microcosms

Summary A series of 48 greenhouse soil microcosms were established and treated with combinations of sewage sludge, Acer saccharum leaves, and the earthworms Eisenia fetida and Lumbricus terrestris. The microcosms were incubated at constant moisture for 110 days. Samples were then taken and analysed for sludge depth, organic-matter content, and waterstable soil aggregates. Weights of surface leaves and weights and numbers of surviving earthworms were determined for each microcosm. L. terrestris significantly reduced sludge depth and the surface organic-matter content of microcosm soil and significantly increased percentages of 4-mm diameter water-stable aggregates. Leaf litter also significantly reduced sludge depth and increased 4-mm water-stable aggregates. E. fetida inhibited surface feeding by L. terrestris, reduced its 110-day survival rate, and inhibited the production of 4-mm water-stable aggregates in L. terrestris treatments. Numbers of E. fetida increased in L. terrestris treatments. Sludge depth, organic-matter content and water-stable aggregates were not significantly different from controls in E. fetida treatments.     

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.     

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.     

Life cycle traits of the parthenogenetic earthworm Octolasion cyaneum (Savigny, 1826)

This laboratory-based study provides baseline life cycle data for the obligatory parthenogenetic earthworm Octolasion cyaneum. Singleton and twin hatchlings were cultured individually with biomass, survival and reproductive condition recorded at 4-weekly intervals during a complete year. After maturation, cocoon production, masses and incubation time were also recorded along with viability and number of hatchlings per cocoon. Individual mean mass of singletons was significantly (P < 0.05) greater than twins at the outset (0.042 and 0.025 g respectively) and remained so until week 52 (2.22 and 1.96 g respectively). Singletons matured more rapidly than twins (24 vs. 32 weeks respectively) and produced more cocoons than twins (3.2 and 2.2 coc worm⁻¹ (4 weeks)⁻¹ respectively). Approximately 20% of all viable cocoons produced twins. Singleton hatchlings weighed significantly (P < 0.05) more than twin hatchlings (0.032 and 0.018 g respectively) but there was no significant difference (P > 0.05) between mean masses of singleton (mean masses 0.033 and 0.032 g) or twin (0.017 and 0.018 g) hatchlings produced by singleton and twin parents. The likelihood that a cocoon contained twins or a singleton was not influenced by the singleton/twin status of the parent. There was no significant difference (P > 0.05) in the incubation times of cocoons produced by singletons and twins (129 and 128 days respectively).     

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.     

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.     

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     

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.     

Impact of landspread sewage sludge and earthworm introduction on established earthworms and soil structure

Summary Sewage sludge was applied to twelve 4-m² plots in two forest (mixed hardwood, Norway spruce plantation) site and one old field site. The earthworm Eisenia fetida was introduced to half the control and half the treated plots. Earthworm populations were sampled by formalin extraction and hand-sorting five times in the year following treatment. One year after treatment, soil samples were wet-sieved and water-stable aggregate size-class arrays were determined.The dominant earthworm in the study site, Lumbricus terrestris, increased in density and mean individual biomass in response to sludge treatment in mixed hardwood and old field plots. In the Norway spruce plots, L. terrestris increased in individual biomass but decreased in density following sludge application. The density of the introduced E. fetida rapidly declined in all control plots. One year after introduction, E. fetida was found only in the sludge-treated Norway spruce plot. The introduction of E. fetida with sludge decreased the density and biomass of L. terrestris in the hardwood plots.Sludge treatment increased the percentages of 4-mm diameter water-stable aggregates in old field and hardwood plots. The addition of E. fetida with sludge in the hardwood plots generated no increase in 4-mm water-stable aggregates. In the old field, sludge + E. fetida increased the 4-mm water-stable aggregates. Little change in water-stable aggregates in response to either treatment combination was seen in the Norway spruce site.     

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.     

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.     

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.     

The effect of feeding behavior on Hg accumulation in the ecophysiologically different earthworms Lumbricus terrestris and Octolaseon cyaneum: A microcosm experiment

 A soil microcosm experiment was performed to assess the uptake of Hg from various Hg-spiked food sources (soil, leaf litter and root litter of Trifolium alexandrinum) by two earthworm species, Lumbricus terrestris (anecic) and Octolaseon cyaneum (endogeic). Treatments were applied in which one of the three food sources was Hg spiked and the other two were not. Additional treatments in which all or none of the food sources were Hg spiked were used as controls. Uptake of Hg from soil into tissues of both earthworm species was significantly higher than uptake of Hg from leaf litter or root litter, indicating that soil may be the most important pool for the uptake of Hg into earthworms. In addition, the anecic L. terrestris significantly accumulated Hg from all Hg-spiked food sources (leaf litter, root litter and soil), whereas the endogeic O. cyaneum took up Hg mainly from soil particles. Interestingly, there was no further increase in Hg in L. terrestris when all food sources were Hg spiked compared to the single Hg-spiked sources. This may be attributed to the relatively high Hg content in the soil, which may have influenced the feeding behavior of the earthworms, although their biomass did not significantly decline. We suggest that, in addition to the physiological differences, feeding behavior may also play a role in the contrasting uptake of Hg by the two earthworm species.     

Population dynamics of the earthworm Aporrectodea trapezoides (Annelida: Lumbricidae) in a Western Australian pasture soil

Summary The changes in size and age-composition of an earthworm population were studied in a Western Australian pasture developed since 1912. The population size in the surface 10 cm was estimated by handsorting during the cool wet season (19 weeks from May to September). Two species, both exotic, were found, Aporrectodea tranpezoides (Lumbricidae) and Microscolex dubius (Acanthodrilidae). Of the 615 individual speciemens collected, 99.7% were A. trapezoides. The abundance of A. trapezoides increased from 58 m^-2 at the time of the opening rains to 170 m^-2 (88.6 g live weight m^-2) after 10.5 weeks. Near the end of the wet season (in October) the density was 37 m^-2. At the time of the opening rains the population consisted of juvenile and semimature individuals. Clitellate earthworms were found 1 month later and predominated from August (10.5 weeks) to the end of the season. Egg capsules were found from August through October. Egg capsules incubated in the laboratory at 16°C hatched on average after 42 days and produced two juveniles. Juvenile and immature earthworms collected from a quiescent state at the end of summer matured within 1 month when reared in moist soil in the laboratory.     

Weight response to the soil water potential of the earthworm Aporrectodea longa

Summary To assess the ability of endogeic earthworms to tolerate variations in soil water potential, groups of these worms were subjected to different, constant levels of soil water suction () over a period of 17 days. At water suctions varying from 0.3 kPa (pF 0.5) to 1990 kPa (pF 4.3), the earthworms showed no physiological ability to a maintain constant internal water content as assessed by the fresh weight. The relationship between weight loss and the increase in water, suction was modelled and the following critical thresholds were identified: <60 kPa did not affect earthworm weight; >620 kPa led to diapause; between these two values, earthworm weight was closely governed by the variation in . At the intermediate suction of 167 kPa, the exchange of water between the earthworms and the soil was at a maximum, and this value is therefore proposed as the level at which the diapause is induced. These modelled values were the diapause is induced. These modelled values were compared with those obtained under field conditions.     

Assessment of earthworm contribution to soil hydrology: a laboratory method to measure water diffusion through burrow walls

The capacity for water diffusion in burrow walls (i.e. the coefficient of sorptivity) either burrowed by Lumbricus terrestris (T-Worm) or artificially created (T-Artificial) was studied through an experimental design in a 2D terrarium. In addition, the soil density of earthworm casts, burrow walls (0–3 mm around the burrow) and the surrounding soil (>3 mm) were measured using the method of petroleum immersion. This study demonstrated that the quantity of water which transits through burrows of L. terrestris in the soil matrix was lower than that transited through soil fractures, due to a reduction of soil porosity in burrow walls (compaction: cast > worms burrow walls > surrounding soil > artificial burrow walls). Earthworm behaviour, in particular burrow reuse with associated cast pressing on walls, could explain the larger burrow wall compaction in earthworm burrows. If water diffusion was lower through the compacted burrows, burrow reuse by the worms makes them more stable (worms would maintain the structure over years) than unused burrows. The present experimental design could be used to test and measure the specific differences between earthworm species in their contributions to water diffusion. Probably, these contributions depend on the presumed related-species behaviours which would determine the degree of burrow wall compaction.     

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.