Earthworm effects on selected physical and chemical properties of soil aggregates

Summary Some physical and chemical properties of 1-to 2-mm aggregates obtained from casts and the burrow-wall material of the earthworm species Lumbricus terrestris, Aporrectodea longa, and Aporrectodea caliginosa were determined in order to show the effects of earthworms on the stabilization of soil aggregates. The results were compared with those of the natural soil from the Ap horizon of a Parabraunerde (Luvisol, FAO). Both the tensile strength and the water stability of aggregates from casts and burrow-wall material were reduced compared with those of the natural aggregates but were increased compared with those of remoulded aggregates. These results indicate that to a great extent existing bonds are destroyed by earthworm ingestion. Nevertheless, earthworm activities are advantageous for the stabilization of reformed aggregates. The coarse sand fraction is reduced by selective ingestion by earthworms. The organic C content is increased by 4.1–21.0% for burrow-wall material and by 21.2–43.0% for casts. The carbonate content of aggregates from casts and burrow-wall material of L. terrestris was reduced by more than 50%, while that of A. longa showed no noticeable changes and that of A. caliginosa was increased by more than 60%. The total content of polysaccharides was increased by 35–87% for casts and by 33–46% for the burrow-wall material of all earthworm species. The most frequently detected monosaccharides were glucose, galactose, and glucosamine. L. terrestris appeared to have the strongest effect on the interparticle bonding of the reformed aggregates, measured both as tensile strength and water stability, followed by A. longa and A. caliginosa.     

The earthworm population of a winter cereal field and its effects on soil and nitrogen turnover

The earthworm population in a winter cereal field in Ireland was studied over a 3-year-period and its effects on soil and N turnover were assessed. The mean annual population density was 346–471 individuals m^-2 and the mean biomass was 56.9–61.2 g m^-2. Twelve species were recorded, the most abundant being Allolobophora chlorotica followed by Aporrectodea caliginosa, and 242 mg at 5°C to 713 mg at 10°C in the case of juvenile Lumbricus terrestris. Gut contents (dry mass of soil) comprised 6.7–15.5% of the A. caliginosa live mass, and 9.7–14.7% of the Lumbricus terrestris mass. Annual soil egestion by the field population was estimated as 18–22 kg m^-2. Tissue production ranged from 81.7 to 218.5 g m^-2, while N turnover resulting from mortality was calculated as 1.5–3.9 g m^-2 depending on the year and the method of calculation. Earthworms were estimated to contribute an additional 3.4–4.1 g mineral N to the soil through excretion, mucus production, and soil ingestion. Independent estimates of N output via mucus and excretion derived from ¹⁵N laboratory studies with Lumbricus terrestris were 2.9–3.6 g m^-2 year^-1.     

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.     

Population dynamics of earthworm communities in corn agroecosystems receiving organic or inorganic fertilizer amendments

 The dynamics of earthworm populations were investigated in continuously-cropped, conventional disk-tilled corn agroecosystems which had received annual long-term (6 years) amendments of either manure or inorganic fertilizer. Earthworm populations were sampled at approximately monthly intervals during the autumn of 1994 and spring and autumn of 1995 and 1996. The dominant earthworm species were Lumbricus terrestris L. and Aporrectodea tuberculata (Eisen), which comprised 50–60% and 8–13%, respectively, of the total annual earthworm biomass. Lumbricus rubellus (Hoffmeister) and Aporrectodea trapezoides (Dugés) were much less abundant and contributed a small fraction of total earthworm biomass. Earthworm numbers and biomass were significantly greater in manure-amended plots compared to inorganic fertilizer-treated plots during the majority of the study period. Seasonal fluctuations in earthworm numbers and biomass were attributed to changes in soil temperature and moisture, and cultivation. Unfavorable climatic conditions in the summer and autumn of 1995 caused earthworm abundance and biomass to decline significantly. Mature L. terrestris, L. rubellus and A. tuberculata were most abundant in May and June of 1995 and 1996, and cocoon production was greatest in June and July 1995 and June 1996. Recruitment of juveniles of Lumbricus spp. and Aporrectodea spp. into earthworm communities occurred primarily in the autumn. Long-term amendments of manure or inorganic fertilizer did not change the species composition of earthworm communities in these agroecosystems. The earthworm populations in both manure and inorganic fertilizer plots have declined significantly after 5 years of continuously-cropped corn. Received: 24 August 1997     

Earthworm species composition affects the soil bacterial community and net nitrogen mineralization

Knowledge of the effects of species diversity within taxonomic groups on nutrient cycling is important for understanding the role of soil biota in sustainable agriculture. We hypothesized that earthworm species specifically affect nitrogen mineralization, characteristically for their ecological group classifications, and that earthworm species interactions would affect mineralization through competition and facilitation effects. A mesocosm experiment was conducted to investigate the effect of three earthworm species, representative of different ecological groups (epigeic: Lumbricus rubellus; endogeic: Aporrectodea caliginosa tuberculata; and anecic: Lumbricus terrestris), and their interactions on the bacterial community, and on nitrogen mineralization from ¹⁵N-labelled crop residue and from soil organic matter.Our results indicate that L. rubellus and L. terrestris enhanced mineralization of the applied crop residue whereas A. caliginosa had no effect. On the other hand, L. rubellus and A. caliginosa enhanced mineralization of the soil organic matter, whereas L. terrestris had no effect. The interactions between different earthworm species affected the bacterial community and the net mineralization of soil organic matter. The two-species interactions between L. rubellus and A. caliginosa, and L. rubellus and L. terrestris, resulted in reduced mineral N concentrations derived from soil organic matter, probably through increased immobilization in the bacterial biomass. In contrast, the interaction between A. caliginosa and L. terrestris resulted in increased bacterial growth rate and reduced total soil C. When all three species were combined, the interaction between A. caliginosa and L. terrestris was dominant. We conclude that the effects of earthworms on nitrogen mineralization depend on the ecological traits of the earthworm species present, and can be modified by species interactions. Knowledge of these effects can be made useful in the prevention of nutrient losses and increased soil fertility in agricultural systems, that typically have a low earthworm diversity.     

Experimental evidence for the role of earthworms in compacted soil regeneration based on field observations and results from a semi-field experiment

In laboratory experiments, earthworms are often observed to burrow through compacted soil layers, leading to the general assumption that these animals play a significant role in regenerating compacted soils in agricultural plots. To demonstrate this role under field conditions, the abundance of earthworm macropores inside compacted zones was estimated on plots under reduced (RT) or conventional tillage (CT). Then, different types of compacted zones typically found in CT (plough pan and compacted clods) and RT plots (compacted volume under wheel tracks) were experimentally simulated in wooden boxes, buried in the field and inoculated with different earthworm species. After 6 weeks of incubation, the number of macropores inside the compacted zones was examined. Field observations showed that approximately 10% and 30% of the compacted zones were colonised by at least one macropore in CT and RT plots, respectively. A significantly greater number of anecics was found in RT plots, but we could not conclude that this ecological type of earthworm plays a more major role in the regeneration process in these plots since there were fewer compacted zones and these covered a smaller area in CT. The semi-field experiment provided evidence that earthworm-mediated regeneration of compacted zones is possible and its nature varies between ecological types of earthworm. Lumbricus terrestris, which makes individual burrows that are vertical and deep, was the main species to cross through the plough pan. The other three earthworm species (Aporrectodea giardi, A. caliginosa and A. rosea) did burrow inside the other types of compacted zones (“wheel tracks” and “compacted clods”). In every case, however, macropore density was far greater in non-compacted zones, illustrating that avoidance of compacted soil by earthworms is important and should be taken into account when extrapolating results from laboratory studies.     

Stress protein response (Hsp70) and avoidance behaviour in Eisenia fetida, Aporrectodea caliginosa and Lumbricus terrestris when exposed to imidacloprid

Purpose  

The earthworm species Eisenia fetida and Eisenia andrei are commonly used in ecotoxicological standard tests. In the present study, we compared the sensitivity of E. fetida with that of two soil-dwelling earthworm species (Aporrectodea caliginosa and Lumbricus terrestris) in order to evaluate the capacity of E. fetida to predict effects of the insecticide imidacloprid. Responses were compared using two endpoints, a biochemical (changes in heat shock protein level (hsp70)) and a behavioural (avoidance behaviour).     

Earthworm feeding activity and development of the humus profile

Earthworm casts and digestive tract contents were simultaneously examined, using the same methods, in a recently formed humus profile in a mountain spruce forest. Earthworm species had distinct diets and an earthworm foodweb could be distinguished. Lumbricus terrestris and Aporrectodea icterica were distinct from the other species examined: the former to some extent as a litter consumer, and both species because they excavated mineral material which was deposited within new top layers of the mull humus. Aporrectodea nocturna and Aporrectodea caliginosa both had a non-specific soil feeding mode. Most of the species enriched the humus profile with amorphous organic matter finely incorporated within a mineral matrix. Besides different food selection, a network of burrows was produced as a consequence of the different burrowing behaviour of each earthworm species. Received: 2 January 1997     

Assessment of the burrow system of Lumbricus terrestris, Aporrectodea giardi, and Aporrectodea caliginosa using X-ray computed tomography

Artificially packed soil columns were inoculated with individuals of different earthworm species (Lumbricus terrestris, Aporrectodea giardi or Aporrectodea caliginosa) and placed under controlled conditions in the laboratory. At the end of the incubation period, which lasted 8 months, three-dimensional reconstructions of the burrow system of each species were obtained using X-ray computed tomography. The particular features of the three burrow systems and the differences between them are discussed in terms of density, orientation and distribution of the burrows and the complexity of the network in relation to variations in soil depth and soil density. Received: 5 February 1997     

Worms from the cold: Lumbricid life stages in boreal clay during frost

The vertical distribution and activity of earthworm life stages were studied in an arable field during 0.5 m deep frost. The anecic Lumbricus terrestris L. were below the frost at the bottom of their home burrows (max. depth 1.0 m) and remained there apparently active. Their burrows were open, free of ice and water. The endogeic Aporrectodea caliginosa Sav., mainly small juveniles, were aestivating in the frost layer, which confirms freeze-tolerance in this species. Large A. caliginosa individuals were actively burrowing below the frost down to 1 m depth at soil temperatures close to +1 °C, frost evidently triggering much deeper burrowing than summer droughts. Demonstrating cold-hardiness, viable cocoons of both A. caliginosa and L. terrestris were obtained within a 0-0.25 m layer, frozen for ca. one month prior to sampling. These two common earthworms of boreal soils seem to over-winter in all life stages and remain active below the frost, potentially contributing to the maintenance of subsoil processes during the winter months.     

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.     

Axial and radial pressure exerted by earthworms of different ecological groups

 The aim of this study was to measure the pressures exerted by earthworms during burrowing. For this purpose we developed two methods with which to quantify the axial and radial pressure. The data were recorded with an electronic balance that was connected to a PC. Artificial earthworm burrows were used to standardize the measurements. Plexiglas tubes with diameters ranging from 2 to 6.3 mm which corresponded to the diameter of the earthworms were used. A pin was placed inside the tubes, on which the earthworms exerted a pressure by peristaltic locomotion. Only the maximum values of the pressure measurement were taken into account for evaluation, and the arithmetic mean was calculated. The measurements were conducted with Aporrectodea longa, Lumbricus terrestris, Aporrectodea caliginosa, Octolasion cyaneum, Allolobophora chlorotica, Aporrectodea rosea, Lumbricus rubellus and Dendrobaena octaedra. The species examined were classified into ecological groups. The mean axial pressures exerted by each group were in the order: epigeic (14–25 kPa), endogeic (27–39 kPa) and anecic (46–65 kPa). For the mean radial pressure the order was: epigeic (39–63 kPa), anecic (72–93 kPa) and endogeic (59–195 kPa). It was apparent from the results that radial pressure is the most important pressure with respect to the burrowing activity of earthworms. Received: 28 April 1998     

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.     

Earthworm burrowing behaviour in 2D terraria with single- and multi-species assemblages

Experiments were performed in 2D terraria to investigate the burrowing behaviour of different earthworm species from various ecological categories in single- and multi-species assemblages. The burrowing behaviour was quantified using image analysis software during a 2-week period. Terraria were found to reveal realistic impressions of the burrowing behaviour of various species according to the ecological classification of Bouché into epigeic, endogeic and anecic species. Results of the study also permit the recommending of classifying various earthworms as intermediate species, e.g. Aporrectodea longa as endo-anecic and Lumbricus rubellus as epi-endogeic. Burrowing activity of endogeic species was significantly reduced in multi-species compositions compared to single-species treatments. Moreover, burrowing activity of Octolasion tyrtaeum was significantly reduced in the presence of Lumbricus terrestris compared to the specific single treatment. This endogeic species profited from the burrowing behaviour, e.g. bioturbation, of L. terrestris, and as such this is circumstantial evidence for commensalism (species interaction, in which one partner benefits while the other is unaffected) between anecic and endogeic earthworm species. Simultaneous burrowing activity of a combined assemblage of both endogeic species, Aporrectodea caliginosa and O. tyrtaeum, was also significantly reduced compared with the particular single treatments. Thus, this seems likely to be a response of interspecific competition and trophic niche separation between endogeic species.     

Characterization of the burrow system of the earthworms Lumbricus terrestris and Aporrectodea giardi using X-ray computed tomography and image analysis

 The burrow systems of two earthworm species (Lumbricus terrestris and Aporrectodea giardi) were studied in artificially packed soil columns placed in controlled conditions in the laboratory. At the end of the incubation, which lasted 246 days, the burrow systems were characterized on the undisturbed columns using X-ray computed tomography. This method provided a set of digitized images corresponding to horizontal 3-mm-thick sections. The following parameters were measured using image analysis on each section: number of biopores, their volume, and their individual orientation calculated using an elliptical model of the earthworm channel. The profiles of these parameters through the columns showed that the burrow systems of L. terrestris and A. giardi, which are both anecic species, were very different in terms of total volume, number of burrows, burrow orientation and extension with soil depth. These results led us to conclude that the burrow system of L. terrestris can be considered as a permanent structure whereas that of A. giardi is closer to the burrow system of endogeic species. Received: 12 June 1998     

Effect of management practices and cropping systems on earthworm abundance and microbial activity in Sanborn Field: a 115-year-old agricultural field

Sanborn Field, an agricultural demonstration field at the University of Missouri-Columbia, has over 100 years of cropping histories and management practices implemented at this site. We examined the effect of these cropping systems and management practices on earthworm populations and microbial activity. A field experiment was conducted to characterize and quantify earthworms and to determine the microbial activity in the same selected plots. We sampled 14 plots at the site, six of which were the original plots established in 1888 with the same cropping histories and management, and eight of which had been modified over the years to accommodate changing farmer needs and scientific questions. Earthworms and soil samples were collected in the spring and fall of 1999. Aporrectodea trapezoides, Aporrectodea caliginosa, and Lumbricus terrestris were the dominant species found in this field. Lumbricus terrestris was commonly associated with the no-tillage plot at Sanborn Field. Due partly to soil moisture conditions, most of the species were found and identified during the spring. Microbial activity, as expected, was greatest during the spring. Manure, no-tillage and crop rotations that include legumes had the greatest earthworm abundance and microbial activity. In general, where no fertility treatments were added to soil or where food sources were lacking, earthworm abundance decreased significantly. The abundance of earthworms found in this field reflected the cropping history and management practices used recently and within the last 100 years. In most cases, microbial activity showed similar trends as earthworm density. However, some dynamic microbial transformations, like nitrification, do not always follow the same trend as potential soil quality biotic indicators. Earthworms, along with microbial activity, may serve as useful soil quality indicators in sustained and short-term field trials.     

Homing ability widens the sphere of influence of the earthworm Lumbricus terrestris L.

We report that the deep-burrowing earthworm Lumbricus terrestris L. possesses short-range homing capability. For 2 months we followed the soil surface activity of 18 field-collected L. terrestris in an experimental laboratory population. We recorded 26 cases where an individual after completely leaving its burrow returned to the burrow by backing along its own outward trail. Maximally, homing occurred from a distance of 0.70 m and after more than 3 h on the soil surface. The evolution of homing ability in L. terrestris is most likely related to the importance of the burrow for survival and reproduction. This adaptation also guarantees individuals an expanded foraging area, which we believe can partly explain the remarkable efficiency of L. terrestris in the burial of surface litter.     

Sensitivity of <Emphasis Type="Italic">Eisenia fetida</Emphasis> in comparison to <Emphasis Type="Italic">Aporrectodea caliginosa</Emphasis> and <Emphasis Type="Italic">Lumbricus terrestris</Emphasis> after imidacloprid exposure. Body mass change and histopathology

Purpose  

The use of only one or a few species—representing an entire taxon—in ecotoxicological standard tests poses risk of underestimating the impact of toxicants on the environment. In earthworm ecotoxicity tests, the species Eisenia fetida or Eisenia andrei are commonly used, and there is evidence that these species respond relatively insensitive towards environmental pollution. With the present study, we wanted to evaluate the risk of underestimating effects of the insecticide imidacloprid in soil organisms by comparing E. fetida with two other earthworm species (Aporrectodea caliginosa and Lumbricus terrestris) regarding their sensitivities towards soil contaminated with this widely used insecticide.     

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.     

Earthworm burrowing in laboratory microcosms as influenced by soil temperature and moisture

Earthworm burrows contribute to soil macroporosity and support diverse microbial communities. It is not well known how fluctuations in soil temperature and moisture affect the burrowing activities of earthworms. The objective of this experiment was to evaluate the maximum depth and length of burrows created by the endogeic earthworm Aporrectodea caliginosa (Savigny) and the anecic earthworm Lumbricus terrestris L. for a range of temperatures (5–20 °C) and soil water potentials (−5 and −11 kPa). The laboratory microcosm was a plexiglass chamber (45 cm high, 45 cm wide) containing 0.14 m² of pre-moistened soil and litter, designed to house a single earthworm for 7 days. Earthworm mass, surface casting and burrowing activities were affected significantly by soil temperature, moisture and the temperature×moisture interaction. Burrow length and maximum burrow depth increased with increasing temperature, but there was less burrowing in wetter soil (−5 kPa) than drier soil (−11 kPa). Weight gain and surface casting, however, were greater in soil at −5 kPa than −11 kPa. Our results suggest more intensive feeding and limited burrowing in wetter soil than drier soil. Earthworms inhabiting the non-compacted, drier soil may have pushed aside particles without ingesting them to create burrows. The result was that earthworms explored a larger volume of soil, deeper in the chamber, when the soil was drier. How these burrowing activities may affect the community structure and activity of soil microorganisms and microfauna in the drilosphere remains to be determined.