Significance of earthworms in stimulating soil microbial activity

 The stimulatory effect of earthworms (Lumbricus terrestris L.) on soil microbial activity was studied under microcosm-controlled conditions. The hypothesis was tested that microbial stimulation observed in the presence of a soil invertebrate would be due to the utilization of additional nutritive substances (secretion and excretion products) that it provides. Changes in microbial activity were monitored by measuring simultaneously CO₂ release and protozoan population density. The increase in CO₂ released in the presence of earthworms was found to result from both earthworm respiration and enhanced microbial respiration. The stimulation of microbial activity was confirmed by a significant increase in protozoan population density, which was 3–19 times greater in the presence of earthworms. The respiratory rate of L. terrestris was estimated to be 53 μl O₂ g^–1 h^–1. Earthworm respiration significantly correlated with individual earthworm weight, but there was no correlation between the increase in microbial respiration and earthworm weight. This finding does not support the hypothesis given above that enhanced microbial respiration is due to utilization of earthworm excreta. A new hypothesis that relationships between microbial activity and earthworms are not based on trophic links alone but also on catalytic mechanisms is proposed and discussed. Received: 26 August 1997     

Biological and physical effects of non-native earthworms on nitrogen cycling in riparian soils

Global nitrogen cycling is being altered by anthropogenic disturbances including invasion by non-native species. European and Asian earthworms have invaded northern temperate forests in North America with dramatic consequences for litter thickness, forest floor plant diversity, and soil nitrogen cycling. Invasive earthworms present at the boundary of terrestrial and aquatic ecosystems (i.e., riparian zones) may alter the flux of nitrogen into adjacent aquatic ecosystems. We examined how nitrogen cycling in riparian soil responds to amendments of invasive earthworms or artificial earthworm burrows. In earthworm-free riparian plots (0.25 m²), we established treatments of invasive earthworms (60 g fresh mass·m⁻²), artificial burrows (120 m⁻²), or control plots and sampled the plots after 30 days. Before and after treatment application we measured major soil characteristics (water-filled pore space, organic matter, and pH), nitrogen pools (exchangeable NH₄⁺ and NO₃⁻), and nitrogen transformation rates (net N-mineralization, net nitrification, and denitrification). Exchangeable NH₄⁺ and NO₃⁻ changed through time but did not differ among treatments. Net N-mineralization and net nitrification rates did not change through time and were similar across all treatments. However, denitrification rates in plots with added earthworms were 4 times greater than rates in control and burrow-only plots, which represents a large rapid increase in gaseous nitrogen flux out of these riparian soils. For all response variables, artificial burrows responded similarly to control plots, suggesting that earthworm biological activity (i.e., feeding, excretion, and mucus production) rather than physical effects (i.e., burrowing and soil aeration) drove the changes in nitrogen cycling. Examination of soil nitrogen pool and flux measurements suggest that this increase in denitrification was coupled with NH₄⁺ consumption by nitrifying bacteria, but future studies are needed to confirm this hypothesis. We conclude that the activity of invasive earthworms in riparian zones can increase the flux of N out of riparian zones, but the hydrologic context of the riparian zone (e.g., pore-water residence time) ultimately controls whether denitrification or nitrate leaching is the dominant flux of N.     

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.     

The effect of earthworm coprolites on the soil water retention curve

The effect of earthworm coprolites on the water retention curves in soils of different geneses and textures was investigated by the method of equilibrium centrifuging. Coprolites sampled in the field were compared with the surrounding soil. The effect of earthworms on a soddy-podzolic light loamy soil (from Moscow oblast) was comprehensively analyzed in the course of a special model experiment in a laboratory. This experiment was necessary because it was difficult to separate the coprolites from the soil, in which additional coprolites could appear under natural conditions. In all the variants of the experiment, the differences between the water retention curves of the coprolites and the surrounding soil (or control substrates unaffected by earthworms) were statistically significant. The development of coprolites favored a considerable increase (up to 20 wt.% and more) of the soil water retention capacity upon equivalent water potentials within the range from 0 to ?1000 kPa. In most cases, the soil water retention capacity increased within the entire range of the soil moisture contents. This could be explained by the fact that strongly swelling hygroscopic plant remains (detritus) were included into the coprolites and by the formation of a specific highly porous aggregate structure.     

Darwin's earthworms revisited

Down House was Charles Darwin's home from 1842 until his death in 1882 and where he wrote “The Formation of Vegetable Mould through the Action of Worms”. The work described here is based upon passages from this book and from further observations on earthworms in this area. General observations were made in addition to systematic sampling in areas selected either from signs of earthworm activity, habitat type or in direct relation to Darwin's documented work.Greatest species richness (n = 9) was found in Middle Field. Greatest earthworm density was present in Darwin's Kitchen Garden (715 m⁻²) with the largest associated biomass (261 g m⁻²). Aporrectodea longa was the most abundant species. Lumbricus terrestris, described by Darwin in terms of its behaviour, but not directly named, was located in relatively low numbers, but its diagnostic middens and associated burrows were easily detected. Earthworms associated with Darwin's cinder and chalk application experiments were also examined. In total, 19 of Britain's 28 earthworm species were located within the nominated World Heritage Site.     

土壤中亚致死剂量毒死蜱对蚯蚓抗氧化防御系统酶活性的影响

以赤子爱胜蚓(Eisenia fetida)为供试生物,研究了暴露于含有亚致死剂量毒死蜱的人工土壤中8周时间内蚯蚓超氧化物歧化酶(SOD)、过氧化氢酶(CAT)、谷胱甘肽过氧化物酶(GSH-Px)活性的变化。结果表明,毒死蜱对蚯蚓SOD、CAT、GSH-Px酶活性具有显著抑制。蚯蚓抗氧化防御系统酶对毒死蜱毒性具有一定的指示作用。除蚯蚓的LC50、产卵率、卵孵化率等常用的蚯蚓生态毒理学指标外,蚯蚓的SOD、CAT、GSH-Px抗氧化酶活性与实验农药的毒性效应具有相关性,但各指标在对毒性的响应敏感性上存在差异,其中,SOD、GSH-Px最为敏感,而CAT最不敏感。因此,在生态毒性诊断时,应选择不同指标作为一套指标体系相互补充,以增强污染诊断的灵敏性及长期诊断。     

Biological activity of acetylated phenolic compounds

In recent years an effort has been made to isolate and identify biologically active compounds that are included in the Mediterranean diet. The existence of naturally occurring acetylated phenolics, as well as studies with synthetic ones, provide evidence that acetyl groups could be correlated with their biological activity. Platelet activating factor (PAF) is implicated in atherosclerosis, whereas its inhibitors seem to play a protective role against cardiovascular disease. The aim of this study was to examine the biological activity of resveratrol and tyrosol and their acetylated derivatives as inhibitors of PAF-induced washed rabbit platelet aggregation. Acetylation of resveratrol and tyrosol was performed, and separation was achieved by HPLC. Acetylated derivatives were identified by negative mass spectrometry. The data showed that tyrosol and its monoacetylated derivatives act as PAF inhibitors, whereas diacetylated derivatives induce platelet aggregation. Resveratrol and its mono- and triacetylated derivatives exert similar inhibitory activity, whereas the diacetylated ones are more potent inhibitors. In conclusion, acetylated phenolics exert the same or even higher antithrombotic activity compared to the biological activity of the initial one.     

Burrowing activity of the earthworms Lumbricus terrestris and Aporrectodea giardi and consequences on C transfers in soil

Two earthworms species, Lumbricus terrestris (epianecic) and Aporrectodea giardi (anecic) were incubated in microcosms with an epigeic ¹³C-labelled litter for 246 d. At the end of the experiment, different soil compartments (surface casts, walls and peripheries of burrows, and surrounding soil) were sampled for ¹³C analysis. Two-dimensional images acquired using X-ray computed tomography allowed to estimate the weight of the ‘burrow wall’ and ‘burrow periphery’ compartments which are required to establish C balance. In the case of L. terrestris, the formed structures were more C litter enriched compared to the other species. The permanent character of the burrow system could lead to a high and constant enrichment of the entire burrow system. As consequence, the percentage of C litter in the ‘burrow wall’ and ‘burrow periphery’ compartments was important in spite of their low volume. The denser system developed by A. giardi resulted in C litter dilution in the whole formed structures. The C litter enrichment decreased with the soil depth, but owing to the intensity of the burrowing activity, the C litter transfers into the ‘burrow walls’ and ‘burrow periphery’ were important and the C litter was homogeneously distributed throughout the whole column.     

Influence of soil properties on the population and activity of geophagous earthworms after five years of bare fallow

Many soil properties influence earthworm populations and activity. To determine which properties are of significance, a broad collection of soils was investigated. Samples from these different soils were kept bare at one site in large plots (3 Mg soil per plot) to liminate crop and weather interference and to isolate the dominating mechanisms of earthworm effects. Earthworm density, biomass, and tunnelling activity were assessed after 5 years of bare fallow. All earthworm parameters varied strongly. Earthworms increased soil respiration by their tunnelling activity, and in turn increased microbial activity and propagated the loss of organic C. Earthworm abundance ranged from 12 to 274 m^-2 and was about 10 times greater than on cropped soils. The range in abundance was mainly caused by variations in the numbers of juveniles. The average soil moisture content was the only soil property among the many properties investigated that was consistently correlated with earthworm abundance and biomass. Even after 5 years of bare fallow with almost no addition of fresh plant biomass and with little water loss by plant transpiration, the earthworm population was controlled by water stress and not by food stress. We therefore conclude that high water consumption by productive crops may degrade the habitat for geophagous earthworms.     

Biological activity of chernozems in the center of the Russian Plain

Specific features of the microbiological and enzymatic activity of chernozems are considered in genetically associated and technogenic series. The biological processes in chernozems follow the main soil-geographical regularities inherent to the Central Chernozemic region. The biological characteristics of the chernozems reflect the dynamic properties of the microorganisms habitat and are indicators of their technogenic degradation. Plowing of chernozems and their intense agricultural use is accompanied by changes in their biological activity. The disturbances revealed in the biosystem of the chernozems caused by plowing and fertilization were of a functional, i.e., reversible character. The changes in the intensity of the biochemical processes in the chernozems were observed only under the long-term application of fertilizers (for not less than 10 years). A single application of fertilizers caused temporary changes.     

Biological activity of ant nests in the middle taiga zone

Ants are the most widespread social insects. Many species of ants influence a range of soil properties when building their nests in soil. The paper discusses the effects of ants on soil biological activity (nitrogen fixation, denitrification), as well as on biomass and the diversity of microorganisms. In many cases, these processes were more active in anthills. Changes in soil pH caused by nest-building activity of ants were also. There were no patterns in the distribution of pH values. Specific differences between microbial complexes of anthills and corresponding reference soils were revealed.     

Biological activity of alpine mountain-meadow soils in the Teberda Reserve

The intensity of the actual and potential CO₂ emissions, nitrogen fixation, denitrification, and methane production were determined by gas chromatography in alpine mountain-meadow soils under different types of phytocenoses at the Teberda State Reserve. The main factors that control the intensity of these processes in the mountain-meadow soils are moisture and accumulation of biophilous elements related to the position of the soils on the biogeochemical catena. The CO₂ emission and intensity of the nitrogen fixation in the soils under Geranium-Hedysarum meadows that occupy transit-accumulative positions were 2–3 times higher that these parameters in the soils under the alpine heathlands and Festuca meadows. The soils under the carpet-like alpine meadows, accumulating moisture and mineral nitrogen, were characterized by the highest intensity of denitrification and methane production.     

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.     

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.     

Identifying earthworms through DNA barcodes

With almost 3000 species, earthworms provide important model systems for studying soil fauna. However, species identification of earthworms is difficult and therefore limiting. The use of DNA barcodes, which are short sequences from standardized regions of the genome, has been regarded as a promising approach to resolve this taxonomic dilemma. We evaluated sequence diversity in the mitochondrial cytochrome-c oxidase I (COI) gene as a tool for resolving differences among species of Chinese earthworms. Members of six genera and 28 species were examined, and species were successfully discriminated in all cases. Sequence divergence within species was generally less than 1%, whereas divergence between species was greater than 15% in all cases. Divergence among individuals of Eisenia fetida were much higher (up to 7.8%); however, this may represent the presence of unrecognized sibling species or subspecies. We conclude that although it cannot completely replace taxonomy, the DNA barcode is a powerful tool for identifying species of earthworms and provides a useful complement to traditional morphological taxonomy.     

Biological activity of chernozem on different elements of microtopography

A pedogenetic stratification of the physicochemical and biological properties has been studied in the profiles of chernozemic soils on different elements of the paleocryogenic microtopography under a shelterbelt within the Kamennaya Steppe Reserve. The biological activity of soil samples was determined in laboratory from the amount of CO₂ produced by the soil upon its incubation. It is shown that the soil properties vary considerably both in the vertical (along the soil profile) and horizontal (along the elements of the microtopography) directions. The methods of correlation and factor analyses have been applied to group the soil properties according to the three major factors and to study the relationships between these groups. A quantitative assessment of the particular factors of soil formation under given pedoclimatic conditions is suggested. The dominant role belongs to the biological factor (50% of the total factor load). This factor is reflected in the soil properties with the maximum degree of differentiation in the soil profile. The paleocryogenic microtopography (17% of the total factor load) specifies the differentiation of soil acidity and the content of carbonates.     

Burial of soil-surface artifacts in the presence of lumbricid earthworms

Rings of wire placed on the soil surface of two pastures containing populations of Lumbricidae were recovered after 52 months. They had been buried at the rate of 9–10 mm per year. At a forest site where only Megascolecidae were present there was no burial. At the pasture sites, populations of Lumbricidae in tubes of soil sterilized with methyl bromide 52 months earlier were indistinguishable from those in untreated soils.     

Distribution of earthworms in soils of Yakutia

The distribution of earthworms in 18 types of tundra, middle-taiga, alas, and floodplain soils of Yakutia has been studied. The species Eisenia nordenskioldi is typical of Yakutian soils. The area, population density, and seasonal dynamics of earthworms in permafrost-affected soils have been determined. It is shown that earthworms are absent in excessively moist peat-muck permafrost-affected soils, excessively dry soddy soils of alases (thermokarst depressions), and soddy alluvial soils under steppe communities. The best living conditions for earthworms are associated with meadow floodplain, meadow alas, and mucky calcareous soils.     

Food preferences of earthworms for soil fungi

Soil fungi are considered to be an important food source for earthworms. Selection experiments were carried out in order to study the preferences of earthworm species for a variety of soil fungi. Nine fungal species (Cladosporium cladosporioides, Rhizoctonia solani, Mucor sp., Trichoderma viride, Fusarium nivale, Phlebia radiata, Glaeophyllum trabeum, Coniophora puteana, Coriolus versicolor) were grown separately in centrifuge tubes on sterilized sand with potato dextrose. Tubes containing different fungal species, 8–9 per experiment, were arranged in a food choice arena. The preference for the fungi of 5 different earthworm species (Lumbricus terrestris, Lumbricus castaneus, Aporrectodea caliginosa, Aporrectodea rosea, Octolasion cyaneum) was tested by adding one specimen per chamber. Removal of sand from the tubes within 6 days was used as the indicator of preference by earthworms. The food preference of earthworms irrespective of ecological group followed a general pattern. F. nivale and C. cladosporioides were the preferred fungal species, followed by fast-growing species such as Mucor sp. and R. solani. In contrast, basidiomycetes were generally refused. The epigeic species L. rubellus had the strongest preference for a single fungal species, in contrast the endogeic species A. rosea fed more evenly on different fungal species. We conclude that early successional fungal species are used as cues by earthworms to detect fresh organic resources in soil.