Organic carbon sequestration in earthworm burrows

Earthworms strongly affect soil organic carbon cycling. The aim of this study was to determine whether deep burrowing anecic earthworms enhance carbon storage in soils and decrease C turnover. Earthworm burrow linings were separated into thin cylindrical sections with different distances from the burrow wall to determine gradients from the burrow wall to the surrounding soil. Organic C, total N, radiocarbon (¹⁴C) concentration, stable isotope values (δ¹³C, δ¹⁵N) and extracellular enzyme activities were measured in these samples. Anecic earthworms increased C stocks by 270 and 310 g m^?2 accumulated in the vertical burrows. C-enrichment of the burrow linings was spatially highly variable within a distance of millimetres around the burrow walls. It was shown that C accumulation in burrows can be fast with C sequestration rates of about 22 g C m^?2 yr^?1 in the burrow linings, but accumulated C in the burrows may be mineralised fast with turnover times of only 3–5 years. Carbon stocks in earthworm burrows strongly depended on the earthworm activity which maintains continuous C input into the burrows. The enhanced extracellular enzyme activity of fresh casts was not persistent, but was 47% lower in inhabited burrows and 62% lower in abandoned burrows. Enzyme activities followed the C concentrations in the burrows and were not further suppressed due to earthworms. Radiocarbon concentrations and stable isotopes in the burrow linings showed an exponential gradient with the youngest and less degraded organic matter in the innermost part of the burrow wall. Carbon accumulation by anecic earthworm is restricted to distinct burrows with less influence to the surrounding soil. Contrary to the initial hypothesis, that organic C is stabilised due to earthworms, relaxation time experiments with nuclear magnetic resonance spectroscopy (NMR) did not reveal any enhanced adsorption of C on iron oxides with C stabilising effect. Our results suggest that earthworm activity does not substantially increase subsoil C stocks but burrows serve as fast ways for fresh C transport into deep soil horizons.     

Endogeic and anecic earthworm abundance in six Midwestern cropping systems

Endogeic and juvenile anecic earthworm abundance was measured in soil samples and anecic populations were studied by counting midden numbers at the sites of two long-term cropping systems trials in South-central Wisconsin. The three grain and three forage systems at each site were designed to reflect a range of Midwestern USA production strategies. The primary objectives of this work were to determine if the abundance of endogeic or anecic earthworms varied among cropping systems or crop phases within a cropping system and were there specific management practices that impacted endogeic or anecic earthworm numbers. The earthworms present in the surface soil were: Aporrectodea tuberculata (Eisen), A. caliginosa (Savigny), A. trapezoides (Dugés); and juvenile Lumbricus terrestris (L.). True endogeic abundance was greatest in rotationally grazed pasture [188 m^?2 at Arlington (ARL) and 299 m^?2 at Elkhorn (ELK)], and smallest in conventional continuous corn (27 m^?2 at ARL and 32 m^?2 at ELK). The only type of anecic earthworm found was L. terrestris L. There was an average of 1.2 middens per adult anecic earthworm and the population of anecics was greatest in the no-till cash grain system (28 middens m^?2 at ARL, 18 m^?2 at ELK) and smallest in the conventional continuous corn system (3 middens m^?2 at ARL, 1 m^?2 at ELK). Earthworm numbers in individual crop phases within a cropping system were too variable from year-to-year to recommend using a single phase to characterize a whole cropping system. Indices for five management factors (tillage, manure inputs, solid stand, pesticide use, and crop diversity) were examined, and manure use and tillage were the most important impacting earthworm numbers across the range of cropping systems. Manure use was the most important management factor affecting endogeic earthworm numbers; but no-tillage was the most important for the juvenile and adult anecic groups and had a significantly positive influence on endogeic earthworm counts as well. The pesticides used, which were among the most commonly applied pesticides in the Midwestern USA, and increasing crop diversity did not have a significant effect on either the endogeic or anecic earthworm groups in this study. Consequently, designing cropping systems that reduce tillage and include manure with less regard to omitting pesticides or increasing crop diversity should enhance earthworm populations and probably improve sustainability.     

Assessment of soil structural differentiation around earthworm burrows by means of X-ray computed tomography and scanning electron microscopy

The burrowing activity of earthworms creates a distinct area around the resulting macropores called the drilosphere, which controls various soil processes. Density and microstructure of the drilosphere were studied and compared with those of the surrounding soil. For this purpose soil cores were separately inoculated with the vertically burrowing earthworm species Lumbricus terrestris. After 70 days some cores were compacted by a hydraulic press (250 kPa) and all cores were analysed by means of X-ray computed tomography. Mean Hounsfield Units were measured for concentric ROI cylinders (ROI = region of interest) of increasing diameters located around vertical macropore sections within selected horizontal slices. Based on these data we estimated stepwise the distribution of bulk density from the inner boundary of the drilosphere to the surrounding soil. In uncompacted soil the bulk density of the drilosphere was increased by 11% over that of the surrounding soil. In cross section, drilosphere and burrow form a concentric area with a total radius up to 2.2 cm. Soil compaction increased the dry bulk density of soil and decreased the diameter of earthworm burrows. Moreover, we found a less dense part of soil between the dense drilosphere and the remaining soil of the compacted core. Scanning electron microscopy revealed that the coarse silt particles of the bulk soil were rearranged to a parallel orientation due to compaction whereas the microstructure of the drilosphere remained unchanged. In any case, the drilosphere revealed a very homogeneous and dense arrangement of silt particles.     

砷污染土壤中接种丛枝菌根真菌和蚯蚓对土壤线虫群落和植物砷吸收的影响

The influences of arbuscular mycorrhizal fungi (MF, Acaulospora spp. and Glomus spp.), rice straw and earthworms (RE, Eisenia foetida) on nematode communities and arsenic (As) uptake by maize (Zea mays L.) in As-contaminated soils were examined in a field experiment conducted in Wujiang, Jiangsu Province, China. The experiment was designed as a 2 × 2 factorial with the factors of MF (inoculated or uninoculated) and RE (added or not added). The results demonstrated that MF inoculation led to significantly higher root colonization of MF and root dry weight. Plants inoculated with both MF and RE had the highest As concentrations in root. The number of total nematodes increased with MF inoculation when RE was absent, and decreased with RE addition when MF was inoculated. The improved abundance of nematodes with the MF treatment implied that the tested MF acted as food sources for fungivores. The abundances of omnivores-predators and plant parasites were reduced by earthworm activity. Twenty-seven genera of nematodes were identified, with Filenchus dominant in all treatments. Trophic diversity (TD), Shannon-Weaver diversity (H′), Simpson dominance index (λ), and species richness (SR) indicated higher species diversity, more proportionate species composition, evenly distributed species, and more food sources in the MF, RE, and their interaction treatments. Maturity index (MI) showed a moderately disturbed environment due to As pollution. Besides enhancing plant uptake of contaminants, MF and RE amendments could also improve soil health by restoring the structure of soil communities, as reflected by more stable nematode community structure.     

Effects of an endogeic and an anecic earthworm on the competition between four annual plants and their relative fecundity

Competition between plants for essential resources determines the distribution of biomasses between species as well as the composition of plant communities through effects on species reproductive potentials. Soil organisms influence plant competitive ability and access to resources; thus they should modify plant community composition. The effects of an endogeic (Aporrectodea caliginosa) and an anecic (Lumbricus terrestris) earthworm species on the competition between grass (Poa annua), two forbs (Veronica persica and Cerastium glomeratum) and legume (Trifolium dubium) were investigated in a greenhouse experiment. We established two types of plant communities: monocultures and polycultures of the four species. L. terrestris increased the biomass of P. annua and V. persica (in monocultures as well as in polycultures). However, the presence of L. terrestris allowed the grass to produce the highest biomass in polycultures suggesting that this earthworm species promoted the growth of P. annua against the other plant species. In monocultures as well as in polycultures, the presence of L. terrestris to increased the number of seeds of T. dubium and the total seed mass of V. persica. These results suggest that L. terrestris enhanced the short term competitive ability of P. annua by promoting its growth. The increased number of seeds of T. dubium in the presence of L. terrestris suggests that this earthworm species could enhance the long-term competitive ability of this legume and may increase its number of individuals after several generations.     

A note on the reduction of runoff from crusted soils by earthworm burrows and artificial channels

The aim of this study was to determine the order of magnitude in which earthworm channels can contribute to the reduction of runoff during simulated rainfall. Two sets of experiments were carried out, the first using soil columns (Ap-horizon of a Luvisol) in which endogeic earthworms had dug channels through previously produced surface seals, the second set consisting of runoff boxes, where artificial channels were made with a needle following a rainfall application that had also produced a pronounced surface seal. In all cases, the persistance of open earthworm burrows led to a considerable decrease in runoff. It was observed that channels smaller than 5 mm in diameter were resealed within the first 15 minutes of rainfall, and did not contribute to percolation in the experiment with soil columns. In the experiment with the runoff boxes, a highly significant correlation was found between number of open channels and runoff rate, the treatments with a slope of 5% and a rainfall intensity of 30 mm/h showing a greater effect when compared to the treatment with 10% slope and an intensity of 60mm/h.     

Volume density of earthworm burrows in compacted cores of soil as estimated by direct and indirect methods

After earthworms of the species Aporrectodea caliginosa and A. rosea had burrowed in compacted cores of soil for 68 days the cores were sectioned horizontally. The upper surface of each sectioned layer of soil was photographed before it was dissected and the dimensions of all burrows within the layer measured. Volume densities calculated from the direct measurement of burrows were compared with the values calculated by stereology from data obtained from two image analysis methods, computerised image analysis and point counting with a systematic lattice. The assumption implicit in all stereology calculations was satisfied for this experiment in that the burrows of both species showed no preferred orientation in the compacted soil. Computerised image analysis could not measure the density of all burrows in the photographs because of the lack of contrast between cast-filled burrows and the soil and the complex shapes of the burrows. Although the volume densities of A. caliginosa burrows calculated from point counts were correlated with the values calculated from direct measurement, point counting over-estimated volume densities by two to three times. In the experiment, A. rosea produced too few airfilled burrows for the lattice to detect. The relative ratios of air-filled to cast-filled burrows calculated from the point counts suggested that approximately two-thirds and eight-ninths of the burrows of A. caliginosa and A. rosea, respectively, were filled with casts.     

Pyrosequencing and mid-infrared spectroscopy reveal distinct aggregate stratification of soil bacterial communities and organic matter composition

This study integrated physical, chemical, and molecular techniques to assess relationships between soil bacterial community structures and the quantity and quality of soil organic carbon (SOC) at the soil microenvironment scale (e.g., within different aggregate size-fractions). To accomplish this goal, soil samples (0–5 cm) were collected from the Texas High Plains region under a variety of dryland and irrigated cropping systems. The soil was separated into macroaggregates, microaggregates, and silt + clay fractions that were analyzed for (1) bacterial diversity via pyrosequencing of the 16s rRNA gene and (2) SOC quantity and quality using a combustion method and mid-infrared diffuse reflectance spectroscopy (mid-IR), respectively. Results from pyrosequencing showed that each soil microenvironment supported a distinct bacterial community. Similarly, mid-IR data revealed distinct spectral features indicating that these fractions were also distinguished by organic and mineral composition. Macroaggregates showed relatively high abundance of Actinobacteria (excluding order Rubrobacteriales) and α-Proteobacteria and contained the most SOC. Microaggregates showed high relative abundance of Rubrobacteriales and the least amount of SOC. Predominance within the soil microenvironment and correlations along the mid-IR spectra were different between members of the order Rubrobacteriales compared with all other members of the Actinobacteria phyla, suggesting they have different ecological niches. Mid-IR results revealed microaggregates had greater absorbance in the 1370–1450 cm^?1 region for phenolic and alkyl groups (possibly recalcitrant C). Silt + clay fractions were distinguished by Gemmatimonadetes and OP10 phyla, which positively correlated with spectral absorption in the1250–1150 cm^?1 range (indicating both degradable and recalcitrant C forms). In contrast to general diversity index measurements, distributions of the more rare bacterial phyla (phyla representing <6% of the identified population) were more important for differentiating between communities in soil microenvironments. To our knowledge, this is the first study to investigate soil bacterial communities among soil aggregates using pyrosequenging and to associate these communities to specific soil C chemistries as indicated by mid-IR absorbance.     

Impact of soil stockpiling and mining rehabilitation on earthworm communities

As key ‘ecosystem engineers’, earthworms improve mineralization of organic matter, plant growth, soil quality, and are an important component of many terrestrial food webs. Under appropriate conditions, they are therefore likely to accelerate the restoration of soil ecosystem function after mining.Conserving naturally occurring populations and facilitating their recolonisation appears as the most efficient way to increase earthworms’ overall effect. The impact of mining activities and restoration measures on New Zealand endemic earthworm communities was tested. Earthworm biomass and diversity were compared in four different habitat types.Mining activities, not surprisingly, are shown here to have a detrimental impact on earthworm communities. Soil stockpiling induces anaerobic conditions at and below a depth of 1 m, where earthworms do not survive. The use of stockpiled soil for vegetation replanting therefore leads to low diversity and low abundance of earthworms. An alternative restoration technique consisting in transferring vegetation and soil units (the vegetation direct transfer) was efficient in preserving earthworm populations with earthworm biomass and diversity not significantly different from those observed in undisturbed areas. Based on these results, we recommend vegetation direct transfer (VDT) to be prioritised whenever it is logistically and economically feasible. When VDT is not applicable, low stockpiles should be prioritised as they will comprise a higher proportion of good quality soil (at the surface) and a lower proportion of anaerobic and compacted soil (below 1 m depth at the studied site).     

Inputs of nitrogen and organic matter govern the composition of fungal communities in soil disturbed by overwintering cattle

Overwintering cattle outdoors causes soil surface disturbance, substantial increases of soil N_tot, C_org, and P and a shift in pH to alkaline levels. Since fungi predominate in unfertilized soils with acidic pH and have filamentous hyphae, we hypothesized that changes caused by overwintering cattle outdoors (trampling, excreta returns, and changes in soil chemistry) will lead to suppressed species richness, lower biomass, and alter the structure of fungal communities. The research was conducted on an upland pasture used more than 10 years for cattle overwintering. Both culture-dependent and -independent methods were used for the determination of either fungal species composition (cultivation; DGGE) or biomass (numbers of CFU; concentration of fungal PLFA marker 18:2ω6,9). Soils under three different levels of cattle disturbance (S - severe, M - moderate, C - no disturbance/control) were investigated during three subsequent years. In addition, the DGGE analysis of soils was completed by comparison with analysis of fresh cattle excrements (Ex). The composition of fungal communities showed significantly higher richness and a substantial shift in species composition in cattle-disturbed soils (S, M) in comparison to the non-disturbed soil (C). The number of separated DGGE bands was significantly higher in S (30.67 ± 1.63; mean ± SD) and M (25.50 ± 1.64) soils than in the C soil (19.33 ± 1.75). Sequencing of typical bands revealed common fungal genera - Alternaria, Penicillium, Fusarium, Rhizopus, Isaria, and Metarhizium. Profiles of the S soil were enriched by bands of rumen-born anaerobic fungi (Neocallimastix, Cyllamyces) occurring mainly in profiles of excrements, where relatively low band richness (14.33 ± 1.15) was observed. The increasing level of cattle disturbance induced an increase in the biomass of complex fungal community over the three-year experimental period from 3.39 ± 2.11 (mean ± SD) nmol of fungal PLFA per gram of the C soil to 5.87 ± 3.16 in the M soil and 9.21 ± 4.69 in the S soil. Concentrations of soil N_tot and C_org were evaluated as the parameters significantly correlating with biomass as well as composition of the fungal community.     

Changes in soil nematode communities under the impact of fertilizers

Changes taking place in the communities of soil nematodes of an artificially sown meadow under the impact of annually applied mineral fertilizers have been studied in a field experiment for nine years. It is shown that changes in the species composition, trophic structure, and numbers of nematodes from different genera depend on the fertilizer applied and on the competitiveness of the plant species grown. The spectra of nematode genera sensitive to the complete mineral fertilizer (NPK) and to the particular nutrients have been identified with the use of a number of parameters, including the maturity index of nematode communities, the biotope preferences of the particular nematode genera, and the general pattern of nematode habitats. The results obtained in this study can be used to assess the effect of mineral fertilizers on the soil fauna and to suggest optimum application rates of mineral fertilizers ensuring the sustainable development of meadow herbs. The use of the data on the trophic structure of nematode communities for predicting the ways of organic matter decomposition in the soil is discussed.     

Effect of the earthworm Lumbricus rubellus on the nematode community in a peat meadow soil

The effect of different densities of Lumbricus rubellus on the nematode community was studied in a field experiment. The stand, a cultivated meadow on peat-muck soil developed from moderately decomposed alder peat, was located on drained fens in the central basin of the Biebrza valley in the north-eastern part of Poland. Samples were taken from soil isolators into which 0, 2, 4 or 6 earthworms were previously introduced. The abundance and trophic structure of the nematode fauna in the different treatments were compared 30, 60, 90 and 120 d after the introduction of L. rubellus. The effect of L. rubellus on soil nematodes was most pronounced at the beginning of the experiment. Thirty days after introduction of L. rubellus, the total number of nematodes in all trials with earthworms was significantly lower than in the control, and nematode numbers decreased with increasing L. rubellus density. On later sampling dates, the results were less clear and 120 d after introduction of L. rubellus no significant effect on the total number of nematodes was observed in the treatments. The abundance of the bacterial-, fungal- and plant-feeding nematodes in the treatments with earthworms was lower than in the control 30 d after introduction of L. rubellus, but significant differences were found only in the case of bacterial feeders.     

Soil organic matter distribution as influenced by enchytraeid and earthworm activity

Loam and sandy soils, and the earthworm casts produced with ¹⁴C-labelled plant material in both soils, were incubated in airtight glass vessels with and without enchytraeids to evaluate the effects of soil fauna on the distribution and fragmentation of organic matter. After 1, 3, and 6 weeks, the amount of C mineralised was determined in soils and earthworm casts, and the soil was fractionated into particulate organic matter (POM), the most active pool of soil organic matter, after complete physical dispersion in water. The percentage weight of fine fractions (0-50 µm) was 67.4% in the loam soil. Sand (coarse, i.e. 150-2,000 µm and fine 50-150 µm) represented 87.2% of total weight in sandy soil, while the percentages of C (PC) were 23.2% in coarse POM (2,000-150 µm) and 11.9% in fine POM (150-50 µm). These percentages were higher than those in loam soil, i.e. 3.4% (coarse POM) and 5.4% (fine POM). The PC in coarse POM (9.50%) and fine POM (16.4%) remained higher in casts from sandy soil than in casts from loam soil (4.7% in coarse and 14.3% in fine POM). The highest percentages of ¹⁴C-labelled leaves were found in fine fractions, 55.9% in casts from loam soil and 48.8% in casts from sandy soil. The C mineralisation of the added plant material was higher in casts from the sandy soil (20.3%) than from the loam soil (13.5%). Enchytraeids enhanced C mineralisation in the bulk sandy soil, but did not affect the mineralisation of added plant material in either soil. The main enchytraeid effect was enhancement of the humification process in the bulk sandy soil, the casts from this soil, and the bulk loam soil.     

Relationships between earthworm communities and burrow numbers under different land use systems

This study addresses the influence of three different land use systems (continuous maize, pasture/maize rotation, permanent pasture) on the relationships between earthworm populations and the number of earthworm burrows quantified in a soil profile. Quantified burrows were limited to those observable by the naked eye (i.e. >2 mm in diameter) and enumerated earthworms were limited to those which could have created the observable burrows (i.e. >0.3 g).The results were combined with data from the literature coming from different geographical regions. This study showed that earthworm abundance decreased with the increasing land management intensity (maize crop vs. pasture), while the number of burrows could be higher or similar under maize compared to pasture. Under maize, despite lower earthworm abundance and the annual destruction of the burrows by tillage, the number of burrows was almost as high as under pasture. This absence of a relationship between burrow numbers and earthworm abundance was observed in the soil profile and for each layer of the profile for each land use system. Furthermore, the burrow number/m^?2 per earthworm strongly varied depending on land use and was far higher under maize when compared to pasture (74 vs. 7). Therefore, a power-law type relationship was clearly established between burrow number/m^?2 per earthworm and earthworm abundance. This power type relationship was also observed when including data from the literature although it followed a different mathematical model. These results were explained by (i) increased earthworm burrowing activity (i.e. an increase in the number of burrows produced by each earthworm) under maize, and (ii) the dynamics of burrow number under pasture (i.e. decreased burrowing activity and burrow destruction process); both results of food accessibility combined with inter-individual competition. The results of the study suggest that farmers should not use the number of pores as an indicator of earthworm abundance, but as an indicator of earthworm activity, which could be integrated in an indicator of soil quality.     

Relationships between earthworm communities and burrow numbers under different land use systems

This study addresses the influence of three different land use systems (continuous maize, pasture/maize rotation, permanent pasture) on the relationships between earthworm populations and the number of earthworm burrows quantified in a soil profile. Quantified burrows were limited to those observable by the naked eye (i.e. >2 mm in diameter) and enumerated earthworms were limited to those which could have created the observable burrows (i.e. >0.3 g).The results were combined with data from the literature coming from different geographical regions. This study showed that earthworm abundance decreased with the increasing land management intensity (maize crop vs. pasture), while the number of burrows could be higher or similar under maize compared to pasture. Under maize, despite lower earthworm abundance and the annual destruction of the burrows by tillage, the number of burrows was almost as high as under pasture. This absence of a relationship between burrow numbers and earthworm abundance was observed in the soil profile and for each layer of the profile for each land use system. Furthermore, the burrow number/m⁻² per earthworm strongly varied depending on land use and was far higher under maize when compared to pasture (74 vs. 7). Therefore, a power-law type relationship was clearly established between burrow number/m⁻² per earthworm and earthworm abundance. This power type relationship was also observed when including data from the literature although it followed a different mathematical model. These results were explained by (i) increased earthworm burrowing activity (i.e. an increase in the number of burrows produced by each earthworm) under maize, and (ii) the dynamics of burrow number under pasture (i.e. decreased burrowing activity and burrow destruction process); both results of food accessibility combined with inter-individual competition. The results of the study suggest that farmers should not use the number of pores as an indicator of earthworm abundance, but as an indicator of earthworm activity, which could be integrated in an indicator of soil quality.     

The heterogeneity of humus profiles and earthworm communities in a virgin beech forest

Thirty sites, encompassing a range of soil and vegetation conditions in the biological reserve of La Tillaie (Fontainebleau Forest, France) were investigated in April 1992. Beech (Fagus sylvatica L.) was the dominant tree species, with several developmental phases forming the forest patchwork. Sessile oak [Quercus petraea (Mattus.) Liebl.] was present but only as old relictual individuals. Gaps in the canopy cover were abundant, mostly caused by wind storms 2 years previously. The next most recent storm was 25 years before, resulting in distinct patches of full-grown trees. Humus profiles were classified and compared with the distribution of earthworm communities, canopy cover, and soil types. Geomorphology was responsible for the main part of the observed variation. Absence of lime in the substrate and direct contact with a sandstone stratum near the ground surface was associated with the absence of earthworms and the appearance of an OH horizon (moder humus). Elsewhere, earthworms were present and humus profiles did not display any OH horizon (mull or mull-like moder humus), but species composition was variable and strongly influenced by the thickness of the superficial sand deposit overlying limestone. On a thick (1 m or more) sandy substrate earthworm communities were dominated by epigeic species together with the anecic Lumbricus terrestris L. The species richness was higher on a shallower sandy substrate (50 cm) where lime was more accessible to tree roots and burrowing animals. The influence of the forest cycle of beech was visible in the latter case (covering most of the area), with an increase in the thickness of the OL and OF horizons and a decrease in endogeic earthworm populations during the phase of intense growth of beech. This fall in burrowing activity was apparent in gaps created by wind storms and fungal diseases within mature stands as early as 2 years after the fall of the trees.