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.     

The effect of Lumbricus rubellus and Lumbricus terrestris on zinc distribution and availability in artificial soil columns

This study investigated the impact of epigeic and (epi)anecic earthworms on the distribution and availability of zinc in the soil profile. Experiments were carried out with Lumbricus rubellus and Lumbricus terrestris in perspex columns (Ø 10 cm), filled with 20 to 23 cm non-polluted soil [organic matter 2%, clay 2.9%, pH 6.4 (0.01 M CaCl₂)], that was covered by a 3- to 5-cm layer of aged zinc-spiked soil (500 mg Zn/kg dry soil) and another 2 cm non-polluted soil on top. After 80 days, columns were sacrificed and sampled in a depth profile. Earthworm casts, deposited on top of the soil, were collected. Each sample was analyzed for total and 0.01 M CaCl₂-exchangeable zinc concentrations. L. rubellus did not go deeper than 3 cm into the soil and therefore no effect on zinc distribution in the soil could be detected. For L. terrestris, total zinc concentrations in the non-polluted layers were slightly but significantly higher in columns with earthworms, and so were the CaCl₂-exchangeable zinc concentrations in the polluted layers of these columns. Casts of L. terrestris collected from the soil surface showed higher total zinc concentrations than those from non-polluted soil. Casts were mainly placed on top of the soil. This study showed that these epigeic and (epi)anecic species have only a slight effect on zinc availability, and that deep burrowing species, like L. terrestris, are able to transport polluted soil from deeper layers to the soil surface.     

Recolonization of methyl-bromide sterilized soils by plant and soil nematodes over 52 months

Recolonization of soils by organisms is dependent not only on biological factors but also on site factors including soil and vegetation. The total nematode populations in soil sterilized 52 months earlier with methyl bromide ranged from 77 to 123% of those in untreated soil; both vegetation and rainfall appear to have been important factors in the recolonization. In a high-rainfall pasture the dominant plant-feeding nematode Helicotylenchus did not recolonize and was replaced by Paratylenchus. Under high rainfall, Iotonchus failed to recolonize either pasture or forest, but Clarkus recolonized well. While indices such as the maturity index, the summed maturity index, PPI, the ratio of fungal: bacterial feeding nematodes, species richness, the Shannon-Weaver index, and indices of evenness, dominance, and diversity showed various effects, none gave consistent trends; rainfall and vegetation probably exerted too much influence. In the light of trends in our data, in data for other ecosystems, and the reality of r-K strategies in animals, it may not be reasonable to expect a global nematode index of soil health or ecosystem condition. While a nematode index may be useful in local or regional studies, research efforts may be better directed towards elucidating key populations of nematodes for investigating the impact of particular land management practices on ecosystem sustainability.     

Quantitative analysis of earthworm burrow systems with respect to biological soil-structure regeneration after soil compaction

 On arable land, tilled with conventional tillage (CT) and conservation tillage (CS) respectively, plots were compacted by wheeling them 6 times with a 5 Mg wheel load in spring 1995. Immediately after compaction, undisturbed soil monoliths were excavated from the compacted and uncompacted plots. The monoliths were defaunated and inoculated with either Lumbricus terrestris or Aporrectodea caliginosa. One monolith from each plot remained uninoculated as a control. After 6 months the monoliths were defaunated again and then scanned with X-ray helical computed tomography. The data were transformed, the void systems inside the monoliths were reconstructed and visualised, and the parameters total void length, total void volume, tortuosity and continuity were quantified. The parameters' values were generally lower in the controls than in the inoculated monoliths. Differences in burrow construction could be explained by the different life strategies of the two earthworm species. Changes in burrow morphology due to tillage system and soil compaction were minor. Only the continuity of the burrow systems clearly changed: decreasing for L. terrestris and increasing for A. caliginosa. This can be explained by a change in the earthworms' burrowing activity to minimise energy expenditure in compacted soil. By extrapolating field data, we concluded that earthworms have great potential for biologically regenerating the soil structure after a single compaction event. Due to higher earthworm abundances in soil managed by CS the regeneration of the soil structure is assumed to be better in these plots than those tilled by CT. Received: 17 December 1997     

Activity,origins and location of cellulases in a silt loam soil

Summary Cellulase activity in a silt loam soil was assayed and characterised using a microcrystalline cellulose substrate (Avicel). Activity was maximal between pH 5.3 and pH 6.0. A 64% loss in activity was observed on air-drying the soil. However, the residual activity was stable to storage at 40°C for 7 days and was resistant to the action of added protease. The component endoglucanase and -D-glucosidase activities in field-moist and air-dried soil were also assayed. The proportion of the soil microbial population able to utilise cellulose was investigated and the persistence of two free (soluble) cellulase preparations of microbial origin was determined following their addition to soil. A rapid decline in the endoglucanase activity of a Streptomyces sp. cellulase preparation was observed while 30% of the original activity of a Trichoderma viride cellulase preparation could still be detected after 20 days. From the data obtained in this study it appears that the major portion of the -D-glucosidase activity is bound to and protected by the soil colloids. By contrast, the major portion of the exo- and endoglucanase activity appears to be free in the soil solution, attached to the outer surfaces of cellulolytic microorganisms or associated in enzyme substrate complexes. The low residual activity measured in air-dried soil may owe its stability to an association with soil colloids or with recalcitrant cellulosic material present in soil.     

Nitrogen mineralization and reorganization in casts of the geophagous tropical earthworm Pontoscolex corethrurus (Glossoscolecidae)

Summary Mineral N concentrations ranged from 133.1 to 167.8 g g^-1 dry soil in fresh casts of the endogeic earthworm Pontoscolex corethrurus fed on an Amazonian Ultisol; this was approximately five times the concentration in non-ingested soil. Most of this N was in the form of NH _inf4 ^sup+ . N also accumulated in microbial biomass, which increased from a control value of 10.5–11.3 to 67.5–74.1 g g^-1 in fresh casts. During a 16-day incubation, part of the NH _inf4 ^sup+ -N was nitrified and/or transferred to the microbial biomass. Total labile N (i.e., mineral+biomas N) decreased sharply at first (ca. 50% in the first 12 h), and then more slowly. The exact fate of this N (microbial metabolites, denitrification, or volatilization) is not known. After 16 days, the overall N content of the casts was still 28% higher than that of the control soil. Incubation of the soil before ingestion by the earthworms significantly increased the production of NH _inf4 ^sup+ in casts. We calculate that in a humid tropical pasture, 50–100 kg mineral N may be produced annually in earthworm casts. Part of this N may be conserved in the compact structure of the cast where the cast is not in close contact with plant roots.     

Disturbance effects on soil solution chemistry due to heating cable installation

Installation of heating cables for warming soil was used to evaluate the effect of disturbance on soil solution chemistry within a northern hardwood forest (Adirondack Mountains, New York). Differences in response among treatments suggested the importance of both the depth and timing of cable installation. There were increases (p>0.05) in many solutes within pilot study plots in which surrogate cable was installed at 15 cm depth. Most notably, mean nitrate concentrations for the 1st year following disturbance were 744 eq l^-1 at 15 cm depth compared to 7 eq l^-1 for the non-disturbed control. A comparison of pilot plots with 5 cm cable depth and an unheated soil-warming control plot with the same cable disturbance showed that the seasonality of soil disturbance may have a key role in response to disturbance. The soil solution response was diminished if installation occurred during the spring, a period of rapid uptake of nitrogen by vegetation. Mean nitrate concentrations were 176 eq l^-1 for 5-cm pilot plots (installed in fall 1991) versus 6 eq l^-1 for 5-cm, unheated soil-warming control plots (installed in spring 1992). Disturbance effects were attenuated over time and not generally apparent 1 year after installation.     

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.     

Effect of increasing oxygen concentration on total denitrification and nitrous oxide release from soil by different bacteria

Summary The effect of increasing oxygen concentrations (0, 5, 10 and 20 Vol% O₂) on total denitrification and N₂0 release was studied in model experiments using a neutral pH loamy soil relatively rich in easily decomposable organic matter and supplied with nitrate (300 g nitrate N/g dry soil). The sterilized soil was inoculated with three different denitrifying bacteria (Bacillus licheniformis,Aeromonas denitrificans andAzospirillum lipoferum) and incubated (80% WHC, 30°C). The gas volume was analysed for O₂, CO₂, N₂O, NO and N₂ by gas chromatography and the soil investigated for changes in ammonium, nitrite, nitrate, pH, total N and C as well as water-extractable C. WithB. licheniformis andAeromonas denitrificans total denitrification increased remarkably with increasing pO₂ as the result of intensified mineralization.Azospirillum lipoferum, however, showed the highest activity at 5 vol% O₂. WithB. licheniformis N₂O was released only in anaerobic conditions and at 5 Vol% O₂ (maximum) or 10 Vol% 02, but not at 20 Vol%, whereasAeromonas denitrificans produced N₂O only in the presence of He gas (maximum) or at 5 Vol% O₂. In contrast to these bacteria, N₂O production withAzospirillum lipoferum was restricted to 10 Vol% O₂ (maximum) and to 20 Vol% 02, with some traces at 5 vol% O₂. With a certain set of conditions, total denitrification and N₂O formation seem to be governed by the mineralization rate of the organisms in question. The increased demand for electron acceptors by a high turnover rate rather than the presence of anaerobic conditions seems to have determined the rate of denitrification.     

Quantitative image analysis of earthworm-mediated soil displacement

The way soil is disrupted and deformed by earthworm movement is hard to quantify non-destructively. Two anecic earthworm species, Aporrectodea longa (Ude) and Lumbricus terrestris L., were compared in their effect on the soil around them as they burrow. Image analysis (particle image velocimetry, PIV) was used successfully to quantify the distance and direction of soil particle displacement by earthworm locomotion giving a unique insight into their effect on the soil structure development. The data collected from both species using PIV show a decline in soil displacement at increasing distance from the earthworm’s body. The quantity of soil being displaced was more to the sides of the earthworms (radially) than in front of the prostomium (axially). Also, L. terrestris displaced more soil than A. longa both axially and radially. The findings from this study suggest that PIV image analysis is a viable tool for examining soil displacement by earthworms and the method used has the potential to be applied to other soil organisms.     

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.     

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.     

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.     

Persistence of hexachlorocyclohexane isomers in soil planted with rice and in rice rhizosphere soil suspensions

Summary The relative persistence of -, and -isomers of hexachlorocyclohexane (HCH) was studied in a flooded soil with and without rice seedlings under greenhouse conditions. -HCH was more stable than - and -HCH in both planted and unplanted systems. - and -HCH decreased to negligible levels (5.5% for the -isomer and 2.4% for the -isomer) after 30 days in planted and unplanted soils. During the same period, 30.9% of the added -HCH was recovered from planted soil and 50.6% from unplanted soil. Likewise, in anaerobically (H₂ + CO₂ atmosphere) incubated mineral salts solution inoculated with suspensions from rice rhizosphere and non-rhizosphere soils, -HCH decreased to low levels (< 15%) within 5 days. Most of the added -HCH was recovered from mineral solution inoculated with nonrhizosphere soil suspension even after 30 days while -HCH decreased to 53.6% of the original level in mineral solution inoculated with rice rhizosphere soil suspension. The data reveal that the degradation of anaerobically unstable HCH isomers is not retarded by the possible aeration of a flooded soil by rice roots.     

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.     

Seasonal differentiation of soil mesofauna in a littoral dune of the Egyptian Mediterranean coast

Summary Soil mesofauna (sensu Ghilarov, i.e., larger than 1 mm) was sampled from under four shrub species (Lygos raetam, Thymelaea hirsuta, Lycium shawii, and Josonia candicans) growing on the littoral oolitic sand dunes at Gharbaniat, 53 km W of Alexandria, Egypt, for a period of more than 30 months, spanning 3 years. Population density (PD) was calculated in relation to area of shrub canopy. Seasons were considered, according to the prevailing climatic conditions as well as to earlier physiological studies on the animals concerned, as: four winter months, four summer months and two months for each of the transitional seasons spring and autumn. The PD values obtained for each season thus defined were combined for the 41 taxa that were sampled. The table of these data was treated by correspondence analysis (CA) and ascending hierarchic classification (AHC), by the Roux DATA-VISION programme (suitable for Apple). Results from such treatment show that fauna as related to shrub species are differentiated along the first factorial axis, while as related to seasons they are differentiated along the second axis. Taxa common to all shrubs and to all seasons are centrally placed and cause some confusion in the resolution. Summer taxa are more distantly placed than those related to the other three seasons. Fauna under Lygos is richer, more diverse, and more complementary as regards trophic levels (with predators), and could probably be the source for replenishing the fauna of the other shrubs at all seasons. The AHC method did not show a similarly clear differentiation.Dedicated to the late Prof. Dr. M.S. Ghilarov     

Earthworms bring compacted and loose soil to a similar mechanical state

We tested the hypothesis that earthworms stabilise loose soil and loosen compacted soil to a similar mechanical state. Casts collected from initially loose soil (980 kg m⁻³) had 10-fold greater viscosity (31 kPa s) and 5-fold greater yield stress (200 Pa) than a control soil without worms. Lumbricus terrestris; Dendrobaena sp. and Aporrectodea longa were all investigated, with no difference found between species. In compacted soils (1300 kg m⁻³), A. longa produced casts with similar mechanical properties to loose soil, with viscosity and yield stress decreased by 45% compared to the control without worms. Earthworms were shown to bring initially loose and compacted soil to an intermediate mechanical state that is more favourable for structural stability and root growth.     

Spatial variation in soil compaction,and the burrowing activity of the earthworm<Emphasis Type="Italic"> Aporrectodea caliginosa</Emphasis>

The effects of soil compaction on earthworm ( Aporrectodea caliginosa nocturna) activity were studied using pot experiments. Two compaction pressures were used when packing the pots; loose soil was packed by applying a pressure of 96 kPa, and compact soil was packed using a compaction pressure of 386 kPa. Split pots which contained both loose and compact soil were also used. In split pots peripheral burrows (those next to the pot wall), were generally longer in the loose half of the pot than they were in the compact half. This implies that earthworms preferred the loose soil. An important finding was that peripheral burrows in the split pots were longer than those made in pots packed uniformly with either loose or compact soil. Our data suggest that the increase in activity in split pots is a response to spatial variation in soil compaction. In the split pots the earthworms tended to avoid the compact half, and we discuss how the avoidance response in the split pots may have increased the proportion of burrows in these pots that were peripheral.     

Earthworms of different functional groups affect the fate of the Bt-toxin Cry1Ab from transgenic maize in soil

The fate of the insecticidal Cry1Ab protein from crop residues (leaves and roots) of the transgenic maize variety MON810 was studied in the presence and absence of two earthworm species (Lumbricus terrestris, Aporrectodea caliginosa; separate incubations) in soil microcosms. The recombinant Cry1Ab protein was quantified using a highly sensitive ELISA. Control microcosms received corresponding non-transgenic plant material. All earthworms survived in the microcosms over a period of 5 weeks, irrespective of whether they received MON810 or non-transgenic plant material. Weight loss was observed for both earthworm species, independent of the plant material or transgenic modification. A strong decline of immunoreactive Cry1Ab in plant residues (mean initial concentration approx. 5000 ng g⁻¹) of MON810 was observed in all treatments, but in microcosms with earthworms this decline was significantly higher with less than 10% of the initial Cry1Ab concentration remaining after 5 weeks. Cry1Ab concentrations in casts were only 0.1% of those found in remaining plant material of the respective microcosms. No immunoreactive Cry1Ab proteins were found in earthworm tissues (threshold of detection: 0.58 ng g⁻¹ fresh weight). No further decline was found for Cry1Ab concentrations in casts of A. caliginosa during a subsequent period of 3 months of incubation in bulk soil (<0.1 ng g⁻¹) after removal of the earthworms from the microcosms, while in casts of L. terrestris the concentration decreased from 0.4 to below 0.1 ng g⁻¹. In conclusion, this study demonstrates that earthworms enhance the decline of immunoreactive Cry1Ab proteins from maize residues.