Differences in burrowing behaviour and spatial interaction between the two earthworm species Aporrectodea nocturna and Allolobophora chlorotica

 To study intraspecific and interspecific interactions between different ecological types of earthworm, the burrowing behaviour of two earthworm species (the anecic earthworm Aporrectodea nocturna and the endogeic earthworm Allolobophora chlorotica) was observed in a microcosm. Earthworms were either alone in the microcosm, together with a conspecific earthworm, or with an earthworm of the other species. Observations under red light, including those of the position of the animals and the burrow dug, were recorded 4 times a day for 8 days and provided the data needed to reconstruct the probable trajectories of each earthworm. Differences in movement and burrowing behaviour were observed. Comparisons between the two species confirmed the expected behaviour of each ecological type: A. nocturna reused its burrow system regularly, whereas A. chlorotica rarely did. Moreover, it was shown that A. chlorotica burrowed less and explored a smaller surface when in the presence of A. nocturna. Besides, A. nocturna burrowed less and explored a smaller surface when in the presence of another A. nocturna. If these interactions occur under natural conditions, they could affect the structure of the burrow systems of the earthworm species examined. Received: 15 January 1999     

C and N turnover of fermented residues from biogas plants in soil in the presence of three different earthworm species (Lumbricus terrestris,Aporrectodea longa,Aporrectodea caliginosa)

A soil microcosm experiment was performed to assess (1) the C- and N- turnover of residues from biogas plants in soils in the presence of three earthworm species (Lumbricus terrestris, Aporrectodea longa and Aporrectodea caliginosa) and (2) the resulting changes in soil chemical and microbiological properties when using these residues as fertilizer in comparison to conventional slurry. Earthworms were exposed in soils, fertilized with an equivalent amount of 120 kg of NH₄-N ha^?1 from: (1) conventional cattle slurry and (2) a fermented residue derived from cattle slurry, grass (silage) and maize. Additional treatments without slurry and earthworms were used as controls.There was considerable evidence that soils fertilized by fermented slurry comprised fewer amounts of readily available nutrients for microbial C and N turnover. We observed significant stimulation of microbial biomass, basal respiration and nitrification in treatments with conventional slurry, especially in the presence of earthworms. However, the stimulation of microbial activity by manure and earthworms were significantly lower in treatments with fermented slurry. Moreover, the results showed clear interactions between different earthworm species and manures. While the biomass of the anecic species (L. terrestris and A. longa) increased in both slurry treatments, the biomass of A. caliginosa (endogeic) decreased, with a significantly stronger biomass decline in treatments with fermented slurry. The metabolic quotients revealed microbial stress metabolism in fermented slurry treatments, predominantly in treatments with A. caliginosa. We conclude that particularly A. caliginosa and soil microorganisms competed for labile C sources in treatments with fermented slurry. An application of these residues as fertilizer might result in a reduction of microbial activity in agricultural soils and in a decline of endogeic earthworms.     

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     

Lethal and sublethal effects of imidacloprid on two earthworm species (Aporrectodea nocturna and Allolobophora icterica)

The chemical imidacloprid is the major component of many widely used insecticides and is relatively persistent in soils. A set of experiments was carried out to estimate the lethal (mortality) and sublethal (weight loss) effects of one of these insecticides, Confidor, on two earthworm species commonly found in agricultural soils. A preliminary experiment in the absence of earthworms showed that imidacloprid was not rapidly degraded, with a decrease of less than 10% after 2 weeks, and that it was distributed in a reasonably homogeneous manner throughout the soil (less than 10% of variation between samples). The LC₅₀ of imidacloprid for the anecic species Aporrectodea nocturna and the endogeic species Allolobophora icterica was between 2 and 4 mg kg^–1 dry soil. This result is consistent with previous findings obtained with other earthworm species and natural soils. When sublethal effects were examined, significant decreases in weight were observed at concentrations of 0.5 and 1 mg kg^–1 dry soil for the two earthworm species whereas no effect was observed at a concentration of 0.1 mg kg^–1 dry soil (NOEC value). These concentrations are close to 0.33 mg kg^–1 which is the Predictive Environmental Concentration. Weight loss appears to be a valuable endpoint that can be used with worms freshly collected in the field as long as variability in the response of a control is taken into account.     

Burrow systems made by Aporrectodea nocturna and Allolobophora chlorotica in artificial cores: morphological differences and effects of interspecific interactions

Burrow systems of earthworms contained in artificial cores were analysed through X-ray computed tomography and 3D skeleton reconstructions. Gas diffusion experiments were carried out on these cores to characterize soil transfer properties associated with the different burrow systems. Three types of cores were studied: cores in which Aporrectodea nocturna, an anecic earthworm was introduced (treatment 1), cores in which Allolobophora chlorotica, an endogeic earthworm was introduced (treatment 2) and cores that contained both species (treatment 3). Comparisons of the characteristics of the burrow systems of treatment 1 and 2 show important differences: the burrow system of A. nocturna comprises fewer burrows, which are longer, less branched, more vertical and have a lower sinuosity. The burrow system of A. chlorotica is characterized by lower continuity, which however did not result in a lower soil diffusivity. To study the burrow systems made by the two species in the same core (treatment 3), a separation that was based on differences in pore diameter between the two species and that takes into account the burrow orientation was designed. This separation was proven to be efficient since it resulted in low percentages of errors (around 10%) when applied to the burrow systems of treatments 1 and 2. Comparison of the burrow systems from treatments 1 and 3 demonstrated that the burrow system of A. nocturna was influenced by the presence of A. chlorotica: in treatment 3, A. nocturna made burrows that were smaller, more vertical and less branched. However, these interactions have to be confirmed under natural conditions.     

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.     

Dynamic study of the burrowing behaviour of Aporrectodea nocturna and Allolobophora chlorotica: interactions between earthworms and spatial avoidance of burrows

The behaviour of earthworms belonging to two different species and ecological types (Aporrectodea nocturna and Allolobophora chlorotica) was studied using two-dimensional (2D) terraria. Two experiments were set up to gain insight into the nature of interactions between these earthworms. Firstly, the evolution of the burrow systems was analysed with the density of the earthworms varying from one to five individuals. Secondly, a burrow system was first established by using one earthworm which was then removed before the introduction of a second earthworm. This second earthworm therefore encountered a burrow system created either by a conspecific earthworm or by an earthworm of the other species. These experiments showed that: (1) intra- and interspecific interactions occur between earthworms, (2) these interactions are dependent on the physical presence of the earthworms, and (3) spatial avoidance can occur (A. chlorotica avoiding burrows created by A. nocturna). The results suggest that earthworm burrow systems are "individual structures", rarely used by other earthworms when inhabited. When abandoned, the burrows may be recolonised depending on the ecological type of the earthworm under consideration.     

The earthworm (Aporrectodea caliginosa) primes the release of mobile and available micronutrients in soil

The objectives of our study were to quantify the impact of endogeic earthworms Aporrectodea caliginosa (Savigny) on iron (Fe), manganese (Mn) and zinc (Zn) mobility and availability in soil. Dried rye straw (Cecale cereale L.), clover aboveground parts (Trifolium pratense L.) or calcium carbonate were added to determine the effects on soil micronutrient mobility. To test the importance of soil–water saturation mediated by earthworms, soil samples were modified to 60% (control) and 100% (as in casts) water holding capacity (WHC). To assess availability of micronutrients, a cucumber plant (Cucumis sativus L.) bioassay were used. Earthworm casts had generally higher amounts of water-soluble micronutrients compared with bulk soils regardless of their moisture contents. The increased micronutrient mobility was more pronounced in casts from soil samples amended with plant residues (especially with straw) and was significantly higher than mobility in control soil for at least 1 week after the casts were deposited. Pre-incubation of soils amended with clover or straw with living earthworms for 4 weeks produced an increase in both shoot biomass and translocation rate of micronutrients (Mn, Zn) into xylem sap of cucumber compared to soils not worked by earthworms. The earthworm-mediated plant performances were determined 4 weeks after the earthworms were removed. The results demonstrated that earthworms can significantly impact the formation of mobile and available micronutrients in a soil. The relationship between micronutrient availability to cucumber plants and earthworm contribution to nitrogen (N) mineralization and micronutrient mobility are discussed.     

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).     

Competitive interactions affect the growth of Aporrectodea caliginosa and Lumbricus terrestris (Oligochaeta: Lumbricidae) in single- and mixed-species laboratory cultures

Negative interactions between earthworms may arise from high earthworm population densities. Under high populations in the field, niche separation or migration away from competitive pressure may help to regulate a multi-species population to a given level. This may not be possible in laboratory experiments, leading to an increase in competitive interactions which may alter earthworm growth rates and affect decomposition and nutrient mineralization processes. The objective of this experiment was to determine how growth rates of the endogeic earthworm Aporrectodea caliginosa Sav. and the anecic earthworm Lumbricus terrestris L. are affected by increasing population density and container size in both single- and multi-species cultures. Earthworm growth responses were compared in 1-L cylindrical pots containing disturbed soil and in 2.3-L PVC cores containing undisturbed soil. The relationship describing intra- and inter-specific competition was not affected by container type for both species. Nonetheless, decreasing the container size restricted the growth of L. terrestris in both single- and multi-species cultures, but only restricted the growth of A. caliginosa in multi-species cultures. For both species, a population density greater than one individual per litre reduced earthworm growth rates significantly, while weight loss in monocultures occurred when there were more than 10 A. caliginosa, and more than three L. terrestris per litre. Growth rates of both species were restricted in all population density treatments including the lowest of 0.9 individuals per litre. Further work is needed to find the population density at which growth rates are not affected and which may be used as an appropriate population in laboratory pot experiments to measure the effects of earthworms on soil processes and plant growth.     

Effects of natural (flooding and drought) and anthropogenic (copper and salinity) stressors on the earthworm Aporrectodea caliginosa under field conditions

Laboratory toxicity tests are usually conducted under stable conditions, while exposures in the field occur under variable environmental conditions. Field studies are therefore more appropriate in understanding the effect of single or mixed pollutants in the environment. Short-term interactive effects of natural environmental factors (flooding and drought) and anthropogenic stressors (copper and salinity) on the earthworm Aporrectodea caliginosa were investigated using outdoor microcosm experiments. Specimens of the lumbricid earthworm A. caliginosa were exposed in microcosms loaded with soils with increasing salinity with electrical conductivity (EC) ranging from 0.08 to 1.05 dS m^?1, with or without copper oxychloride spray treatments at recommended and elevated dosages. The experiment was conducted in August/September (end of winter) and repeated in November/December (end of spring) in the Stellenbosch area, South Africa to attain exposure under variable environmental conditions. In the soil, changes in Cu concentrations along the gradient of salinity were monitored using three methods: CaCl₂, DTPA and nitric acid extraction. Survival, weight change, and cocoon production of worms and body Cu concentrations were used as indices of interaction. None of the three extraction methods could reveal interactive effects between salinity and Cu in both seasons either because concentrations of Cu were too low or below detection limits. Copper, on its own, did not have a significant effect on the measured worm parameters during both seasons. During the winter experiment, flooding of microcosms significantly reduced the survival and affected the weight change of worms, and probably caused leaching of chemicals. Interaction between salinity and Cu had no significant effects on the measured worm parameters in winter while salinity only had a significant negative effect on weight change of worms. During spring, significant synergistic interaction between salinity and Cu occurred but only at 0.3 dS m^?1 by day 14 of the exposure period. At this and higher levels, salinity had a significant individual effect on survival and weight change of worms at days 14 and 28. The results indicate that higher toxicity of salinity could be expected during the dry spring periods than during the wet winter periods which are typical for southern temperate zones.     

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.     

Survival of Aporrectodea caliginosa and its effects on nutrient availability in biosolids amended soil

Few earthworms are present in production agricultural fields in the semi-arid plains of Colorado, where earthworm populations may be constrained by limited water and/or organic matter resources. We conducted a 12-week laboratory incubation study to determine the potential of a non-native endogeic earthworm (Aporrectodea caliginosa) to survive in a low-organic matter Colorado soil (1.4% organic C content), supplemented with or without biosolids, and to determine the effects of A. caliginosa on soil microbial biomass and soil nutrient availability. A factorial design with three main effects of A. caliginosa, biosolids addition, and time was used. Data was collected through destructively sampling at one, two, four, eight, and twelve weeks. During the 12-week study, 97.5% of the worms in the soil survived, and the survival of the earthworms was not significantly affected by the addition of biosolids. The addition of biosolids, however, did significantly reduce the gain in mass of the earthworms (8% mass gain compared to 18% in soil without biosolids). The presence of A. caliginosa significantly increased soil NH₄-N, and NO₃-N concentrations by 31% and 4%, respectively, which was less than the six fold increases in both soil NH₄-N, and NO₃-N concentrations supplied from biosolids. Microbial biomass carbon was not affected by A. caliginosa, but microbial biomass N was affected by an earthworm × biosolids interaction at week 1 and 12. We concluded that A. caliginosa can survive in a low-organic matter Colorado soil under optimal moisture content and that once established, A. caliginosa can provide modest increases in inorganic N availability to crops Colorado agroecosystems.     

Depth of cocoon deposition by three earthworm species in mesocosms

Earthworms were maintained in two types of soil-filled mesocosm. Type 1, designed for use in soil-inoculation studies, was only 0.15 m deep. Sampling revealed the position at which cocoons were deposited by earthworms in mono-species culture. Whilst adequate for shallow-working worms, larger species may have experienced restricted burrow formation and associated cocoon deposition. Therefore, Type 2 mesocosms (1.0 m deep) were also used. Here, earthworms were found to burrow throughout the soil columns, but cocoons were mainly deposited within 0.25 m of the soil surface (95% overall). The deepest cocoon deposition was at 0.4 m by Lumbricus terrestris, although 45% of the cocoons for this species were located in the upper 0.05 m of the soil, compared with 70% and 71% for Aporrectodea longa and Octolasion cyaneum, respectively. Comparisons between mesocosms showed that their depth affected cocoon distribution in the soil and that differences were also present compared with field-collected results. Reasons for this are discussed, as are implications for soil inoculation with earthworms. If cocoons are viewed as a potential inoculum for soil restoration work, their harvesting and spreading in soil may assist successful colonisation.     

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.     

Fate and dispersal of recombinant bacteria in a soil microcosm containing the earthworm Lumbricus terrestris

Summary A model ecosystem was designed containing Lumbricus terrestris in soil. The microcosm is suitable for assessing the dispersal and survival of genetically engineered microorganisms. After the inoculation of genetically engineered microorganisms their number in the worm excretions decreased continuously to reach the level of the detection limit within 50 days.     

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

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

Maize residue application reduces negative effects of soil salinity on the growth and reproduction of the earthworm Aporrectodea trapezoides,in a soil mesocosm experiment

We studied the effects of maize residue application on some life-cycle parameters of the earthworm Aporrectodea trapezoides in saline agricultural soils with electrical conductivity (EC) ranging from 1.58 to 7.35 dS m⁻¹. This experiment was carried out under controlled laboratory conditions for 150 days. Results showed that soil salinity significantly affected the growth and reproduction of earthworms, decreasing survival, numbers and mean fresh weights of adults, juveniles and cocoons. Maize residue application gave a greater survival of earthworms at all salinity levels, but the differences were only significant at an EC of 7.35 dS m⁻¹, although the mean weight of adult earthworms was significantly increased by maize residue application at all salinity levels. At an EC of 1.58 dS m⁻¹ and 3.35 dS m⁻¹, the application of maize residues gave significantly higher numbers of cocoons and juveniles, but in soils with 5.26 dS m⁻¹ and 7.35 dS m⁻¹ earthworms did not produce any cocoons over the experimental period, irrespective of maize residue application. These results indicated that maize residue application alleviated the negative effects of soil salinity on the growth and reproduction of A. trapezoides up to 3.35 dS m⁻¹, above which maize residues only increased the growth but not on the reproduction of earthworms.     

Differential morphogenetic responses, ginsenoside metabolism and RAPD patterns of three Panax species

Genetic and metabolomic demarcations between two Indian and one American congeners of Genus Panax have been discerned. Genomic DNA was isolated from the root derived callus cultures of these species and amplified by AP-PCR. RAPD analyses of the DNA with six most responding arbitrary oligonucleotide decamers provided a total of 70 reproducible bands for computation of the similarity matrix amongst the Panax species. Only 18 of these were monomorphic giving an estimate of about 74% polymorphism among the test species examined. The similarity coefficient values based on the amplification pattern support an equidistant position of the three test species. The molecular demarcations between the species are also manifested in terms of their characteristic cultural requirements, in vitro growth kinetics, regeneration competence and ginsenoside complement of their calli. The Indian congeners i.e. P. sikkimensis and P. pseudoginseng were distinguishable by higher proportions of ginsenoside Rf and Ro (40% and 20%, respectively) in the crude saponin fractions. Furthermore P. quinquefolium calli mainly accumulated ginsenoside Rb₂ and Rg₁, whilst P. sikkimensis callus was rich in Rd fraction. P. quinquefolium showed high similarity with P. sikkimensis with respect to plasticity and totipotency for somatic embryogeny whereas P. pseudoginseng callus was highly recalcitrant and lacked regenerative capacity. The chemical and genetic fingerprints alongwith morphogenetic responses of the three species under controlled in vitro environment strongly advance the case of P. sikkimensis as an independent species, rather than a conglomerate of location specific variety or sub-species of P. pseudoginseng. The findings are also of relevance to formulations and evaluation of ginseng-based health foods.