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     

Sublethal effects of imidacloprid on the burrowing behaviour of two earthworm species: Modifications of the 3D burrow systems in artificial cores and consequences on gas diffusion in soil

Earthworms have been termed ‘ecosystem engineers’ (sensu [Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosysem engineers. Oikos 69, 373-386.]) because of the important roles they play in the soil. As a consequence, it is assumed that if earthworms change their behaviour following exposure to pesticides or pollutants this could have a drastic impact on soil functioning. To test this assumption under laboratory conditions, we studied the burrow systems made by two earthworm species (the anecic Aporrectodea nocturna and the endogeic Allolobophora icterica) in artificial soil cores containing imidacloprid, a widely used neonicotinoid insecticide. After 1-month incubation period, the macropores created in the soil core were analyzed by tomography. In order to further characterize transfer properties associated with burrow systems gas diffusion measurements were also carried out. The burrow systems made by the two earthworm species were very different: A. nocturna made more continuous, less branched, more vertical and wider burrows than A. icterica. Some changes to A. nocturna burrow systems were observed after exposure to imidacloprid (they made a smaller burrow system and burrows were more narrow), but only at the highest concentration of imidacloprid used (0.5 mg kg⁻¹). A. icterica worms were more sensitive to imidacloprid and many differences in their burrow systems (length, sinuosity, branching rate and number of burrows) were observed at both concentrations tested (0.1 and 0. 5 mg kg⁻¹). As a consequence, the continuity of the burrow systems made by both species was altered following imidacloprid treatment. Gas diffusion through the A. nocturna soil cores was reduced but no difference in gas diffusion was observed in the A. icterica soil cores.     

Effect of earthworm activity (Aporrectodea giardi) on atrazine adsorption and biodegradation

We investigated the influence of earthworm (Aporrectodea giardi) activity on soil properties and on atrazine (AT) adsorption and biodegradation by comparing a coarse‐textured smectite‐free wetland soil (Brittany, France) with the earthworm casts derived from the top horizon of this soil. Casts are characterized by lower pH, are enriched in organic carbon (OC) and clay content, have a larger cation exchange capacity, and a greater exchangeable Ca content. The clay mineralogy of the soil studied and casts is characterized by a muscovite–kaolinite–chlorite association. In addition, the clay fraction of the soil contains lepidocrocite (γ‐FeOOH), which was not found in the casts. Atrazine adsorption isotherms were reasonably well described by the Freundlich equation and were all non‐linear. The mean amounts of adsorbed AT for starting concentrations of 3–30 mg litre^?1 ranged from 8 to 34%, being largest in earthworm casts. Soil AT adsorption capacity was well correlated with OC content. Non‐decomposed organic matter present in the coarse size fractions and specific compounds present in earthworm casts (proteins, mono‐ and polysaccharides, polyphenols, sugars, lignin) and microbial and fungal biomass contribute to AT adsorption. Weak electrostatic (physical) sorption of AT on organic compounds and on mineral surfaces prevails. For casts, the formation of additional hydrophobic interactions between AT and SOM is proposed. We also studied AT biodegradation by the model bacterium Pseudomonas sp. strain ADP in the presence of soils or earthworm casts. An enhancement of the AT disappearance rate was observed in the presence of all the solid matrices tested compared with that obtained in an aqueous medium. The biodegradation rate was shown to be dependent not only on the OC content of the solid matrix, but mainly on its composition and structure.     

Effect of food type and placement on earthworm (Aporrectodea tuberculata) burrowing and soil turnover

Subsurface-dwelling Aporrectodea tuberculata, a common earthworm in Upper-Midwest (USA) agricultural fields, may be a significant component of agroeco-systems with regard to soil mixing and preferential transport of water and chemicals. In this study we looked at effects of food residue placement and food type on A. tuberculata burrowing and soil turnover in two-dimensional Evans box microcosms. Four food residue placements mimicked patterns induced by primary tillage and two food types, readily available and natural food sources, with no food as a control. An average earthworm population of 100 earthworms m^-2 was calculated to generate 1058 km ha^-1 of new burrows and turnover 7.9 Mg ha^-1 of soil in 1 week of activity at 20°C. Burrowing was random until food sources were encountered, at which time burrowing appeared to center around the food source.     

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.     

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.     

Toxic effects of two organophosphate insecticides,monocrotophos and dichlorvos to common earthworm Lampito Mauritii (Kinberg)

The lethal concentrations (LC₅₀ 96 h^?1) were measured experimentally by exposing the earthworms (Lampito mauritii) in moist vermiculite and in water. The morphological changes observed during the exposure of animals to the monocrotophos and dichlorvos were outlined. The mortality rate was higher in the water medium than in moist vermiculite. The hyperactivity at low pesticide concentrations is found to influence the size of the population.     

Terbuthylazine and carbofuran effects on growth and reproduction within three generations of Eisenia andrei (Oligochaeta)

Sublethal effects of terbuthylazine and carbofuran on the growth and reproduction of Eisenia andrei were investigated over a period of three generations. Reproduction was assessed by measuring the coccon production of worms treated chronically with pesticides. Inhibition of cocoon production was found in the parental generation. Hatchlings were raised from cocoons to provide the F₁ generation. During raising a more rapid growth of juveniles treated with terbuthylazine was observed, compared with the growth of untreated worms. The increase in vitality was also found in cocoon production. Groups treated with terbuthylazine produced more cocoons than controls. The F₂ generation was raised from hatchlings of the F₁ generation, and here, also the terbuthylazine treatments increased earthworm growth, but not cocoon production. Exposure to carbofuran decreased cocoon production in all generations. Growth of the F₁ generation was not influenced by low concentrations of carbofuran.     

Life-cycle traits of the dimorphic earthworm species <Emphasis Type="Italic">Allolobophora chlorotica</Emphasis> (Savigny, 1826) under controlled laboratory conditions

Allolobophora chlorotica exists as two colour morphs, pink and green. Field observations have indicated that the two morphs have ecological preferences linked to soil moisture: the green morph dominating in wet soils and the pink morph in dry soils. The aim of this laboratory-based research was to investigate the potential differences in fitness and adaptation to soil-moisture conditions of the two morphs measured in terms of growth rate, reproductive output and cocoon viability. An initial experiment maintained hatchlings of both morphs individually under standard culture conditions. On maturation, these were paired (intra-morph), and cocoon production, viability and incubation time were determined. The green morph had significantly faster (P < 0.01) growth rates than the pink morph. Cocoon production was also significantly greater in the green compared with the pink morph (3.2 and 1.5 cocoons worm⁻¹ 28 days⁻¹, respectively) with corresponding viabilities of 87 and 58%. In a second experiment, the growth rates of pink and green hatchlings were assessed under wet and dry soils (29 and 21% soil moisture, respectively). The growth of the pink morph was not influenced significantly (P > 0.05) by soil moisture. In contrast, lower soil-moisture content significantly (P < 0.05) slowed growth and maturation of the green morph. These results support field observations relating to distribution of the two A. chlorotica colour morphs. We suggest that soil-moisture content may act to isolate these morphs, providing, in extremes, a barrier to inter-morphic mating.     

The effect of two endogeic earthworm species on zinc distribution and availability in artificial soil columns

The objective of this study was to determine the impact of earthworm bioturbation on the distribution and availability of zinc in the soil profile.Experiments were carried out with Allolobophora chlorotica and Aporrectodea caliginosa in 24 perspex columns (∅ 10 cm), filled with 20-23 cm non-polluted soil (OM 2%, clay 2.9%, pH 0.01 M CaCl₂ 6.4), that was covered by a 3-5 cm layer of aged zinc spiked soil (500 mg Zn/kg dry soil) and another 2 cm non-polluted soil on top. After 80 and 175 days, columns were sacrificed and each cm from the top down to a depth of 15 cm was sampled. Earthworm casts, placed on top of the soil, were collected. Each sample was analyzed for total and CaCl₂-exchangeable zinc concentrations.Effects of earthworm bioturbation were most pronounced after 175 days. For A. chlorotica, total and CaCl₂-exchangeable zinc concentrations in the polluted layers were lower with than without earthworms. Total zinc concentrations in the non-polluted layers were higher in columns with earthworms. Casts of A. chlorotica collected on the soil surface showed slightly higher total zinc concentrations than non-polluted soil. Casts were found throughout the whole column. For A. caliginosa there were no differences in total zinc concentration between columns with and without earthworms. CaCl₂-exchangeable zinc concentrations in the polluted layers were lower for columns with earthworms. Casts were mainly placed on top of the soil and contained total zinc concentrations intermediate between those in non-polluted and polluted soil layers.This study shows that different endogeic earthworm species have different effects on zinc distribution and availability in soils. A. chlorotica transfers soil throughout the whole column, effectively mixing it, while A. caliginosa decreases metal availability and transfers polluted soil to the soil surface.     

Influence of animal wastes on growth and reproduction of the African earthworm species Eudrilus eugeniae (Oligochaeta)

The growth and reproduction of Eudrilus eugeniae were evaluated in four animal species wastes under laboratory conditions. Two hatchlings were introduced in 100 g of each animal waste i.e. cow, sheep, pig, and chicken after 15 days of pre-composting. Biomass gain, mortality, sexual maturity, and cocoons production were monitored periodically for 21 weeks. No mortality was observed in any waste. The maximum weight gain per worm and the highest growth rate per worm per week were obtained in chicken waste. Net biomass gain per worm were 1.01 ± 0.52 g, 1.318 ± 0.07 g, 0.87 ± 0.1 g, and 1.69 ± 0.15 g respectively for cow, sheep, pig, and chicken wastes. The highest number of cocoons produced per worm per day was obtained in chicken waste followed in decreasing order by sheep, cow, and pig waste. The mean number of cocoons produced per worm per day in chicken waste was 40.87% greater than these produced per day in pig waste.Among the four animal species, chicken, sheep, and cow were the most favourable wastes for the growth and reproduction of E. eugeniae, and hence can be recommended as feed materials in large scale vermicomposting facilities.     

Effects of seasonal and diurnal temperature fluctuations on population dynamics of two epigeic earthworm species in forest soil

Temperature fluctuations are a fundamental entity of the soil environment in the temperate zone and show fast (diurnal) and slow (seasonal) dynamics. However, responses of soil ecosystem engineers, such as earthworms, to annual temperature dynamics are virtually unknown. We studied growth, mortality and cocoon production of epigeic earthworm species (Lumbricus rubellus and Dendrobaena octaedra) exposed to temperature fluctuations in root-free soil of a mid-European beech-oak forest. Both earthworm species (3 + 3 individuals of each species) were kept in microcosms containing soil stratified into L, F + H and A_h horizons. In the field, earthworm responses to smoothing of diurnal temperature fluctuations were studied, simulating possible global change. In the laboratory, earthworm responses to seasonal (±5 °C of the annual mean) and diurnal temperature fluctuations (±5 °C of the seasonal levels) were analyzed in a two-factorial design. Both experiments lasted 12 months to differentiate between seasonal and diurnal responses. In the third experiment overwintering success of both earthworm species was investigated by comparing effects of constant temperature regime (+2 °C), and daily or weekly temperature fluctuations (2 °C ± 5 °C).Temperature regime strongly affected population performance of the earthworms studied. In the field, smoothed temperature fluctuations beneficially affected population development of both earthworm species (higher biomass, faster maturity and reproduction, lower mortality). Consequently, density of both species increased faster at smoothed than at ambient temperature conditions. In the laboratory, responses of L. rubellus and D. octaedra to temperature treatments differed; however, in general, earthworms benefited from the absence of diurnal fluctuations. Total earthworm numbers were at a maximum at constant temperature and lowest in the treatment with both diurnal and seasonal temperature fluctuations. However, after one year L. rubellus tended to dominate irrespective of the temperature regime. In the overwintering experiment L. rubellus sensitively responded to even short-term winter frost and went extinct after one week of frost whereas D. octaedra much better tolerated frost conditions. Earthworms of both species which survived frosts were characterized by a significant body weight decrease during the period of frosts and fast recovery in spring suggesting a different pattern of individual resource expenditure as compared with constant +2 °C winter regime. Contrasting trends in the population dynamics of L. rubellus and D. octaedra during the frost-free period and during winter suggest that in the long-term temperature fluctuations contribute to the coexistence of decomposer species of similar trophic position in the forest litter. The results are discussed in context of consequences of climate change for the functioning of soil systems.     

Effects of liming on survival and reproduction of two potentially invasive earthworm species in a northern forest Podzol

During the last several decades, colonization of soil by exotic earthworms and their effects on soil properties and biodiversity have been reported in forests of North America. In some northern hardwood stands, acid soils or harsh climate may have prevented earthworm colonization. However, climatic change and the increasing use of liming to restore the vigor of declining sugar maple (Acer saccharum Marsh.) stands, situated on base-poor soils in USA and Canada, could make many of these sites more suitable for earthworm colonization. We tested survival and reproduction of two exotic earthworm species (Lumbricus terrestris and Amynthas hawayanus) in unlimed and limed soils at the northern limit of the northern hardwood forest distribution in Canada. Improving soil parameters of base-poor, acidic soils by liming positively influenced activity, survivability and reproductive output of L. terrestris in this northern hardwood forest. In contrast, the high mortality and low vigor of L. terrestris observed in the unlimed plots show that soils in this area with a pH of 4.3 are not favorable to this species. Our results suggest that A. hawayanus was very active prior to winter at both soil pHs, but was not able to complete its life cycle during one year at this latitude. Both earthworm species significantly reduced organic C and total N, and increased the C/N ratio of the forest floor. Given that forest liming activities are increasing in proximity to human activities, there is high probability that some earthworm species, such as L. terrestris, will invade limed northern hardwood forests in the next decades, with possible consequences for soil organic matter turnover, nutrient cycling and forest biodiversity and dynamics.     

DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine

To evaluate atrazine (2-chloro-4-ethylamino-6-isopropylamino-1, 3, 5-triazine) ecotoxicology in soil, the effect of atrazine on the activity of antioxidative enzymes (superoxide dismutase, SOD; catalase, CAT; and guaiacol peroxidase, POD) and DNA damage induced by atrazine were investigated in earthworms. Atrazine was added to artificial soil at rates of 0, 2.5, 5 and 10 mg per kg of soil. Earthworm tissues exposed to each treatment were collected on the 7th, 14th, 21st, and 28th day of the treatment. Compared to the controls, the CAT activity was stimulated at 2.5 mg kg⁻¹ treatment except on the 14th day, and inhibited at 5, 10 mg kg⁻¹ atrazine except 5 mg kg⁻¹ on the 28th day and 10 mg kg⁻¹ on the 21st day; the overall SOD activity was inhibited, while the POD activities were stimulated by all atrazine concentrations in 28 days. The olive tail moments of single-cell gel electrophoresis of coelomocytes, as an indication of DNA damage, were increased after treatment with different doses of atrazine on the 7th, 14th, 21st, and 28th day, and significant differences were found compared to the controls. In conclusion, atrazine induces oxidative stress and DNA damage on earthworms, and the adverse effects may be the important mechanisms of its toxicity to earthworms.     

The effects of low lead levels on the growth and reproduction of the African earthworm Eudrilus eugeniae (Oligochaeta)

 The effects of sublethal concentrations of lead nitrate on the growth and reproduction of the African composting earthworm species, Eudrilus eugeniae, was studied by exposing worms in an organic substrate to lead-nitrate-contaminated food over a period of 76 days. The results revealed that growth was initially affected negatively by the presence of lead, while the maturation rate and cocoon production were not affected. In agreement with other studies on Eisenia fetida, cocoon viability was affected negatively by lead, making this a sensitive toxicity endpoint. Received: 14 October 1998     

Disentangling effects of habitat diversity and area on orthopteran species with contrasting mobility

Loss of semi-natural grasslands and reduction of habitat diversity are considered major potential threats to arthropod diversity in agricultural landscapes. The main aim of this study was to investigate how area and habitat diversity, mediated by shrub encroachment after grassland abandonment, affect species richness of orthopterans in island-like grasslands, and how contrasting mobility might alter species richness response to both factors. We selected 35 isolated patches in landscapes dominated by arable land (durum wheat) in order to obtain two statistically uncorrelated gradients: (i) one in habitat area ranging from 0.2 to 55 ha and (ii) one in habitat diversity ranging from patches dominated by one habitat (either open grasslands or shrublands) to patches with a mosaic of different habitats. Habitat loss due to land-use conversion into arable fields was associated with a substantial loss of species with a positive species-area relationship (SAR), with sedentary species having a steeper and stronger SAR than mobile species. Halting habitat loss is, therefore, needed to avoid further species extinctions. Shrub encroachment, triggered by abandonment, presented a hump-shaped relationship with habitat diversity. An increase in habitat diversity enhanced species richness irrespective of patch area and mobility. Maintaining or enhancing habitat diversity, by cutting or burning small sectors and by reintroducing extensive sheep grazing into abandoned grassland, are suggested as complementary strategies to mitigate further decline of orthopteran diversity in the remnant patches. This would be equally important in both small and large patches.     

Influence of drying and ageing on the stabilization of earthworm (Lumbricidae) casts

The influence of drying and ageing on the stabilization of casts produced by the endoge′ic earthworm, Aporrectodea rosea, from a soil, which was hard-setting and low in organic matter, were investigated in the laboratory. Casts and uningested soil were aged-most for up to 32 days, dried for up to 21 days, or subjected to different wetting and drying cycles over 30 days. The dispersion index of aged-moist casts decreased from 0.40 to 0.25 over 32 days, while dispersion index of dried casts decreased from 0.40 to 0.01 over 21 days. The dispersion index of air-dried casts was not significantly increased by five cycles of wetting and drying. The dispersion index of dried casts was not significantly less than that of dried soil. In soils wetter than a matric potential of approximately –35kPa, stabilization of casts was probably due to a combination of cohesion of soil particles, age-hardening and growth of microorganisms. However, in soils drier than –35kPa, cementation was probably the major mechanism of stabilization. The addition of wheat straw to the soil prior to ingestion by earthworms increased dispersion from aged-moist casts, but did not influence dispersion from dried casts. The addition of wheat straw decreased the number of air-dried casts which slaked severely. The concentration of soluble carbohydrate decreased with dispersion index as casts and uningested soil were each dried. This suggested that soluble carbohydrate may have been denatured with or without being bonded to soil particles during drying. Received: 7 May 1996