Endogeic Earthworm Species Research Articles

Management of grassland: A necessary tool to maintain plant and earthworm diversity

In temperate grassland, earthworms contribute to the major soil processes which determine most of the ecosystem services. The characteristics of plant communities in grassland are key factors in maintaining earthworm communities, however effects of different herbage management on earthworms remain largely unknown. In this context, the aim of the present study was to determine the long-term effects of herbage management on grassland plant and earthworm communities. Plants and earthworms were sampled in a 14-years-old experiment in upland grasslands (Massif central, France). Abandoned grasslands were compared with mowed grasslands and with pastures grazed by cattle (at low or high intensities) or grazed by sheep (at low intensity). Compared to abandoned grassland, herbage management by grazing or by mowing display higher leguminous plant, community-weighted mean Ellenberg light values as well as plant richness while they display lower percentage of plant litter and community-weighted mean Ellenberg nitrogen values. The differences in plant richness were associated with a significant change in plant community structure. Compared to the abandoned grassland, herbage management by grazing or mowing significantly display higher earthworm biomass and total richness. Except for pastures grazed by cattle at high intensity, earthworm abundance was at least twice that in the grassland at low grazing intensity or mowing compared to the abandoned grassland. Earthworm communities were significantly different between grazed and mown treatments notably due to changes within Aporrectodea anecic and endogeic earthworm species. Overall, herbage management by animals or by mechanical export is beneficial for plant and earthworm diversity although no clear differences between management practices for earthworm richness, total biomass or total abundance were observed. Our results highlight that abandonment does not preserve biodiversity (plant, soil macrofauna) while management of grassland by grazing or mowing is a necessary tool for biodiversity conservation and improvement.

Role of soil texture and earthworm casts on the restoration of soil enzyme activities after exposure to an organophosphorus insecticide

Pesticides exert important effects on the soil fauna and health. However, little is known about the interactions of soil, microorganisms and earthworms in the presence of pesticides and about their respective roles in the soil biological activity. The aim of this study was to evaluate the effect of the soil type on enzyme activities, measured in bulk soil and in casts of two earthworm species, after exposure to the organophosphorus pesticide parathion. To this aim, two endogeic earthworm species (Apporectodea caliginosa and Allolobophora chlorotica) were cross-acclimated in two different soil textures (each representing the most favorable soil environment for that species). Enzyme activities were measured as a soil quality indicator in samples of bulk soil (collected at day 4 and day 7 of exposure to parathion) and in earthworm casts (collected at day 7). A short exposure (4 days) to parathion significantly (ANOVA, p < 0.001) inhibited carboxylesterases (25–43 % of inhibition) and alkaline phosphatase (∼23 % of inhibition). At day 7 of exposure, parathion impact on the overall soil enzyme activities mainly depended on the soil texture. Indeed, activity inhibition was higher (ANOVA, p < 0.001) in silt-clay soil (decrease by 37 %) than in silt-loamy soil (decrease by ∼18 %). Conversely, parathion effect was not influenced by earthworm presence/absence and earthworm species. However, after soil exposure to parathion, earthworms (both species) improved enzyme activity restoration in their casts.

Reasons to move far away: studying the drivers of Carpetania matritensis (Hormogastridae: Crassiclitelatta) dispersal behaviour

Dispersal is a crucial process for animal populations as it allows the colonisation of new habitats and the maintenance of genetic diversity. However, it has not been studied enough for soil fauna, which is the basis for a wide variety of ecosystem services. Therefore, the study of their dispersal and the factors that trigger this behaviour is a relevant area of knowledge for the maintenance of the services they provide. For this work, Carpetania matritensis, an endogeic earthworm species endemic to the central Iberian Peninsula, has been used as a model to study the effect of habitat quality and conspecific density on dispersal and exploratory behaviour. The experiment was carried out in horizontal mesocosms divided into three sectors of the same dimensions: an inoculation section (left), a crossing section (centre) and a target sector (right). Those sectors were occupied by soil, a favourable habitat for earthworms, or sand, which represents an unsuitable habitat for earthworms and a physical barrier for their displacement. Earthworms were inoculated at two different densities (2 and 6 individuals per mesocosm; 848.86 and 2546.58 individuals/m3 respectively) and at two experimental durations (4 and 8 days) for each of the three different experimental treatments (unsuitable-unsuitable-suitable (U-U-S), suitable-unsuitable-suitable (S-U-S) and suitable-suitable-suitable (S-S-S), depending on the habitat type filling the inoculation, crossing and target section respectively). The results showed a large effect of treatment on the dispersal rate, being higher when earthworms were inoculated in an adverse environment, establishing habitat quality as a driver of the species’ dispersal behaviour. No significant effects of conspecific density, experimental duration or its interactions were found. Further studies are needed to clarify the species dispersal behaviour with a view to its conservation.

Distribution of epi-endogeic and endogeic earthworm species (Oligochaeta: Lumbricidae) in the forest belt of the Northwest Caucasus.

The distribution of the often dominant in density and biomass epi-endogeic and endogeic earthworm species in forests of the Northwest Caucasus was estimated based on a large array of field data and GIS modeling of modern potential areas. Quantitative accountings of earthworms were conducted annually from 2014 to 2019 in different types of forests: sticky alder forest, small-leaved forests, broadleaf forests (hornbeam and beech forests), coniferous-deciduous forests, dark coniferous forests, and pine forests (792 geographic locations). It is shown that the native species of the Caucasian fauna dominate in the number and biomass from piedmont to high mountain forests. The most widespread species that is found in all types of forests from low to high mountains and makes the main contribution to the biomass of earthworms is the Crimean-Caucasian subendemic Dendrobaena schmidti. Peregrine species of epi-endogeic and endogeic earthworms inhabit sticky alder forest, small-leaved, broadleaf and pine forests in which they inhabit together with native species, while not dominating either in numbers or in biomass among other species. Dark coniferous forests are inhabited mainly by the native endogeic species D. schmidti and A. jassyensis. Maxent modeling shows that the species of the endogeic earthworm group have wider potential areas than epi-endogeic species. The most significant bioclimatic factors that make the greatest contribution to the distribution: amount of precipitation in the driest month, altitude above the sea level, isothermality.

Earthworm-biochar interactions: A laboratory trial using Pontoscolex corethrurus

Biochar application can improve soil quality, but at high rates may cause negative effects on soil organisms such as earthworms. Conversely, as ecosystem engineers and catalysts of microbial activity, earthworms can also affect soil quality and interact with biochar, though little is known concerning endogeic earthworm species interactions with biochar. Hence, a standard ecotoxicological laboratory trial was undertaken to assess the impact of Brazil-nut husk biochar application (0, 2.5, 5 and 10% w/w) on the endogeic cosmopolitan species Pontoscolex corethrurus , and the effects of bioturbation and gut passage on biochar chemical characteristics (assessed using pyrolysis coupled with gas chromatography and mass spectrometry) and morphology (evaluated using scanning electron microscopy). Biochar addition up to 10% w/w had no negative effects on P. corethrurus , and ingested biochar particles showed signs of physical degradation and bacterial colonization. Nine pyrolysis-produced chemical biomarkers (phenolic and aromatic compounds) were detected that can be used as indicators of biochar presence in soils and earthworm castings. Earthworm casts showed distinct macromolecular chemical signatures compared with uningested artificial soil with and without biochar. Earthworm bioturbation and biochar ingestion may have important effects on functionalization and biochar chemical and physical properties that should be considered in field applications, especially where endogeic biochar-consuming species are present. • Biochar did not negatively affect P. corethrurus even at the highest dose (10% w/w). • Py-GC–MS detected various pyrolysis-produced biomarker compounds in the biochar. • Biochar in casts shows novel chemical fingerprints and a structural breakdown. • Passage through earthworm guts promotes biochar functionalization. • Earthworm biological roles should be considered in field biochar application.

Depth distribution of soil organic matter and burrowing activity of earthworms—mesocosm study using X-ray tomography and luminophores

Earthworms feed on organic matter present at the soil surface or within the soil. Thus, its distribution in the soil profile is likely to greatly influence earthworm behavior and, in turn, their burrow system. To test this idea, two anecic and two endogeic earthworm species were introduced into repacked soil cores (depth = 30 cm) upper half filled with a top soil containing 4% organic matter (0–15 cm) and lower half filled with a deep soil at 2% organic matter (15–30 cm). Earthworm behavior was studied using X-ray tomography combined with luminophores (colored particulate tracers of 63–125 μm size) placed at 0, 3, and 12 cm depth, a method widely used in sediment ecology. We observed that anecic and endogeic earthworms had contrasting reactions to the conditions with only endogeic species burrowing more intensively in the upper part. From a quantitative point of view, only a few percent of luminophores were displaced. However, luminophore displacements also provided qualitative information to complement the tomography: (i) endogeic species and especially Aporrectodea caliginosa bioturbated the most soil close to the surface (3 cm depth) and (ii) the two anecic species influenced the luminophore distribution differentially with Lumbricus terrestris displacing significantly more luminophores, whatever their initial depth, than Aporrectodea nocturna due to intense surface cast activity. Beyond methodological developments, our study found that endogeic earthworms burrow more in zones with higher organic matter contents and this explains why they are mainly found close to the soil surface in non-tilled soils.

Soil dissipation and bioavailability to earthworms of two fungicides under laboratory and field conditions.

The representativeness of laboratory studies of the fate of pesticides in soil in field conditions is questionable. This study aimed at comparing the dissipation and bioavailability to earthworms of two fungicides, dimoxystrobin (DMX) and epoxiconazole (EPX), over 12months under laboratory and field conditions. In both approaches, the fungicides were applied to the same loamy soil as a formulated mixture at several concentrations. We determined total DMX and EPX concentrations in the soil using exhaustive extraction, their environmental availability using mild extraction and their bioavailability through internal concentrations in exposed earthworms. The initial fungicide application appeared as much better controlled in terms of dose and homogeneity in the laboratory than in the field. One year after application, a similar dissipation rate was observed between the laboratory and field experiments (ca 80% and 60% for DMX and EPX, respectively). Similarly, the ratio of available/total concentrations in soil displayed the same trend whatever the duration and the conditions (field or lab), EPX being more available than DMX. Finally, the environmental bioavailability of the two fungicides to earthworms was heterogeneous in the field, but, in the laboratory, the bioaccumulation was evidenced to be dose-dependent only for DMX. Our findings suggest that the actual fate of the two considered fungicides in the environment is consistent with the one determined in the laboratory, although the conditions differed (e.g., presence of vegetation, endogeic earthworm species). This study allowed better understanding of the fate of the two considered active substances in the soil and underlined the need for more research dedicated to the link between environmental and toxicological bioavailability.

Elucidating pesticide sensitivity of two endogeic earthworm species through the interplay between esterases and glutathione S-transferases

Earthworms are common organisms in soil toxicity-testing framework, and endogeic species are currently recommended due to their ecological role in agroecosystem. However, little is known on their pesticide metabolic capacities. We firstly compared the baseline activity of B-esterases and glutathione-S-transferase in Allolobophora chlorotica and Aporrectodea caliginosa. Secondly, vulnerability of these species to pesticide exposure was assessed by in vitro trials using the organophosphate (OP) chlorpyrifos-ethyl-oxon (CPOx) and ethyl-paraoxon (POx), and by short-term (7 days) in vivo metabolic responses in soil contaminated with pesticides. Among B-esterases, acetylcholinesterase (AChE) activity was abundant in the microsomal fraction (80% and 70% of total activity for A. caliginosa and A. chlorotica, respectively). Carboxylesterase (CbE) activities were measured using three substrates to examine species differences in isoenzyme and sensitivity to both in vitro and in vivo exposure. CbEs were mainly found in the cytosolic fraction (80% and 60% for A. caliginosa and A. chlorotica respectively). GST was exclusively found in the soluble fraction for both species. Both OPs inhibited B-esterases in a concentration-dependent manner. In vitro trials revealed a pesticide-specific response, being A. chlorotica AChE more sensitive to CPOx compared to POx. CbE activity was inhibited at the same extent in both species. The 7-d exposure showed A. chlorotica less sensitive to both OPs, which contrasted with outcomes from in vitro experiments. This non-related functional between both approaches for assessing pesticide toxicity suggests that other mechanisms linked with in vivo OP bioactivation and excretion could have a significant role in the OP toxicity in endogeic earthworms.

Dominant tree species and earthworms affect soil aggregation and carbon content along a soil degradation gradient in an agricultural landscape

Soil organic matter (SOM) is considered an important determinant of soil fertility in tropical agroecosystems. While numerous studies have shown the value of agroforestry in increasing soil nutrients and improving crop yield, few have addressed the systematic impacts of duration of cultivation on soil aggregation and C storage in such systems. A study was conducted in South Nandi (Kenya) to assess spatial influence of three dominant trees (Croton megalocarpus, Eucalyptus grandis and Zanthoxylum gilletii) on soil aggregation and C content in agroforestry systems. The study was conducted in a chronosequence experimental set-up where farms were continuously cultivated for 10, 16 and 62 years since conversion from primary forest. It was hypothesized that soil aggregates and whole soil and aggregate-associated C would decrease with duration of cultivation, with the magnitude of influence being reduced by the presence of trees and abundance of earthworms and termites. Greater abundance of small macroaggregates and microaggregates were recorded in soils under the canopy of Z. gilletii with an average weight of 62.8 g and 9.4 g 100 g−1 of soil compared to 53.9 g and 3.1 g 100 g−1 in soils under C. megalocarpus and 48.7 g and 3.9 g 100 g−1 in soils under E. grandis, respectively. These differences could be attributed to the high number of endogeic earthworm species, Nematogenia lacuum (Ocnerodrilidae) in soils under the canopy of Z. gilletii trees. Since N. lacuum is a small-sized species (40–55 mm long), it produces small faecal pellets and thus, we could infer that this species may have contributed to the fragmentation of large macroaggregates into small macroaggregates and microaggregates. The C content decreased by almost 40% in soils under longer duration of cultivation, with higher magnitude of differences associated with Z. gilletii trees. Increased microbial population in earthworms’ casts can increase mineralization rates, which may explain the low aggregate-associated C content under Z. gilletii trees where high number of N. lacuum were recorded. This study shows the significance of specific trees in shaping soil aggregation process and soil C content which could have far-reaching implications for the long-term C storage in the soil and hence net contributions to climate change mitigation.

Combining bulk and amino acid stable isotope analyses to quantify trophic level and basal resources of detritivores: a case study on earthworms.

Quantification of the bacterial, fungal, and plant energy channels to the nutrition of detritivores is methodologically challenging. This is especially true for earthworms that ingest large amounts of litter and soil mixed with microorganisms. Novel methods such as compound-specific stable isotope analysis (CSIA) of C and N of individual amino acids promise major progress in this field in comparison with bulk stable isotope analysis (bulk SIA). Here, we combine CSIA and bulk SIA of carbon and nitrogen to quantify the linkage of epigeic and endogeic earthworm species to different energy channels across boreal and temperate forest ecosystems. The results showed pronounced flux of energy directly from plants to earthworms (33-50% of essential amino acids, EAA) refining the position of earthworms in soil food webs as both competitors and consumers of microorganisms. Epigeic earthworm species primarily relied on plant litter and endogeic species primarily relied on bacteria and soil organic matter. The linkage of both groups to plant or microbial energy channel was likely driven by the quality of detritus. Both bulk 15N and 13C enrichments were related to the trophic level of earthworms. Furthermore, 15N enrichment was related to the proportions of bacterial and plant EAA in the diet. Strong negative correlation between trophic level (CSIA of nitrogen) and the proportion of plant EAA (CSIA of carbon) suggests that both novel methods can indicate the degree of microbivory in detritivores. CSIA of amino acids provide detailed and baseline-independent information on basal resources and trophic levels of detritivores.

Interspecific differences in biochemical and behavioral biomarkers in endogeic earthworms exposed to ethyl-parathion

Earthworms are common organisms in the soil toxicity-testing framework, and the epigeic Eisenia andrei and E. fetida are the recommended species. However, Eisenia species are rarely found in agricultural soils and recent studies have pointed out endogeic species are more sensitive to pesticides than Eisenia. Allolobophora chlorotica and Aporrectodea caliginosa are two endogeic soil-dwelling species that are abundant in the agroecosystem. However, knowledge on pesticide impact on this ecological group of earthworms is still incipient. Herein, we compared the biochemical (acetylcholinesterase [AChE] and carboxylesterase [CbE] activities) and behavioral (burrowing, casting and feeding) biomarker responses of these two endogeic earthworm species exposed for 7 days to soils contaminated with 0.1, 1 and 10 mg kg−1 ethyl-parathion. The results showed marked species-specific differences in both groups of biomarkers, suggesting A. caliginosa the most sensitive species to this organophosphorus pesticide under the exposure conditions in this study. Moreover, an in vitro inhibition trial with ethyl-paraoxon evidenced a higher sensitivity of A. caliginosa AChE activity compared with that of A. chlorotica. This finding suggested that this molecular target endpoint could contribute to the interspecific differences of behavioral responses rather than CbE activity; this latter considered a potent mechanism of OP removal. Our results suggest the inclusion of more than one endogeic earthworm species to assess toxicity from organophosphorus insecticides. However, the use of A. caliginosa in the environmental risk assessment framework of organophosphorus contamination is highly recommended because of its higher sensibility to this class of pesticides, in addition to its abundance in the agroecosystem.

Landscape features impact connectivity between soil populations: a comparative study of gene flow in earthworms.

Landscape features are known to alter the spatial genetic variation of aboveground organisms. Here, we tested the hypothesis that the genetic structure of belowground organisms also responds to landscape structure. Microsatellite markers were used to carry out a landscape genetic study of two endogeic earthworm species, Allolobophora chlorotica (N=440, eight microsatellites) and Aporrectodea icterica (N=519, seven microsatellites), in an agricultural landscape in the North of France, where landscape features were characterized with high accuracy. We found that habitat fragmentation impacted genetic variation of earthworm populations at the local scale. A significant relationship was observed between genetic diversity (He , Ar ) and several landscape features in A.icterica populations and A.chlorotica. Moreover, a strong genetic differentiation between sites was observed in both species, with a low degree of genetic admixture and high Fst values. The landscape connectivity analysis at the regional scale, including isolation by distance, least-cost path and cost-weighted distance approaches, showed that genetic distances were linked to landscape connectivity in A.chlorotica. This indicates that the fragmentation of natural habitats has shaped their dispersal patterns and local effective population sizes. Landscape connectivity analysis confirmed that a priori favourable habitats such as grasslands may constitute dispersal corridors for these species.

Effects of soil and leaf litter quality on the biomass of two endogeic earthworm species

Earthworms drive important ecosystem functions like decomposition and nutrient mineralization in many terrestrial ecosystems, which is why factors controlling their mass gain are of great scientific interest. We conducted a microcosm experiment using two common endogeic earthworm species (Aporrectodea caliginosa and Octolasion tyrtaeum) and two different soils (one from a beech-dominated forest and one from a mixed tree species forest in Germany) to test litter quality (different nutrient concentrations) and soil quality effects (low and high) on relative mass gain of earthworms. We hypothesized that mass gain of endogeic earthworms is driven by both soil and litter quality. Soil pH, carbon (C) and nitrogen (N) concentrations were used to characterize soil quality, while leaf litter N, phosphorus (P), calcium (Ca), and magnesium (Mg) concentrations were used as proxies for leaf litter quality. Forest soils were incubated with leaf litter of six common tree species in Central Europe (Fagus sylvatica, Acer platanoides, Acer pseudoplatanus, Carpinus betulus, Tilia spp., and Fraxinus excelsior) that span a gradient in leaf litter quality. In addition, we determined soil microbial biomass C as a potential food source of endogeic earthworms. After three months, relative earthworm mass gain of A. caliginosa and O. tyrtaeum was significantly higher in soil from the mixed tree species forest (high quality soil: +218% and +240%, respectively) compared to soil from the beech-dominated forest (low quality soil: +160% and +162%, respectively). Relative mass gain of A. caliginosa increased significantly with all leaf litter nutrients in low quality soil, whereas in high quality soil only leaf litter Ca positively affected relative mass gain. Similarly, relative mass gain of O. tyrtaeum increased significantly with increasing concentrations of leaf litter N, Mg, and Ca in the low quality soil. In the high quality soil, only leaf litter Mg significantly increased relative mass gain. Overall, our results indicate that leaf litter quality effects on endogeic earthworm mass gain were more important in low quality soil for both earthworm species. Notably, microbial biomass was significantly higher in high quality soil (506 ± 135 μg C g−1 soil dw) compared to low quality soil (217 ± 64 μg C g−1 soil dw), but microbial biomass was not significantly affected by leaf litter type and was a poor predictor of relative earthworm mass gain. This finding indicates that endogeic earthworms did not significantly depend on soil microbial biomass, but rather on the quality of dead organic material in the soil and surface leaf litter. As earthworms may prefer feeding on certain microbial taxa, and we only measured total soil microbial biomass, future studies could investigate if leaf litter quality effects on earthworms are mediated by changes in soil microbial community structure, micronutrients, and organic compounds.

Effect of the endogeic earthworm Aporrectodea tuberculata on aggregation and carbon redistribution in uninvaded forest soil columns

The long-term impact of earthworm presence on soil carbon (C) dynamics of previously uninhabited northeastern forests is still largely unknown. Currently, earthworm presence is understood to both enhance soil respiration and create stable microaggregates, processes assumed to have conflicting effects on long term C storage. To date, studies investigating earthworm-created microaggregates and occluded C have rarely been done in undisturbed forest soils. A paired mesocosm study (n = 5) was conducted investigating the impact of the endogeic earthworm species Aporrectodea tuberculata on the physical proportion of microaggregates and the associated mineral soil C of a minimally disturbed forest soil. Pairs analyzed after 4 weeks of incubation demonstrated no significant aggregate effects. At 4 months, paired cores with earthworms (WW) showed a 67% increase in large macroaggregates (>2000 μm diameter, lgMA), compared to cores without earthworms (NW). While distribution shifted among various microaggregate pools (free and occluded within macroaggregates), the net proportion of microaggregates in the soil (dry weight basis) was unaltered. After 4 months, the mineral soil of WW cores had an average of 60% more C than the NW cores due to the relocation of the forest floor. The C associated with the microaggregate fractions increased an average of 56%. Of this increase in C, 95% was accounted for by the microaggregates occluded within the lgMA fraction, a fraction that was almost 4 times greater in the WW cores. Over 50% of the C relocated into the mineral soil was associated with the physically protected microaggregate fractions, indicating that though this species of earthworm did not alter the proportion of microaggregates in these soils, they occluded a substantial proportion of C within those physical fractions. In this particular forest soil, the actions of Aporrectodea tuberculata increased the physically protected C pool through microaggregate restructuring and C enrichment.

Selection of focal earthworm species as non-target soil organisms for environmental risk assessment of genetically modified plants

By means of a literature survey, earthworm species of significant relevance for soil functions in different biogeographical regions of Europe (Atlantic, Boreal, Mediterranean) were identified. These focal earthworm species, defined here according to the EFSA Guidance Document on the environmental risk assessment (ERA) of genetically modified plants, are typical for arable soils under crop rotations with maize and/or potatoes within the three regions represented by Ireland, Sweden and Spain, respectively. Focal earthworm species were selected following a matrix of four steps: Identification of functional groups, categorization of non-target species, ranking species on ecological criteria, and final selection of focal species. They are recommended as appropriate non-target organisms to assess environmental risks of genetically modified (GM) crops; in this case maize and potatoes. In total, 44 literature sources on earthworms in arable cropping systems including maize or potato from Ireland, Sweden and Spain were collected, which present information on species diversity, individual density and specific relevance for soil functions. By means of condensed literature data, those species were identified which (i) play an important functional role in respective soil systems, (ii) are well adapted to the biogeographical regions, (iii) are expected to occur in high abundances under cultivation of maize or potato and (iv) fulfill the requirements for an ERA test system based on life-history traits. First, primary and secondary decomposers were identified as functional groups being exposed to the GM crops. In a second step, anecic and endogeic species were categorized as potential species. In step three, eight anecic and endogeic earthworm species belonging to the family Lumbricidae were ranked as relevant species: Aporrectodea caliginosa, Aporrectodea rosea, Aporrectodea longa, Allolobophora chlorotica, Lumbricus terrestris, Lumbricus friendi, Octodrilus complanatus and Octolasion cyaneum. Five out of these eight species are relevant for each biogeographical region with an overlap in the species. Finally, the earthworm species Ap. caliginosa (endogeic, secondary decomposer) and L. terrestris (anecic, primary decomposer) were selected as focal species. In the Mediterranean region L. terrestris may be substituted by the more relevant anecic species L. friendi. The selected focal species are recommended to be included in a standardized laboratory ERA test system based on life-history traits.

Different impacts of native and exotic earthworms on rhizodeposit carbon sequestration in a subtropical soil

Earthworms are known to regulate the sequestration of soil and leaf litter carbon (C). However, their impacts on the more accessible rhizospheric C, which represents a major energy source for soil food webs and an essential factor for C sequestration, are still unclear. Previous studies indicate that earthworms regulate the dynamics of SOC and leaf litter-C by increasing C accessibility to microbiota. However, in the case of labile rhizodeposit-C, microbiota might not require any pre-conditioning by earthworms and may rapidly metabolize most of this root-derived C. Consequently, potential pathways by which earthworms may affect the fate of rhizodeposit-C would be to regulate the biomass and/or activity of rhizosphere microbiota and, further, to mineralize/stabilize microbial products. A 13CO2 labelling experiment was performed to determine the impacts of four different earthworm species on the fate of tree rhizodeposit-C in a subtropical soil. We hypothesized that endogeic earthworm species, representing primarily geophagous species, would closely interact with soil microbiota and sequester the microbially metabolized rhizodeposit-C more efficiently than epigeic and anecic earthworm species. We found that irrespective of ecological group affiliation, the three native earthworms did not affect rhizodeposit-C sequestration. In contrast, the exotic endogeic species stimulated the immobilization of rhizodeposit-C in the biomass of root-associated bacteria and/or arbuscular mycorrhizal fungi and, further, accessed the microbiota-metabolized rhizodeposit-C more efficiently. As a consequence, the exotic endogeic earthworm species transiently tripled rhizodeposit-C retention in soil. We propose that the weak linkages between native earthworms and rhizodeposits-related microbiota limit earthworm impacts on rhizodeposit-C sequestration. However, the exotic endogeic species Pontoscolex corethrurus may potentially alter rhizodeposit-C dynamics in invaded areas by shifting rhizosphere microbial community composition. This work highlights a distinct mechanism by which earthworms can regulate C dynamics and indicates a significant contribution of invasive earthworm species to belowground processes.

Morphological and functional characterisation of the burrow systems of six earthworm species (Lumbricidae)

Earthworm burrow systems are generally described based on postulated behaviours associated with the three eco- logical types. In this study, we used X-ray tomography to obtain 3D information on the burrowing behaviour of six very common anecic (Aporrectodea nocturna and Lumbricus terrestris) and endogeic (Aporrectodea rosea, Allolobophora chlorotica, Aporrectodea caliginosa, Aporrectodea icterica) earthworm species, introduced into repacked soil cores for 6 weeks. A simple water infiltration test, the Beerkan method, was also used to assess some functional properties of these burrow systems. Endogeic worms make larger burrow sys- tems, which are more highly branched, less continuous and of smaller diameter, than those of anecic worms. Among the anecic species, L. terrestris burrow systems are shorter (9.2 vs 21.2 m) with a higher number (14.5 vs 23.5) of less branched burrows (12.2 vs 20.2 branches m �1 ), which are also wider (7.78 vs 5.16 mm) than those of A. nocturna .I n comparison, the burrow systems made by endogeic species appeared sim- ilar to each other. However, A. rosea burrows were short and narrow, whereas A. icterica had a longer burrow system (15.7 m), more intense bioturbation intensity (refilled macropores or soil lateral compaction around them) and thus a greater number of burrows. Regarding water infiltration, anecic burrow systems were far more efficient due to open burrows linking the top and bottom of the cores. For endogeic species, we observed a linear relationship between burrow length and the water infiltration rate (R 2 =0.49, p<0.01). Overall, the three main characteristics significantly influenc- ing water infiltration were burrow length, burrow number and bioturbation volume. This last characteristic highlighted the effect of burrow refilling by casts.

Burrowing and casting activities of three endogeic earthworm species affected by organic matter location

Abstract Earthworms are crucial for production and maintenance of soil structure and their activities can strongly impact soil functioning ( e.g. water regulation, nutrient dynamics). This laboratory study investigated the bioturbation activity of three endogeic species, Allolobophora chlorotica , Allolobophora icterica and Aporrectodea caliginosa , as affected by different locations of organic matter (OM) in the soil profile: OM scattered on the soil surface (surface-OM) or homogeneously mixed into the soil (mixed-OM). Microcosms, each containing a combination of one species (three individuals) and one OM location, were subjected to controlled environmental conditions (temperature, humidity and day/night cycle) for 60 days. At the end of the experiment, microcosms were cut into multiple horizontal cross-sections every centimetre and bioturbation activities were analyzed based on the number of burrows, the burrowed area and the percentage of burrowed area totally refilled with casts. Results showed that regardless of species, there was significantly fewer burrows and a greater percentage of burrowed area refilled with casts under mixed-OM than under surface-OM. A. chlorotica and A. caliginosa had a significantly greater burrowed area under mixed-OM than under surface-OM. Regardless of OM location, as depth increased, burrow number and area decreased for A. chlorotica and generally increased for A. icterica . In contrast, burrowing activity of A. caliginosa was affected by OM location as depth increased: under mixed-OM, burrow number decreased but burrowed area remained constant, whereas under surface-OM, burrow number remained constant and burrowed area increased. These results improve understanding of effects of endogeic species on soil structure and highlight effects of OM location on earthworm bioturbation. Especially this study gives information about the burrowing activity of A. icterica which has so far been little documented, and also informs about refilled burrows which is a major parameter for soil functioning.

Effects of endogeic earthworms on the soil organic matter dynamics and the soil structure in urban and alluvial soil materials

Earthworms are considered as key actors of soil processes at different spatial and temporal scales and provide essential ecosystem services linked to climate regulation or primary production. However, little is known about their basic functional roles (e.g. organic matter decomposition, soil structuring processes) in perturbed systems such as urban or alluvial soils. Alluvial soils are characterized by regular physical perturbation through flooding and associated erosion/sedimentation processes which are rather similar to perturbations (e.g. temporal instability, spatial heterogeneity) affecting urban soils. Due to their close soil characteristics, we hypothesized that in both cases, soil functioning is similar with respect to soil fauna activity. Under controlled conditions, our objective was to investigate the effects of two endogeic earthworm species, Allolobophora chlorotica (pink morph) and Aporrectodea rosea (the two most abundant species found in the studied urban site), on soil organic matter (SOM) dynamics and soil structure (network of earthworm burrows) comparing an urban and an alluvial soil. We investigated the growth of individuals (weight gain and reproduction success) and assessed their effects on SOM decomposition (cumulative C–CO2 emission, nitrogen and phosphorus mineralization) and soil structure (macroporosity, total length and connectivity of segments) after one and three months of incubation. Our results showed higher growth of A. rosea in the alluvial soil compared to the urban soil. However, the total length of burrows, carbon and nitrogen mineralization were often higher in the urban soil especially when the two species were combined. This trend can be mainly explained by lower organic matter content found in the urban soil which may influence positively the burrowing activity and negatively the growth of earthworms. Endogeic earthworms appear a key feature of the soil functioning in the urban context through their roles on organic matter transformation, the formation and maintenance of the soil structure.

Predicting soil micro-variables and the distribution of an endogeic earthworm species through a model based on large-scale variables

Studies on spatial patterns of distributions of soil dwelling animals have usually relied on soil micro-variables or statistical analyses based on presence/absence data. Geographic Information Systems (GIS) allow easy access to large-scale variables to build species distribution models. In this study, we used MaxEnt to model the distribution of the endogeic earthworm Hormogaster elisae. Significant differences were found between the predicted suitability values of localities where the species was present and those where it was absent, validating the predictive model. Most of the large-scale training variables showed significant correlation with soil micro-variables known to influence the biology of the species, proving the ability of the model to predict (to an extent) soil variables from environmental ones. The methodology could be extended to other soil fauna.