Indirect effects of earthworms on microbial assimilation of labile carbon

Interactions between earthworms and microorganisms can be important in regulating the rate of soil carbon turnover and maintaining soil fertility in agroecosystems. Despite the significance of earthworms in nutrient cycling in agroecosystems, the indirect influence of earthworms on C assimilation by microorganisms has not been adequately quantified. We assessed microbial assimilation of ¹³C-labeled acetate in earthworm (Lumbricus terrestris) middens and surrounding soil collected from maize agroecosystems. Incorporation of ¹³C into microbial lipids was used as an indicator of microbial growth rates. Earthworm middens had significantly lower concentrations of microbial phospholipid phosphates and lower natural abundance δ¹³C than the surrounding soil. After incubation with ¹³C-labeled acetate, microbial communities in earthworm middens had greater ¹³C/¹²C ratios of microbial lipids than microbial communities from surrounding soil. The ¹³C enrichment per unit of microbial phospholipid was much greater in middens than in surrounding soil indicating that: (i) microbial lipid synthesis was significantly higher in the earthworm middens; (ii) microbial assimilation efficiency for ¹³C-labeled acetate was greater in midden soil; or (iii) assimilation of ¹³C-labeled acetate relative to other C sources was proportionately greater in middens than in the surrounding soil. Our results suggest that there were functional differences between microbial communities in earthworm middens and surrounding soil, probably due to a combination of physical, chemical, and biological changes in the midden microenvironment. The resulting differences in microbial communities or activity increased microbial growth rates and assimilation of readily available C substrates in middens relative to surrounding soil.     

蚯蚓菌根互作对土壤酶活、 甘薯根系生长及养分吸收的影响

【目的】蚯蚓和丛枝菌根真菌处于不同的营养级,但在促进植物生长和提高土壤肥力等方面却都发挥着积极作用。单独对土壤微生物或土壤动物的研究较多,但对土壤微生物与土壤动物之间相互作用的研究很少。因此研究它们对土壤和植物生长的作用可为挖掘土壤生物的潜力和提高土壤生物肥力提供依据。【方法】采用盆栽试验,研究了蚯蚓(Eisenia fetida)与丛枝菌根真菌(Rhizophagus irregularis)互作对甘薯生长和养分吸收的影响。试验采用两因素完全随机试验设计,分为接种和不接种菌根真菌及添加和不添加蚯蚓。试验共4个处理: 不加菌根和蚯蚓(CK); 接种菌根真菌(AM); 添加蚯蚓(E); 添加蚯蚓和菌根真菌(E+AM),每个处理4次重复。调查了甘薯养分吸收、 根系形态及土壤养分变化,采用Canoco4.5软件对土壤生物与植物对应关系进行RDA (redundancy analysis)分析。【结果】接种菌根真菌显著提高了甘薯地上和地下部生物量(P0.05),而添加蚯蚓的处理仅提高了甘薯地上部生物量。同时添加蚯蚓和菌根的处理显著提高了甘薯地上地下部生物量,并且高于其他三个处理(P0.05)。与对照相比,接种菌根真菌显著提高了土壤磷酸酶活性(P0.01),增幅近一倍; 同时提高了土壤磷的植物有效性,土壤有效磷含量下降了30%左右。添加蚯蚓后土壤脲酶活性从5.45 mg NH+4-N/g显著增加到8.71 mg NH+4-N/g,土壤碱解氮的含量从5.82 mg/kg显著增加到6.89 mg/kg (P0.05)。RDA分析表明蚯蚓菌根互作对甘薯地上和地下部氮磷含量、 根表面积、 根体积、 根平均直径和根尖数均存在显著的正交互效应。蚯蚓菌根互作通过调控土壤酶和改变土壤养分有效性促进甘薯对土壤氮磷养分的吸收。【结论】蚯蚓(Eisenia fetida)通过调控土壤脲酶和碱性磷酸酶增加了土壤中氮磷的有效性从而促进甘薯地上部生长。丛枝菌根真菌(Rhizophagus irregularis)通过调控土壤磷酸酶和增加植株地上地下部吸磷量从而促进甘薯生长。添加蚯蚓或接种菌根真菌均能增加根系吸收面积和根体积从而促进甘薯对养分的吸收。蚯蚓和菌根真菌相互作用通过调控土壤酶和改变土壤养分有效性以及促进根系发育从而互补的促进甘薯养分吸收和生长。     

A critical review of current methods in earthworm ecology: From individuals to populations

Earthworms play an important role in the functioning of many terrestrial ecosystems, and while their importance is frequently acknowledged significant challenges still remain in determining their operant roles within the soil. This lack of knowledge becomes increasingly important as the spatial scale of analysis increases from individuals to populations within the landscape. To effectively develop understanding, research techniques must be able to determine the effects that earthworms have on the soil system, as well as to establish how many and which species are present. A range of techniques are required to facilitate meaningful analysis from the micro-scale within a soil profile (e.g. drilosphere effects) to a field scale or landscape scale. Furthermore, an additional framework of understanding is required to investigate the role of earthworms in the biogeochemical cycles.By critically evaluating recent advances in methods and data analysis techniques in three areas of earthworm research we highlight that combinations of common approaches often offer the most significant insights into the functional roles of earthworms within a soil system. Through particular reference to earthworm sampling and identification, biochemical functions and persistent pollutant ecotoxicology of temperate ecosystems we emphasise how a range of investigation methods can be a hindrance to developing a whole-system level understanding. The complex and diverse nature of soil systems means that a traditional compartmentalised approach studying single species using a single research technique is no longer sufficient to gain further insights into the earthworm contribution to ecosystem goods and services delivered at the whole landscape scale. The integration of technologically advanced methods in combination with systems based modelling will be critical to develop landscape scale understanding of the functions of earthworms as individuals and as populations within in their ecosystems.     

蚯蚓对土壤温室气体排放的影响及机制研究进展

土壤是温室气体的重要源和汇。蚯蚓是土壤物质循环的重要参与者,能够直接或间接影响土壤CO2、N2O和CH4等温室气体的产生和释放。蚯蚓呼吸产生的CO2,是土壤呼吸的重要组成部分;蚯蚓自身肠道、分泌液、消化物和排泄物等微环境促进反硝化过程释放N2O。蚯蚓还通过取食、掘穴、排泄等活动,改变土壤理化性质、微生物组成和活性及其他土壤动物的组成,影响地上植物生长,调节土壤分解、矿化、硝化、反硝化和甲烷生成及氧化等生态过程,间接影响土壤温室气体的排放。蚯蚓对土壤温室气体排放的影响逐渐受到重视,但目前研究仍以室内培养和单因子环境条件的模拟为主,缺少野外原位实验和多环境因子的交互实验研究。长期监测和同位素示踪技术,是深入探讨蚯蚓影响温室气体排放机制的重要手段。温室气体类型上,CO2和N2O是研究热点,CH4研究比较罕见。未来研究,应重视不同生态类群蚯蚓与土壤理化特征、微生物组成、其他类群土壤动物和地上植物间的交互作用,加强机制研究,并关注土壤污染环境下蚯蚓功能性状的变化;综合评价蚯蚓对土壤温室气体排放和土壤碳氮固定的影响,科学评估蚯蚓活动对土壤碳氮释放的促进或减缓作用。     

Molecular and morphological analyses of faeces to investigate the diet of earthworm predators: Example of a carnivorous land snail endemic to New Zealand

Ecosystem services provided by earthworms include increasing soil fertility, recycling organic material and provision of food for numerous predatory species. Estimating the role of earthworms in food webs is essential for a thorough evaluation of the ecosystem services they provide. Although their soft bodies are rapidly digested, earthworm remains can be detected via their chaetae in the faeces of predators.This study proposes a method for the identification of predated earthworm species using only predator faeces. We conducted morphological and molecular analyses of earthworm remains in the faeces of a highly endangered carnivorous land snail (Powelliphanta augusta) endemic to a restricted area of New Zealand.Microscopic examination of faecal strings from P. augusta showed the presence of earthworm chaetae in 47 of the 49 strings examined, suggesting an important role for earthworms in snail diets. Although earthworm tissue was not detectable in snail faeces, earthworm DNA was still present in sufficient quantity for molecular identification. Results showed that this land snail feeds on at least five species of New Zealand endemic earthworms.The method developed here is particularly appropriate for investigating the diet of potential invertebrate and vertebrate predators for which feeding behaviour is difficult to observe and gut content analysis is not possible. Such studies can help to develop a more complete understanding of the ecosystem services provided by earthworm communities. In this case it also helps the conservation of a rare and endangered predatory snail species.     

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.     

Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (N/N and C/C)

The soil animal food web has become a focus of recent ecological research but trophic relationships still remain enigmatic for many taxa. Analysis of stable isotope ratios of N and C provides a powerful tool for disentangling food web structure. In this study, animals, roots, soil and litter material from a temperate deciduous forest were analysed. The combined measurement of δ¹⁵N and δ¹³C provided insights into the compartmentalization of the soil animal food web. Leaf litter feeders were separated from animals relying mainly on recent belowground carbon resources and from animals feeding on older carbon. The trophic pathway of leaf litter-feeding species appears to be a dead end, presumably because leaf litter feeders (mainly diplopods and oribatid mites) are unavailable to predators due to large size and/or strong sclerotization. Endogeic earthworms that rely on older carbon also appear to exist in predator-free space. The data suggest that the largest trophic compartment constitutes of ectomycorrhizal feeders and their predators. Additionally, there is a smaller trophic compartment consisting of predators likely feeding on enchytraeids and potentially nematodes.     

Trophic transfer of fatty acids from gut microbiota to the earthworm Lumbricus terrestris L

The diet of earthworms includes soil organic matter, soil microbes and other microfauna, but the relative contribution of these dietary components to earthworm nutrition is not well known. Analysis of fatty acid (FA) profiles can reveal trophic relationships in soil food webs, leading to a better understanding of the energy and nutrient flows from microbiota to earthworms. The objective of this study was to determine the origin of FAs assimilated by the earthworm Lumbricus terrestris L. We analysed the pattern of FAs in: (i) the bulk soil, (ii) soil in the earthworm gut, (iii) the absorptive tissue of the earthworm gut wall, and (iv) the muscular layers of the earthworm body wall. Multivariate analyses performed on the FA profiles suggest that the microbial community in the earthworm gut differs from that in bulk soil. Diverse bacterial and fungal derived FAs, which earthworms cannot synthesize, were found in the earthworm gut wall and body wall, and in the neutral lipids (storage lipids) of the gut wall. The major compounds isolated were 20:4ω6, 20:5ω3 and 18:2ω6, followed by the monoenoic 18:1ω7 and 18:1ω9c, and the saturated 18:0. The microbial FA assemblage in the gut wall resembled the gut soil more than the bulk soil, and the body wall of L. terrestris showed the same microbial derived FA pattern as the gut wall, although at reduced concentrations. We propose the existence of a specific microbial community in the earthworm gut that provides FAs to the earthworm. It appears that L. terrestris may derive more of its energy and nutrients from gut specific microbiota than from microbiota already present in the ingested soil, based on the trophic relationships revealed through FA analysis.     

土食性大型土壤动物转化土壤有机碳的14C示踪法应用研究进展

土壤有机C是维持全球C平衡过程中的重要C库,其降解和转化在地球化学循环中占有重要地位。大型土壤动物对土壤有机C的稳定性起着重要的调控作用。14C示踪技术由于在测定目标化合物的转化速率和定位代谢产物和残留物分布上的优势,近年来在土壤有机C稳定性研究中得到了广泛应用。本文综述了3种典型土食性大型土壤动物,白蚁(Isoptera:Termitidae)、甲虫幼虫(Coleoptera:Scarabaeidae)和蚯蚓(Oligochaeta:Lumbricidae),对土壤稳态有机C降解转化的14C示踪研究结果及相关的微生物作用。食土白蚁和甲虫幼虫的极端碱性(pH10～12.5)肠道段和肠道内的特殊蛋白酶的共同作用促使这两种动物可以选择性地降解和矿化腐殖酸中的稳态多肽等组分,进一步提高腐殖酸的腐殖化程度。食土蚯蚓体内含有高活性的纤维素酶,能促进纤维素的降解。虽然木质素在蚓粪中能发生降解,蚯蚓也能降解植物树叶,但是食土蚯蚓能否降解或选择性降解稳态土壤有机C的研究还极少。大型土壤动物肠道内含有大量微生物及酶,这些微生物在土壤动物降解和腐殖化有机C的过程中所起的具体作用如何以及这些酶的来源还不是很清楚。文中总结了目前对大型土壤动物转化土壤有机C认识上的不足,并对一些优先研究方向提出了建议。     

木质素与蚯蚓对黑麦草生物量及土壤微生物群落的影响

采集农田土壤,设置添加木质素和蚯蚓不同组合处理的黑麦草盆栽试验,在测定植物生物量的基础上,结合定量PCR、高通量测序等方法,研究木质素和蚯蚓及其联合作用对土壤细菌、真菌群落的影响.结果显示:木质素显著降低了黑麦草的生物量,而蚯蚓能够缓解木质素的抑制作用,促进黑麦草生长.木质素明显抑制了土壤细菌、真菌数量,并改变群落结构...     

The action of an animal ecosystem engineer: Identification of the main mechanisms of earthworm impacts on soil microarthropods

Non-trophic interactions are shaping soil food web structure and functions. Particularly, the action of ecosystem engineers, such as earthworms, are likely to fundamentally impact the abiotic and biotic properties of their environment. The present study aimed to identify the main mechanisms through which earthworms belonging to varying ecological groups - epigeic, endogeic and anecic species - affect soil microarthropods by reviewing the literature on this topic and by performing meta-analyses.Earthworm ecological groups differed considerably in their impacts on microarthropods, whereas effects did not vary significantly between microarthropod taxa at the habitat scale. Inconsistent impacts of epigeic species on soil microarthropods are most likely due to differences in earthworm densities. Effects can thus be positive in the case of moderate densities or negative in the case of high densities and associated distinct changes in the physical structure of the upper soil organic layers. By contrast, impacts of endogeic earthworms appeared to be mainly negative and were primarily due to competition with microarthropods for food resources. Consequently, negative impacts on soil microarthropods intensified with increasing earthworm density and biomass. This interaction between endogeic earthworms and microarthropods is better referred to as amensalism due to the competitive predominance of earthworms. Impacts of anecic earthworm species differed significantly from that of endogeic ones; they were neutral at the habitat scale and positive on the microhabitat scale. Moreover, impacts were independent of earthworm densities due to the quasi-territorial behaviour of anecic earthworms. Positive effects were mainly attributed to the formation of stable microhabitats by anecic species; namely burrows/middens, rich in nutrients and microorganisms.The present study points to the relevance of the non-trophic biotic interactions that drive the composition of belowground food webs by identifying the most essential mechanisms underlying the impacts of animal ecosystem engineers on soil microarthropods. Moreover, as earthworms emerge as important biological invaders, the results of the present study may help to fully appreciate, estimate and model the consequences of this momentous global change phenomenon. Particularly, the spread of exotic epigeic and endogeic earthworm species likely threatens soil microarthropod density, diversity and functions.     

Can the invasive earthworm,Amynthas agrestis,be controlled with prescribed fire?

Biological invasions are one of the most significant global-scale problems caused by human activities. Earthworms function as ecosystem engineers in soil ecosystems because their feeding and burrowing activities fundamentally change the physical and biological characteristics of the soils they inhabit. As a result of this “engineering,” earthworm invasions can have significant effects on soil physical, chemical and biological properties. The species Amynthas agrestis (family Megascolecidae) was introduced to the United States from Asia, and has expanded its distribution range to include relatively undisturbed forests. Here, to clarify life history traits, we reared individuals under seven different conditions of food provision using litter, fragmented litter and soil, and also analyzed the stable isotope ratios of field-collected specimens to investigate their food resources in the field. Second, we examined whether prescribed fire can be used to manage invasive earthworms. We constructed eight experimental plots, each with 100 individuals of A. agrestis each, and burned half of the plots. The feeding experiment showed that the earthworms in units containing soil and some form of organic matter (litter and/or fragmented litter) produced many cocoons, indicating that litter and fragmented litter are important food resources for them. Stable isotope analyses also supported this result. During the experimental fires, average soil temperature at 5 cm depth increased by only 7.7 °C (average maximum of 32.2 °C). Litter mass was significantly reduced by the fires. Although numbers of A. agrestis and cocoons recovered from burned and unburned plots were not different, the viability of cocoons was significantly lower in burned plots. Fire may also reduce the survival rate of juveniles in the next year by depriving them of their preferred food resource. Most native earthworms in the United States live in the soil, while many invasive ones live in the litter layer and soil surface. Therefore, prescribed fire could be a viable tool for control of invasive earthworms without negatively impacting native earthworm populations.     

Decomposition and mineralization of energy crop residues governed by earthworms

Energy crops are increasingly cultivated in agricultural management systems world-wide. A substitution of food crops (e.g. cereals) by energy crops may generally alter the biological activity and litter decomposition in soil due to their varying structural and chemical composition and subsequently modify soil functioning. A soil microcosm experiment was performed to assess the decomposition and microbial mineralization of different energy crop residues in soil compared to a food crop, with or without earthworms. Residues of the energy crops winter rape (Brassica napus), maize (Zea mays), miscanthus (Miscanthus giganteus) and the food crop oat (Avena sativa) were each provided as food source for a mixed earthworm population, each consisting of one individual of Lumbricus terrestris, Aporrectodea caliginosa, and Octolasion tyrtaeum. After 6 weeks, the rate of litter loss from the soil surface, earthworm biomass, microbial biomass-C and -N, microbial activity, and enzyme activities were determined. The results emphasized, that litter loss and microbial parameters were predominantly promoted by earthworms and were additionally influenced by the varying structural and chemical composition of the different litter. Litter decay by earthworms was highest in N-rich maize litter treatment (C-N ratio 34.8) and lowest in the case of miscanthus litter (C-N ratio 134.4). As a consequence, the microbial biomass and basal respiration in soils with maize litter were higher, relative to other litter types. MBC-MBN ratio in soil increased when earthworms were present, indicating N competition between earthworms and microorganisms. Furthermore, enzyme activities responded in different ways on the varying types of litter and earthworm activity. Enzymes involved in the N-cycle decreased and those involved in the C-cycle tended to increase in the presence of earthworms, when litter with high C-N ratio was provided as a food source. Especially in the miscanthus treatments, less N might remain for enzymatic degradation, indicating that N competition between earthworms and microorganisms may vary between different litter types. Especially, an expansion of miscanthus in agricultural management systems might result in a reduced microbial activity and a higher N deficit for microorganisms in soil.     

Digestion and residue stabilization of bacterial and fungal cells,protein, peptidoglycan,and chitin by the geophagous earthworm Metaphire guillelmi

Microbial biomass is an important source of soil organic matter, which plays crucial roles in the maintenance of soil fertility and food security. However, the mineralization and transformation of microbial biomass by the dominant soil macrofauna earthworms are still unclear. We performed feeding trials with the geophagous earthworm Metaphire guillelmi using ¹⁴C-labelled bacteria (Escherichia coli and Bacillus megaterium) cells, fungal (Penicillium chrysogenum) cells, protein, peptidoglycan, and chitin. The mineralization rate of the microbial cells and cell components was significantly 1.2–4.0-fold higher in soil with the presence of M. guillelmi for seven days than in earthworm-free soil and 1–11-fold higher than in fresh earthworm cast material. When the earthworms were removed from the soil, the mineralization of the residual carbon of the microbial biomass was significantly lower than that in the earthworm-free soil, indicating that M. guillelmi affects the mineralization of the biomass in soil in two aspects: first stimulation and then reduction, which were attributed to the passage of the microbial biomass through the earthworm gut, and that the microorganisms in the cast could play only minor roles in the stimulated mineralization and residual stabilization of microbial biomass. Large amounts (8–29%) of radiolabel of the tested microbial biomass were assimilated in the earthworm tissue. Accumulation of fungal cells (11%) and cell wall component chitin (29%) in the tissue was significantly higher than that of bacterial cells (8%) and cell wall component peptidoglycan (15%). Feeding trails with ¹⁴C-lablled microbial cells and cell components provided direct evidence that microbial biomass is a food source for geophagous earthworm and fungal biomass is likely a more important food source for earthworms than bacterial biomass. Findings of this study have important implications for the roles of geophagous earthworms in the fate of microbial biomass in soil.     

Competition between invasive earthworms (Amynthas corticis, Megascolecidae) and native North American millipedes (Pseudopolydesmus erasus, Polydesmidae): Effects on carbon cycling and soil structure

Invasive earthworms can have significant impacts on C dynamics through their feeding, burrowing, and casting activities, including the protection of C in microaggregates and alteration of soil respiration. European earthworm invasion is known to affect soil micro- and mesofauna, but little is known about impacts of invasive earthworms on other soil macrofauna. Asian earthworms (Amynthas spp.) are increasingly being reported in the southern Appalachian Mountains in southeastern North America. This region is home to a diverse assemblage of native millipedes, many of which share niches with earthworm species. This situation indicates potential for earthworm-millipede competition in areas subject to Amynthas invasion.In a laboratory microcosm experiment, we used two ¹³C enriched food sources (red oak, Quercus rubra, and eastern hemlock, Tsuga canadensis) to assess food preferences of millipedes (Pseudopolydesmus erasus), to determine the effects of millipedes and earthworms (Amynthas corticis) on soil structure, and to ascertain the nature and extent of the interactions between earthworms and millipedes. Millipedes consumed both litter species and preferred red oak litter over eastern hemlock litter. Mortality and growth of millipedes were not affected by earthworm presence during the course of the experiment, but millipedes assimilated much less litter-derived C when earthworms were present.Fauna and litter treatments had significant effects on soil respiration. Millipedes alone reduced CO₂ efflux from microcosms relative to no fauna controls, whereas earthworms alone and together with millipedes increased respiration, relative to the no fauna treatment. CO₂ derived from fresh litter was repressed by the presence of macrofauna. The presence of red oak litter increased CO₂ efflux considerably, compared to hemlock litter treatments.Millipedes, earthworms, and both together reduced particulate organic matter. Additionally, earthworms created significant shifts in soil aggregates from the 2000-250 and 250-53 μm fractions to the >2000 μm size class. Earthworm-induced soil aggregation was lessened in the 0-2 cm layer in the presence of millipedes. Earthworms translocated litter-derived C to soil throughout the microcosm.Our results suggest that invasion of ecosystems by A. corticis in the southern Appalachian Mountains is unlikely to be limited by litter species and these earthworms are likely to compete directly for food resources with native millipedes. Widespread invasion could cause a net loss of C due to increased respiration rates, but this may be offset by C protected in water-stable soil aggregates.     

Dual stable isotope analysis (δC and δN) of soil invertebrates and their food sources

More research is required to validate and refine natural abundance stable isotope ratio techniques as a tool for the investigation of the feeding ecology of soil animals and trophic relations in soil food webs. Isotope ratios of C (δ¹³C) and N (δ¹⁵N) were measured in herbivorous and detritivorous invertebrate groups, namely lumbricid earthworms (7 species), enchytraeid worms (3 species), slugs (3 taxa), and their potential food sources in an arable system. Intrapopulation δ¹⁵N variation in the slug Deroceras reticulatum (n=52) was large (range 4.2‰), possibly reflecting spatial variability in the food sources. Significant correlations between C:N ratios and isotope ratios in earthworms suggest that factors other than feeding may influence isotopic patterns. One enchytraeid species, Enchytraeus buchholzi, was enriched in ¹³C and strongly depleted in ¹⁵N compared to all other groups. Invertebrates formed a continuum when considered in relation to C and N separately, but fell into two distinct groups on the basis of combined C and N isotope ratios. The less enriched group represents herbivorous and litter-feeding species, while the more enriched group represents soil feeders. It is concluded that δ¹³C measurements could provide a means of assigning separate baseline δ¹⁵N values to primary and secondary decomposers, which in turn could improve the inference of higher trophic levels, omnivory and intraguild predation.     

Changes in the fatty acid profiles through the digestive tract of the earthworm Lumbricus terrestris L.

The gut of many soil arthropods contains a complex and mutualistic microbial community that usually assists the host with digestion. The same is probably true for earthworms, but the nature and function of the microbiota inhabiting their gut are virtually unknown. In this paper, we studied the microbial community in the gut content of the earthworm Lumbricus terrestris L. and in the bulk soil by assessing their fatty acid (FA) profiles. Our results indicated that the total FA concentration in the earthworm gut was about two orders of magnitude greater than in bulk soil, with higher concentration of bacteria (up to 500-fold), fungal and metazoan-derived FAs. Several FAs appearing in the gut were not present in bulk soil. PCA analysis revealed that the microbial community in the gut was different from that in the bulk soil, and that significant changes occurred between midgut, hindgut and proctodeum. Cluster analysis of bacterial and fungal-derived FA profiles grouped the bulk soil samples apart from the gut samples, where the hindgut profiles were more closely related to those from the proctodeum than those from the midgut. We showed important changes in the FA concentration and composition occurring at very small spatial scales inside the gut of the earthworm L. terrestris. These results have implications for understanding earthworm digestion, and they suggest that the microbial community in the earthworm gut is not a casual combination of microorganisms already present in the soil. Further study is needed to determine how these gut microbial communities are involved in earthworm digestion processes.     

Livestock grazing activities and wild boar rooting affect alpine earthworm communities in the Central Pyrenees (Spain)

In alpine areas, shifts in traditional grazing activities are globally affecting ecosystem properties and rural livelihoods. The ongoing decrease in extensive husbandry, with a decline in sheep numbers and a relative increase in cattle stocking rates, has resulted in the abandonment of large alpine grazing areas. This pastoral change has been recently associated with increased disturbances of wild boar (Sus scrofa), mainly within cattle-stocked ranges. In turn, cattle areas favor earthworm communities, a preferred trophic resource for wild boars in mountain environments. However, it is unknown whether wild boar disturbances, together with grazing activities, can affect earthworm communities. Our aim is to analyze the abundance, richness and ecological categories of earthworms and soil parameters (soil C and N concentrations, moisture, and C:N ratio) in relation to the occurrence of wild boar disturbances and grazing activities at different stocking pressures. We sampled two different grazing scenarios differing in the distribution of cattle along a grazing gradient, which was represented by three levels of stocking pressure (high, intermediate and low). Our results showed a complex effect of grazing activities and disturbances on the abundance and richness of earthworms, along with variations in C:N ratio and soil moisture, especially with increasing cattle presence. At high-stocking pressures differences in earthworm abundance and richness between disturbed and undisturbed areas were limited, whereas at intermediate-stocking pressures earthworms were favored by wild boar disturbances. Ecological categories of earthworms responded differently; endogeic species were the most affected by grazing pressures and wild boar rooting, with highest occurrence at high-stocking pressures and within boar disturbed areas. In sum, pastoral use and soil disturbances affected earthworm community structure and composition in complex ways. These results indicate an interaction of processes that is relevant to understand current changes in alpine ecosystems.     

The effect of feeding behavior on Hg accumulation in the ecophysiologically different earthworms Lumbricus terrestris and Octolaseon cyaneum: A microcosm experiment

 A soil microcosm experiment was performed to assess the uptake of Hg from various Hg-spiked food sources (soil, leaf litter and root litter of Trifolium alexandrinum) by two earthworm species, Lumbricus terrestris (anecic) and Octolaseon cyaneum (endogeic). Treatments were applied in which one of the three food sources was Hg spiked and the other two were not. Additional treatments in which all or none of the food sources were Hg spiked were used as controls. Uptake of Hg from soil into tissues of both earthworm species was significantly higher than uptake of Hg from leaf litter or root litter, indicating that soil may be the most important pool for the uptake of Hg into earthworms. In addition, the anecic L. terrestris significantly accumulated Hg from all Hg-spiked food sources (leaf litter, root litter and soil), whereas the endogeic O. cyaneum took up Hg mainly from soil particles. Interestingly, there was no further increase in Hg in L. terrestris when all food sources were Hg spiked compared to the single Hg-spiked sources. This may be attributed to the relatively high Hg content in the soil, which may have influenced the feeding behavior of the earthworms, although their biomass did not significantly decline. We suggest that, in addition to the physiological differences, feeding behavior may also play a role in the contrasting uptake of Hg by the two earthworm species.     

Earthworm activities and the soil system

Summary Earthworms find in soil the energy, nutrient resources, water and buffered climatic conditions that they need. According to the food resource they exploit and the general environmental conditions, earthworms can be grouped into different functional categories which differ essentially in morphology, size, pigmentation, distribution in the soil profile, ability to dig galleries and produce surface casts, demographic profiles and relationships with the soil microflora. Soil characteristics are both the determinant and the consequence of earthworm activities, since these animals greatly influence the functioning of the soil system. When present, they build and maintain the soil structure and take an active part in energy and nutrient cycling through the selective activation of both mineralization and humification processes. By their physical activities and resultant chemical effects, earthworms promote short and rapid cycles of nutrients and assimilable carbohydrates. Thus earthworms represent a key component in the biological strategies of nutrient cycling in soils and the structure of their communities gives a clear indication of the type of soil system that they inhabit.