STUDIES ON THE RELATIONSHIPS BETWEEN EARTHWORMS AND SOIL FERTILITY: I. BIOLOGICAL STUDIES IN THE FIELD

Changes in the seasonal activity of several species of earthworms have been followed in a permanent pasture field for 18 months, 1945–6. The two soil conditions which chiefly determine activity are temperature and moisture. Other factors are the occurrence of an obligatory diapause in the two species Allolobophora nocturna and A. longa , and changes in population in A. chlorotica and Lumbricus terrestris.
Soil temperature and soil moisture also determined the weight of soil thrown up in the form of wormcasts during autumn, winter and spring. It is suggested that only two species, A. nocturna and A. longa , are responsible for wormcasts and that the other four common species present play little or no part in this activity.
At Rothamsted it was found that the previous agricultural history of the field is an important factor in determining the fauna. Old permanent pasture is characterized by a high percentage of A. nocturna and a rather lower percentage of A. caliginosa. Ploughing old permanent pasture and reseeding to grass after 1 or 2 years arable reduces the proportions of A. nocturna and A. caliginosa and increases that of Eisenia rosea. Arable fields have A. chlorotica as the dominant species and pasture fields 2–7 years grass after many years of arable fanning still show a high percentage of A. chlorotica and a low proportion of A. nocturna.
A survey of the Carse of Stirling, Scotland, showed that soil type is also an important factor in determining the earthworm fauna. A. caliginosa was the dominant species on the three soil types studied, but the subdominant species varied. On clay soil, A. longa was subdominant; on loam, A. longa and L. rubellus ; on sandy soil, A. longa, L. rubellus and A. chlorotica. The dominant species of pasture land at Rothamsted, A. nocturna , was not found at Stirling.     

蚯蚓在我国南方土壤修复中的应用

蚯蚓作为生物量最大的土壤动物, 对土壤生态系统和环境质量影响深远。本研究介绍了华南地区主要应用的皮质远盲蚓(Amynthas corticis)、毛利远盲蚓(A. morrisi)、壮伟远盲蚓(A. robustus)、参状远盲蚓(A. aspergillum)、南美岸蚓(Pontoscolex corethrurus)和赤子爱胜蚓(Eisenia fetida)的生态特征, 阐述了它们与土壤pH值、酶活性、金属富集和有效性改变、孔道和微团聚体形成之间的紧密关系: (1)蚯蚓生存的土壤酸碱性范围较广(pH为3.8-7.9), 其存活率与土壤类型、有机质含量和成分、土壤污染程度和蚯蚓种类相关; (2)肠道内、蚓粪和蚓触圈的酶活性分别表征了蚯蚓取食喜好、土壤养分循环及微生物种群特征; (3)蚯蚓能够富集不同种类的金属并改变其有效性, 这些变化具有蚓种间、金属种类间和土壤类型之间的差异; (4)蚯蚓活动及其生产的蚓粪能改变土体结构、产生孔道、影响土壤团聚体数量、大小和分布。蚯蚓的上述作用使其在解决中国南方红壤酸化、土壤金属污染、茶园土壤养分不平衡、高速公路建设临时用地土壤损毁等方面具有广阔的应用前景。目前, 由于华南远盲蚓的生理特征差异研究较少, 远盲蚓繁育技术的缺乏一定程度上限制了这些蚯蚓在中型和大型尺度下应用技术的研究和推广。有必要进一步挖掘蚯蚓在土壤修复中的潜力, 进行蚯蚓主导的相关技术研发, 深入探讨其影响机制。     

NMR-based metabolomics using earthworms as potential indicators for soil health

Soil health is key for sustainable productivity and adaptation to climate change. Agricultural practice can significantly impact on soil health. The aim of this study was to examine the effect of two land management regimes on organisms (earthworms) that may be used as indicators for soil health via NMR metabolomics. Earthworms are important in the soil decomposition process and viewed as a sentinel species in soil. The presence/absence of earthworm species and their relative abundances provide a gross indication of the health of the soil and it is expected that land use would affect earthworm metabolism as the populations rose or declined in response to changing soil health parameters. In order to test this hypothesis metabolomics approaches were employed to determine if biological indicators of soil change can be detected. Two species of earthworms, an unidentified native species and the European species Aporrectodea caliginosa, were collected from properties in Victoria, Australia where the land was treated with either biological (organic) or conventional (chemical) treatment regimes. Both lipid and aqueous NMR metabolomics for earthworms was employed, demonstrating that class classifications can be achieved with both datasets and provide orthogonal, complementary, chemical information. The study indicates that land-use has a measurable effect on the biochemistry of worm populations. Potential biomarkers of land use and worm stress were found, including elevated levels of glucose, maltose, alanine and triacylglycerides. This study demonstrates the utility of NMR metabolomics approaches in detecting biomarkers related to land treatment regimes and potentially soil health attributes. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

两种代表性蚯蚓对设施菜地土壤微生物群落结构及理化性质的影响

不同生态型蚯蚓的取食偏好和生境有所差异,因此蚯蚓的生态型差异可能关乎其对土壤性质的不同影响;有关不同生态型蚯蚓对土壤性质尤其是微生物学性质影响的研究有助于了解蚯蚓生态功能的作用机制。在野外调控试验的第4年采集土壤,研究了牛粪混施和表施处理下内层种威廉腔环蚓(Metaphire guillelmi)和表层种赤子爱胜蚓(Eisenia foetida)对设施菜地土壤微生物群落结构和主要理化性质的影响。结果表明,土壤微生物群落结构同时受到蚯蚓种类和牛粪施用方式的影响。牛粪表施时,两种蚯蚓均显著降低了菌根真菌、真菌生物量和原生动物生物量(P0.05);牛粪混施时,不同蚯蚓的影响有所差异,威廉腔环蚓明显增加了菌根真菌、真菌生物量和放线菌生物量,而赤子爱胜蚓的作用不明显。此外,两种蚯蚓均提高了土壤孔隙度、团聚体稳定性和土壤p H、矿质氮以及微生物生物量碳氮水平,但提高幅度取决于蚯蚓种类和牛粪施用方式。冗余分析表明蚯蚓影响下土壤微生物群落结构的变化与团聚体稳定性、p H、速效磷、矿质氮呈正相关,而与土壤容重呈负相关。     

Studies on Artioposthia triangulata (Dendy) (Tricladida: Terricola), a predator of earthworms

Observations had linked the disappearance of earthworms from a grass field to the presence of Artioposthia triangulata. An experiment demonstrated that this land planarian could severely and quickly reduce numbers of four earthworm species. Two different approaches to sampling A. triangulata were investigated on a grassland site. The first used four different trap types (wood, ceramic tile, 'corriboard' plastic and 5 mm polystyrene beneath a ceramic tile) measuring 15 cm x 15 cm which were compared over a period of 18 wk. The second used one, or two, applications of dilute formalin solution to quadrats followed by counting the residual planarians by hand-sorting the soil beneath the quadrat to a depth of 30 cm. The polystyrene traps were the most effective for detecting the presence of A. triangulata. No planarians were ever found by hand-sorting after two formalin applications and it was concluded that formalin sampling provided a good estimate of the population density. Counts under traps were not related to absolute estimates of population densities so polystyrene type traps should only be used for detection of the planarians. A multiple regression relationship of A. triangulata weight over time in 5% formalin is presented and allows the original liveweight to be calculated from the weight in preservative. Planarian and earthworm population densities in eight fields were sampled and the planarians were found to be randomly distributed. Counts of planarians in 0.25 m² quadrats were not related to numbers of earthworms but overall field population densities were. It is concluded that A. triangulata is a severe threat to the earthworm populations of Northern Ireland.     

Effects of high copper concentrations on soil invertebrates (earthworms and oribatid mites):

Data in the literature on the toxicity and uptake of copper by soil invertebrates are contradictory. Copper toxicity and bioaccumulation studies were therefore performed using earthworms and oribatid mites. Field-simulating experiments in soil-filled plastic containers showed that earthworms try to escape moderately toxic situations and that they are much more sensitive than oribatid mites to temporary high Cu²⁺ concentrations in soils. The total copper concentration in the bodies of the earthworm species Octolasium cyaneum was measured in experiments with different soil types and different amounts of added CuSO₄. The copper concentrations in the earthworms increased in response to the higher concentrations of the copper fraction extractable with 2.5% acetic acid in the soil. Furthermore, internal copper concentrations showed a slight tendency to oscillate. The worms died when the concentrations within their bodies exceeded about 100–120 ppm, calculated on a dry weight basis. To interpret the experimental results, a compartment model is proposed which describes the dynamics of different fractions of copper in worms living in varying soil environments. Applying this model, the different reports on toxicity and uptake of copper in the literature no longer contradict each other.     

Nutrient availability and maize growth in a soil amended with earthworm casts from a South African indigenous species

The study was undertaken to assess the availability to maize of nutrients from earthworm casts (wormcasts) collected from a grazing paddock in the Eastern Cape province of South Africa. Maize (cv PAN 473) was grown in pots filled with ground wormcasts, non-casted surrounding soil and a mixture of the two media. Fertiliser application increased growth and uptake of nutrients by maize grown on both wormcast and non-casted soil. Maize grown on wormcasts had significantly (p < 0.05) higher plant height, stem diameter, dry weight and showed higher nutrient uptake and lower fertiliser response than that grown on corresponding non-casted surface soil. The uptakes of plant nutrients, growth and dry matter yields were in the order fertiliser>wormcasts>non-casted soil. Mixing worm casts with non-casted soil improved maize growth and nutrient uptake over non-casted soil. It is concluded that wormcasts could be used as a soil amendment for crop production, especially in small-scale production systems.     

The soil fauna as a food source for moles

Moles feed mainly on insects and earthworms and may eat 18 to 36 k (40 to 80 lb) per annum, collected in an area of about 1/25 hectare (1/10 acre). This largely restricts them to deciduous woodland and old grassland on "mull" soils since field populations of soilinsects cannot provide them with enough food but earthworm populations can. Slugs and millipedes may be relatively unpalatable.
Caches of earthworms stored by moles consist almost entirely of Lumbricus terrestris immobilized by removal or multilation of the anterior 3–5 segments. It is still uncertainhow and when the caches are made. Earthworm cocoons are prominent in the diet of moles in pastures but how they are located is not yet known.     

Invasion of exotic earthworms into ecosystems inhabited by native earthworms

The most conspicuous biological invasions in terrestrial ecosystems have been by exotic plants, insects and vertebrates. Invasions by exotic earthworms, although not as well studied, may be increasing with global commerce in agriculture, waste management and bioremediation. A number of cases has documented where invasive earthworms have caused significant changes in soil profiles, nutrient and organic matter dynamics, other soil organisms or plant communities. Most of these cases are in areas that have been disturbed (e.g., agricultural systems) or were previously devoid of earthworms (e.g., north of Pleistocene glacial margins). It is not clear that such effects are common in ecosystems inhabited by native earthworms, especially where soils are undisturbed. We explore the idea that indigenous earthworm fauna and/or characteristics of their native habitats may resist invasion by exotic earthworms and thereby reduce the impact of exotic species on soil processes. We review data and case studies from temperate and tropical regions to test this idea. Specifically, we address the following questions: Is disturbance a prerequisite to invasion by exotic earthworms? What are the mechanisms by which exotic earthworms may succeed or fail to invade habitats occupied by native earthworms? Potential mechanisms could include (1) intensity of propagule pressure (how frequently and at what densities have exotic species been introduced and has there been adequate time for proliferation?); (2) degree of habitat matching (once introduced, are exotic species faced with unsuitable habitat conditions, unavailable resources, or unsuited feeding strategies?); and (3) degree of biotic resistance (after introduction into an otherwise suitable habitat, are exotic species exposed to biological barriers such as predation or parasitism, “unfamiliar” microflora, or competition by resident native species?). Once established, do exotic species co-exist with native species, or are the natives eventually excluded? Do exotic species impact soil processes differently in the presence or absence of native species? We conclude that (1) exotic earthworms do invade ecosystems inhabited by indigenous earthworms, even in the absence of obvious disturbance; (2) competitive exclusion of native earthworms by exotic earthworms is not easily demonstrated and, in fact, co-existence of native and exotic species appears to be common, even if transient; and (3) resistance to exotic earthworm invasions, if it occurs, may be more a function of physical and chemical characteristics of a habitat than of biological interactions between native and exotic earthworms.     

Interactions of earthworms with Atrazine-degrading bacteria in an agricultural soil

In the last 10 years, accelerated mineralization of Atrazine (2-chloro-ethylamino-6-isopropylamino-s-triazine) has been evidenced in agricultural soils repeatedly treated with this herbicide. Here, we report on the interaction between earthworms, considered as soil engineers, and the Atrazine-degrading community. The impact of earthworm macrofauna on Atrazine mineralization was assessed in representative soil microsites of earthworm activities (gut contents, casts, burrow linings). Soil with or without earthworms, namely the anecic species Lumbricus terrestris and the endogenic species Aporrectodea caliginosa, was either inoculated or not inoculated with Pseudomonas sp. ADP, an Atrazine-degrading strain, and was either treated or not treated with Atrazine. The structure of the bacterial community, the Atrazine-degrading activity and the abundance of atzA, B and C sequences in soil microsites were investigated. Atrazine mineralization was found to be reduced in representative soil microsites of earthworm activities. Earthworms significantly affected the structure of soil bacterial communities. They also reduced the size of the inoculated population of Pseudomonas sp. ADP, thereby contributing to the diminution of the Atrazine-degrading genetic potential in representative soil microsites of earthworm activities. This study illustrates the regulation produced by the earthworms on functional bacterial communities involved in the fate of organic pollutants in soils.     

Earthworm invasions of ecosystems devoid of earthworms: effects on soil microbes

Recent studies document North American earthworm invasions and their profound effects on the structure of the soil profile, which is the habitat for soil microorganisms (mainly fungi and bacteria). Dramatic alterations made to these layers during earthworm invasion significantly change microbial community structure and therefore microbial activities such as C transformations. Understanding the impacts of earthworm invasion on the microbes themselves will give insight into earthworm effects on microbial activities. Bacterial and actinomycete communities in earthworm guts and casts have not been studied in environments recently invaded by earthworms. Earthworm invasion tended to decrease fungal species density and fungal species diversity and richness. The presence of earthworms decreased zygomycete species abundance probably due to disruption of fungal hyphae. Physical disruption of hyphae may also explain decreased mycorrhizal colonization rates, decreased mycorrhizal abundance and altered mycorrhizal morphology in the presence of earthworms. Mixing of organic layers into mineral soil during earthworm invasion tended to decrease microbial biomass in forest floor materials while increasing it in mineral soil. In newly invaded forest soils, microbial respiration and the metabolic quotient tended to decline. In forests where either the microbial community has had time to adapt to earthworm activities, or where the destruction of the forest floor is complete, as in invasions by the Asian Amynthas hawayanus, the presence of earthworms tends to increase the metabolic quotient indicating a shift to a smaller, more active microbial community.     

Independent effects of arbuscular mycorrhiza and earthworms on plant diversity and newcomer plant establishment

Questions: How do arbuscular mycorrhiza and earthworms affect the structure and diversity of a ruderal plant community? Is the establishment success of newcomer plants enhanced by these soil organisms and their interactions? Methods: We grew a native ruderal plant community composed of different functional groups (grasses, legumes and forbs) in the presence and absence of arbuscular mycorrhizal fungi (AMF) and endogeic earthworms in mesocosms. We introduced seeds of five, mainly exotic, plant species from the same functional groups after a disturbance simulating mowing. The effects of the soil organisms on the native ruderal plant community and seedling establishment of the newcomer plants were assessed. Results: After disturbance, the total above‐ground regrowth of the native plant community was not affected by the soil organisms. However, AMF increased plant diversity and shoot biomass of forbs, but decreased shoot biomass of grasses of the native plant community. Earthworms led to a reduction in total root biomass. Establishment of the introduced newcomer plants increased in the presence of AMF and earthworms. Especially, seedling establishment of the introduced non‐native legume Lupinus polyphyllus and the native forb Plantago lanceolata was promoted in the presence of AMF and earthworms, respectively. The endogeic earthworms gained more weight in the presence of AMF and led to increased extraradical AMF hyphal length in soil. However, earthworms did not seem to modify the effect of AMF on the plant community. Conclusion: The present study shows the importance of mutualistic soil organisms in mediating the establishment success of newcomer plants in a native plant community. Mutualistic soil organisms lead to changes in the structure and diversity of the native plant community and might promote newcomer plants, including exotic species.     

Role of diurnal rhythm of oxygen consumption in emergence from soil at night after heavy rain by earthworms

Abstract. Two species of earthworms were used to unravel why some earthworm species crawl out of the soil at night after heavy rain. Specimens of Amynthas gracilis , which show this behavior, were found to have poor tolerance to water immersion and a diurnal rhythm of oxygen consumption, using more oxygen at night than during the day. The other species, Pontoscolex corethrurus , survived longer under water and was never observed to crawl out of the soil after heavy rain; its oxygen consumption was not only lower than that of A. gracilis but also lacked a diurnal rhythm. Accordingly, we suggest that earthworms have at least two types of physical strategies to deal with water immersion and attendant oxygen depletion of the soil. The first is represented by A. gracilis ; they crawl out of the waterlogged soil, especially at night when their oxygen consumption increases. The other strategy, shown by P. corethrurus , allows the earthworms to survive at a lower concentration of oxygen due to lower consumption; these worms can therefore remain longer in oxygen-poor conditions, and never crawl out of the soil after heavy rain.     

The diversity of earthworms in 200 Scottish fields and the possible effect of New Zealand land flatworms (Arthurdendyus triangulatus) on earthworm populations

Earthworm populations from 200 fields (132 pasture and 68 arable) in Scotland are compared. Earthworms populations from two pasture fields at a Scottish farm infested with the New Zealand terrestrial planarian, Arthurdendyus triangulates (a predator of earthworms), are compared with a subset of these 200 fields (none of which had planarians at the time of the survey). A variety of univariate and multivariate methods are used for comparison. Results from the 200 fields show that the number of individuals, number of species, richness and diversity decline eastwards and northwards across Scotland. There is an overall difference between pasture and arable fields at the same farm, with fewer anecic earthworms (Aporrectodea longa and Lumbricus terrestris), but more Aporrectodea rosea, in arable fields. Conversely, species richness and cumulative species diversity is greater in arable fields, and sample similarity is less. The planarian‐infested fields show differences from the subset of western Scottish pasture fields and from each other. Both have fewer Aporrectodea caliginosa (and endogeic total) and A. longa (and anecic total) than the western pasture fields. One field has fewer L. terrestris and fewer earthworms in total. Univariate factors show no significant differences between the infested fields and similar non‐infested fields, but multivariate analysis suggests differences. Waterlogging and recent growth of rushes in the infested fields are discussed in relation to the reduced population of earthworms and to rainfall.     

Freeze tolerance in Aporrectodea caliginosa and other earthworms from Finland

Earthworms that live in subarctic and cold temperate areas must deal with frost even though winter temperatures in the soil are often more moderate than air temperatures. Most lumbricid earthworms can survive temperatures down to the melting point of their body fluids but only few species are freeze tolerant, i.e. tolerate internal ice formation. In the present study, earthworms from Finland were tested for freeze tolerance, and the glycogen reserves and glucose mobilization (as a cryoprotectant) was investigated. Freeze tolerance was observed in Aporrectodea caliginosa, Dendrobaena octaedra, and Dendrodrilus rubidus, but not in Lumbricus rubellus. A. caliginosa tolerated freezing at -5 degrees C with about 40% survival. Some individuals of D. octaedra tolerated freezing even at -20 degrees C. Glycogen storage was largest in D. octaedra where up to 13% of dry weight consisted of this carbohydrate, whereas the other species had only 3-4% glycogen of tissue dry weight. Also glucose accumulation was largest in D. octaedra which was the most freeze-tolerant species, but occurred in all four species upon freezing. It is discussed that freeze tolerance may be a more common phenomenon in earthworms than previously thought.     

Resident plant diversity and introduced earthworms have contrasting effects on the success of invasive plants

Theoretical predictions and empirical studies suggest that resident species diversity is an important driver of community invasibility. Through trait-based processes, plants in communities with high resident species diversity occupy a wider range of ecological niches and are more productive than low diversity communities, potentially reducing the opportunities for invasion through niche preemption. In terrestrial plant communities, biotic ecosystem engineers such as earthworms can also affect invasibility by reducing leaf litter stocks and influencing soil conditions. In a greenhouse experiment, we simultaneously manipulated resident species diversity and earthworm presence to investigate independent and interactive effects of these two variables on the success of several invasive plants. Higher diversity of resident species was associated with lower biomass of invasives, with the effect mediated through resident species biomass. The presence of earthworms had a strong positive effect on the biomass of invasive species across all levels of resident species diversity and a weaker indirect negative effect via decreased soil moisture. Earthworms also weakened the positive correlation between resident species diversity and productivity. We did not observe any interactive effects of resident species biomass and earthworms on invasive species success. Partitioning the net biodiversity effect indicated that selection effects increased with resident species diversity whereas complementarity effects did not. Results suggest that managing for diverse forest communities may decrease the susceptibility of these communities to invasions. However, the presence of introduced earthworms in previously earthworm-free sites may undermine these efforts. Furthermore, future studies of plant community invasibility should account for the effects of introduced earthworms.     

Non-native earthworms alter the assembly of a meadow plant community

Non-native earthworms can alter ecosystems by modifying soil structure, depredating seeds and seedlings, and consuming soil organic matter, yet the initial responses of plant communities to earthworm invasions remain poorly understood. We assessed the effect of non-native earthworms on seedling survival during germination and after establishment using six native and six non-native plant species grown from seed in single- and multi-species experimental mesocosms. We examined the extent to which earthworms (1) influenced seedling survival, (2) selectively depredated native versus non-native plants, (3) impacted establishment based on seed size and/or root morphology, and (4) shaped community assembly. The effect of earthworms on seedling survival varied temporally and among species but inconsistently with respect to species origin. Differences in seed/seedling survival translated to changes in community assembly. Earthworms tended to reduce species abundance, richness, evenness, and diversity in multi-species mesocosms and led to the divergence of communities by treatment. In general, species with large seeds and fibrous roots dominated communities with earthworms present, whereas species with small seeds and taproots only persisted in multi-species mesocosms without earthworms. Our findings suggest that earthworms act as ecological filters in the early stages of invasion to shape community composition based on plant morphological traits.

     

A comparative study of gut microbiota profiles of earthworms fed in three different substrates

The gut microbiome of earthworms has a complex interdependence with the host. When the soil minerals pass through earthworm’s gut, they may affect the gut microbiota. To gain insight into the response of gut microbiota to the passed minerals, we fed earthworm (Eisenia fetida) on nutrient-poor soil and ore powder, and used high throughput sequencing to characterize the earthworm intestinal microbial community to find evidence for a core bacterial community of the E. fetida. The results showed that earthworms’ gut maintained a core microbiome that appeared in all samples. These core microbiota may play a significant role in a species’ environmental interactions. The composition of intestinal microbiomes varied with substrates. The earthworm guts from two nutrient-poor substrates had similar microbial communities and they were different from nutrient-rich substrate. Proteobacteria and Bacteroidetes were more abundant in the gut of earthworms kept on a nutrient-poor substrate such as ore powder or mineral soil than in the gut of earthworms kept in organic-rich compost soil; some of these microorganisms may help earthworms survive in nutrient-poor substrates.     

Grunting for worms: seismic vibrations cause Diplocardia earthworms to emerge from the soil

Harvesting earthworms by a practice called 'worm grunting' is a widespread and profitable business in the southeastern USA. Although a variety of techniques are used, most involve rhythmically scraping a wooden stake driven into the ground, with a flat metal object. A common assumption is that vibrations cause the worms to surface, but this phenomenon has not been studied experimentally. We demonstrate that Diplocardia earthworms emerge from the soil within minutes following the onset of grunting. Broadband low frequency (below 500 Hz) pulsed vibrations were present in the soil throughout the area where worms were harvested, and the number of worms emerging decreased as the seismic signal decayed over distance. The findings are discussed in relation to two hypotheses: that worms are escaping vibrations caused by digging foragers and that worms are surfacing in response to vibrations caused by falling rain.     

Adsorption by soil of water-soluble phosphate from earthworm casts

Summary The equilibrium solution phosphate concentrations of mixtures of surface wormcasts and soil obtained from different depths were measured and from these concentrations, indices of the immobilization, by soil, of soluble phosphate from the wormcasts were derived. These were found to correlate with the nett P-adsorption capacity of soil taken from the same depths. It is suggested that the decrease in availability of soluble phosphate from wormcasts with increase in depth may result from an increase in adsorptive capacity for phosphate by the surrounding soil.