Current and Potential Roles of Soil Macroinvertebrates (Earthworms,Millipedes, and Isopods) in Ecological Restoration

Soil macroinvertebrates have a considerable impact on soil functions important to the restoration process, such as decomposition; yet, soil organisms have received relatively little attention in restoration ecology in terms of their applicability as agents of restoration. Here, we review how large obligate detritivores (earthworms, millipedes, and isopods) have been used to accomplish restoration goals, assess restoration progress, and function as bioindicators. Patterns of detritivore community succession and how these communities are themselves restored during restoration of perturbed ecosystems are also discussed. We conclude with a discussion of increased utilization of these taxa in future and ongoing restoration projects as well as the outreach activities that should be associated with use of these organisms.     

Some Remarks on the Socio-Cultural Background of Restoration Ecology

Restoration ecology plays an important role in nature conservation policy in Europe today. It establishes the scientific basis for restoring ecosystems altered or destroyed by man to a more “natural” state. The goals of restoration ecology can generally be described in terms of increased biodiversity, enhanced water retention capacity, avoidance of soil erosion, etc. In practice, however, a discrepancy exists between the high ideals of restoration goals and reality, where one often encounters limiting factors. These limiting factors can include the conflict between different restoration goals, the unpredictability of restoration goals owing to long‐term effects and stochastic events, the insufficient social acceptance of landscape changes during restoration processes, and the use of restoration processes themselves (e.g., undisturbed succession, certain management measures like impoverishment of fertilized areas) as restoration goals in place of a certain resource quality (such as species composition, population sizes, water quality). Two examples from southern Germany show that restoration goals in European cultural landscapes can only be implemented successfully when they are integrated into the respective land use systems.     

Ecosystem effects of non-native earthworms in Mid-Atlantic deciduous forests

In many mid-Atlantic forests where both native and non-native earthworms exist, it is the non-native species that are the dominant component of the soil macrofauna. Few earthworm ecology studies, however, focus attention on these forest systems in order to determine the relative ecological roles and potential interactions of the native and non-native earthworms. In a series of field samplings and experimental manipulations we collected data on the effects of earthworms on below-and aboveground ecosystem processes. Earthworm abundance and the ecological processes measured were dynamic in space and time across the range of study sites. Leaf litter decay rates doubled at sites that had abundant non-native earthworms. Earthworms also altered the abundance of soil fungi, the activity of extracellular enzymes, soil respiration, and the growth of tree seedlings but the effects varied among sites depending on differences in land-use history and forest age. Red oak seedling growth was less at sites that had abundant earthworms but tulip poplar and red maple seedlings grew equally well with and without abundant earthworms. These preliminary results suggest that non-native earthworms have significant ecosystem effects, even in forests where native earthworms still occur. Land use history, however, plays an important role in determining what those effects will be, and these effects are likely to be dynamic, depending on the abundance of non-native earthworms.     

A Striking Profile: Soil Ecological Knowledge in Restoration Management and Science

Available evidence suggests that research in terrestrial restoration ecology has been dominated by the engineering and botanical sciences. Because restoration science is a relatively young discipline in ecology, the theoretical framework for this discipline is under development and new theoretical offerings appear regularly in the literature. In reviewing this literature, we observed an absence of in‐depth discussion of how soils, and in particular the ecology of soils, can be integrated into the developing theory of restoration science. These observations prompted us to assess the current role of soil ecological knowledge in restoration research and restoration practice. Although soils are universally regarded as critical to restoration success, and much research has included manipulations of soil variables, we found that better integration of soil ecological principles could still contribute much to the practice of ecosystem restoration. Here we offer four potential points of departure for increased dialog between restoration ecologists and soil ecologists. We hope to encourage the view that soil is a complex, heterogeneous, and vital entity and that adoption of this point of view can positively affect restoration efforts worldwide.     

The potential of earthworms to restore ecosystem services after opencast mining – A review

Opencast coal mining has several environmental impacts, which require land rehabilitation when mining operations are finished. For that reason, restoration after such extractive industries’ work is common and has been well studied. However, many ecological restoration schemes do not examine to what extent complete and functioning ecosystems have been restored above and below ground. While the aim should be to restore functioning ecosystems, most restoration plans focus only on vegetation and above ground macro-fauna.Among the potential species that are likely to be important early in mine land restoration, earthworms are particularly good candidates. They provide several ecosystem services that are likely to accelerate soil restoration, improve primary production and facilitate the restoration of a functional ecosystem in mining areas. These services include the following: increase in topsoil fertility, food for a wide range of predators and recycling of waste organic materials on rehabilitated areas.Here, we outline some of the challenges specifically facing opencast mining restoration and describe how the ecosystem services provided by earthworms may address some of these challenges.     

The ecology of restoration: historical links, emerging issues and unexplored realms

Restoration ecology is a young academic field, but one with enough history to judge it against past and current expectations of the science's potential. The practice of ecological restoration has been identified as providing ideal experimental settings for tests of ecological theory; restoration was to be the 'acid test' of our ecological understanding. Over the past decade, restoration science has gained a strong academic foothold, addressing problems faced by restoration practitioners, bringing new focus to existing ecological theory and fostering a handful of novel ecological ideas. In particular, recent advances in plant community ecology have been strongly linked with issues in ecological restoration. Evolving models of succession, assembly and state-transition are at the heart of both community ecology and ecological restoration. Recent research on seed and recruitment limitation, soil processes, and diversity–function relationships also share strong links to restoration. Further opportunities may lie ahead in the ecology of plant ontogeny, and on the effects of contingency, such as year effects and priority effects. Ecology may inform current restoration practice, but there is considerable room for greater integration between academic scientists and restoration practitioners.     

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.     

Science, Art, or Application—the "Karma" of Restoration Ecology

The present state of restoration ecology is far away from Bradshaw’s “acid test for ecology.” The conclusions drawn from the series of papers in this issue and from the Jena workshop suggest some directions in which the field may progress. More attention must be paid to the degraded state, which should be evaluated by its specific features and carefully analyzed before any restoration plan is laid down. Restoration goals have to be realistic, which includes the appreciation of globally changing conditions, resulting in a paradigm‐shift toward “forward‐restoration.” Basically, the transition from the degraded state conditions to the target state is a kind of succession that is manipulated by the application of goal‐orientated and system‐specific disturbances. Whenever possible, restorationists should step back and make use of naturally occurring succession, which requires a sophisticated restoration strategy, involving flexible management responses, multiple alternative target states, robust measurements for the restoration progress, and careful long‐term monitoring. The unique feature of restoration ecology is the involvement of socioeconomic decisions, and conceptual frameworks for ecological restoration have to implement the specific links to natural succession. To bridge the gap between ecological theory and on the ground restoration, it is essential that restoration practice is translated into the vocabulary and thinking of basic ecology. If all these aspects are integrated, ecological restoration as an application—and restoration ecology as an applied science—may develop into an acid test for our understanding of interactions between people and their environment, rather than for pure ecology.     

Earthworms use odor cues to locate and feed on microorganisms in soil

Earthworms are key components of temperate soil ecosystems but key aspects of their ecology remain unexamined. Here we elucidate the role of olfactory cues in earthworm attraction to food sources and document specific chemical cues that attract Eisenia fetida to the soil fungi Geotrichum candidum. Fungi and other microorganisms are major sources of volatile emissions in soil ecosystems as well as primary food sources for earthworms, suggesting the likelihood that earthworms might profitably use olfactory cues to guide foraging behavior. Moreover, previous studies have documented earthworm movement toward microbial food sources. But, the specific olfactory cues responsible for earthworm attraction have not previously been identified. Using olfactometer assays combined with chemical analyses (GC-MS), we documented the attraction of E. fetida individuals to filtrate derived from G. candidum colonies and to two individual compounds tested in isolation: ethyl pentanoate and ethyl hexanoate. Attraction at a distance was observed when barriers prevented the worms from reaching the target stimuli, confirming the role of volatile cues. These findings enhance our understanding of the mechanisms underlying key trophic interactions in soil ecosystems and have potential implications for the extraction and collection of earthworms in vermiculture and other applied activities.     

Restoration Ecology: Repairing the Earth's Ecosystems in the New Millennium

The extent of human‐induced change and damage to Earth's ecosystems renders ecosystem repair an essential part of our future survival strategy, and this demands that restoration ecology provide effective conceptual and practical tools for this task. We argue that restoration ecology has to be an integral component of land management in today's world, and to be broadly applicable, has to have a clearly articulated conceptual basis. This needs to recognize that most ecosystems are dynamic and hence restoration goals cannot be based on static attributes. Setting clear and achievable goals is essential, and these should focus on the desired characteristics for the system in the future, rather than in relation to what these were in the past. Goal setting requires that there is a clear understanding of the restoration options available (and the relative costs of different options). The concept of restoration thresholds suggests that options are determined by the current state of the system in relation to biotic and abiotic thresholds. A further important task is the development of effective and easily measured success criteria. Many parameters could be considered for inclusion in restoration success criteria, but these are often ambiguous or hard to measure. Success criteria need to relate clearly back to specific restoration goals. If restoration ecology is to be successfully practiced as part of humanity's response to continued ecosystem change and degradation, restoration ecologists need to rise to the challenges of meshing science, practice and policy. Restoration ecology is likely to be one of the most important fields of the coming century.     

Earthworms and eco-consequences: Considerations to soil biological indicators and plant function: A review

Earthworms have been well reported to have a beneficial effect on soil microbes, soil microbial biomass (SMB), fungal community, soil structure, water retention and plant growth in different terrestrial ecosystems. However, the interactions between environmental stressors and various species of earthworms and the subsequent effect on soil microbes, organic matter, soil structure and plant growth are still uncertain. The purpose of this analysis was to test 1- the impact of environmental stressors on earthworm behaviour. 2- the effect of various earthworms on soil microbes, plant growth, soil structure and the carbon cycle. We noted that less fatal temperatures are generally unknown, but higher fatal temperatures range from 25 to 48 °C. Earthworms have a role to play, depending on the nature of organic residues, in both the formation and degradation of soil aggregates. Improvements in microbial biomass and plant growth have been established according to temperature, soil toxicity, soil type, earthworms abundance, organic residues types and field conditions. We observed that although the summer temperature in the arid area was approximately (°C 48), it was found that a particular type of earthworm (Namalycastis indica) was responsible for improving soil characteristics.While a great deal of analysis has been carried out on the role of earthworms within the soil ecology, such a review identifies important knowledge gaps, particularly in the determination of the impacts of earthworm species on the soil structure, microbial biomass and plant productivity, in particular since most papers focused on European species and overlooked the role of earthworms in the arid landscape. Further research is recommended to compare the impacts of different earthworms species on soil microbes and plant growth in various soil types, earthworm abundance, field conditions, organic residues locations, inorganic fertilizers, pesticides, fertile or non-fertile soils and diverse conditions of drought and moisture.     

A modest proposal for restoration ecology

Restoration ecology struggles to mitigate human‐caused ecological damage. Non‐native species are a particular challenge. This article describes two restoration attempts following introduced species in California and then makes a radical culling proposal. Environmental regulations, legal protections, and restoration projects are necessary to preserve ecosystem services, but such policies are often unpopular. Restorers often struggle when public opinion opposes evidence‐based practice, and this occurs particularly when the interventions involve killing mammals. Therefore, restoration efforts may benefit from more attention to how individuals perceive the acceptability of environmental policies and how to communicate policy options effectively for individuals to make informed decisions. Restoration ecology can follow the recent shift of medicine away from imperatives and toward informed patient choice. Restoration projects may benefit from recent advances in psychology and communication that help individuals make policy decisions that align with their personal values.     

蚯蚓在生态系统中的作用

蚯蚓能够对许多决定土壤肥力的过程产生重要影响, 被称为“生态系统工程师”。它通过取食、消化、排泄和掘穴等活动在其体内外形成众多的反应圈, 从而对生态系统的生物、化学和物理过程产生影响。蚯蚓在生态系统中既是消费者、分解者, 又是调节者, 它在生态系统中的功能具体表现在: (1) 对土壤中有机质分解和养分循环等关键过程的影响; (2) 对土壤理化性质的影响; (3) 与植物、微生物及其他动物的相互作用。蚯蚓活动及其在生态系统中的功能受蚯蚓生态类群、种群大小、植被、母岩、气候、时间尺度以及土地利用历史的综合控制。蚯蚓外来种入侵与生态系统的关系以及蚯蚓对全球变化的响应和影响是两个值得关注的问题。土壤本身的复杂性, 蚯蚓自然历史和生物地理学知识的缺乏, 野外控制蚯蚓群落方法的滞后等都限制了蚯蚓生态学的发展。其他新技术如研究养分循环的碳氮同位素分析和揭示土壤微结构的图像分析等技术的应用是蚯蚓生态功能研究的迫切需要。     

Effects of Soil Nutrient Heterogeneity and Earthworms on Aboveground Biomass of Experimental Plant Communities

Soil nutrients are commonly heterogeneously distributed and earthworms are one of the most common soil organisms. While effects of both soil nutrient heterogeneity and earthworms have been well studied, their interactive effect on plant community productivity has rarely been tested. In a greenhouse experiment, we constructed experimental plant communities by sowing seed mixtures of four grasses, two legumes and two forbs in either a heterogeneous soil consisting of low and high nutrient soil patches or a homogeneous soil where the low and high nutrient soil patches were evenly mixed. The earthworm Eisenia fetida was either added to these soils or not. Aboveground biomass of the whole communities, grasses and legumes did not differ between the homogeneous and heterogeneous soils or between the soils with and without earthworms. However, soil nutrient heterogeneity reduced aboveground biomass of forbs, and such an effect did not interact with earthworms. In response to soil heterogeneity and earthworms, biomass ratio of the three functional groups showed similar patterns as that of their biomass. At the patch level, aboveground biomass of the whole community, grasses and legumes were greater in the high than in the low nutrient soil patches within the heterogeneous soil. A similar pattern was found for the forbs, but this was only true in the absence of earthworms. Our results suggest that soil nutrient heterogeneity and earthworms may not influence aboveground biomass of plant communities, despite the fact that they may modify the growth of certain plant functional groups within the community.     

Drought stress in rice (Oryza sativa L.) is enhanced in the presence of the compacting earthworm Millsonia anomala

Earthworms increase growth of most plant species through a number of poorly investigated mechanisms. We tested the hypothesis that earthworm modifications of soil structure and the resulting changes in water availability to plants explain this positive effect. Addition of endogeic earthworms Millsonia anomala induced a 40% increase in shoot biomass production and a 13% increase in CO₂ assimilation rate of well watered rice plants grown in pots. Conversely, when plants were subjected to water deficit, presence of earthworms had no effect on shoot biomass production and a negative impact on CO₂ assimilation rate (−21%). Early stomatal closure in presence of earthworms indicated lower water availability. The hypothesis that earthworms improve plant biomass production through soil physical structure modification was thus rejected. Three hypotheses were tested to explain this decrease in water availability: (i) a decrease in soil water retention capacity, (ii) an increase in evaporation from the soil or/and (iii) an increase in plant transpiration. Results showed that earthworms significantly reduced soil water retention capacity by more than 6%, but had no effect on evaporation rate. Water losses through transpiration were greater in the presence of earthworms when the soil was maintained at field capacity, but this was not the case under drought conditions. This experiment showed that the endogeic compacting earthworm M. anomala significantly increased plant photosynthesis by an undetermined mechanism under well-watered conditions. However, photosynthesis was reduced under drought conditions due to reduced soil water retention capacity.     

Introduced earthworms in agricultural and reclaimed land: their ecology and influences on soil properties, plant production and other soil biota

Accidental and deliberate introductions of earthworms into agricultural and reclaimed land are natural experiments that provide opportunities to understand the attributes of successful invaders and their impacts on local biota and ecosystem processes. We consider various case studies (e.g., earthworm invasions in agricultural soils in Australia and Brazil) and deliberate introductions of earthworms into reclaimed mine sites, landfills and cutaway peat in the U.K. and Ireland. Invasions of exotic earthworms, such as European Lumbricidae in Australia, have been geographically extensive, but remain very patchy at regional and field scales. Their impacts on soil properties, plant production and other biota are therefore also likely to be patchy. Various methods have been developed to deliberately inoculate exotic earthworms into disturbed lands, with varying degrees of success. The factors controlling success are, in general, poorly understood. A broad range of impacts of invasive earthworms on soil properties (e.g., soil structure, nutrient availability, burial of surface materials, incidence of root diseases) and plant yield and quality have been reported. Less is known of the impacts of invasive earthworms on other soil fauna, but they are likely to occur due to alterations in food availability and habitat structure. Influences on other biota are likely to extend to aboveground communities as well as those belowground. Introductions of earthworms to disturbed lands can yield substantial benefits in agricultural productivity and amelioration of soil degradation. However, the potential impact of the promotion or control of such introductions on non-target biota and ecosystem processes in pristine ecosystems nearby should be considered.     

喀斯特地区石漠化治理的理论模式探讨

基于恢复生态学的基本原理,提出了石漠化形成与治理的触发模型：生态系统所固有的推动自我发展的能力,称为主导力;使生态演替顶级偏离预定态的干扰因素,称为触发因子;主导力与触发因子相互作用,共同决定了生态演替的终态.石漠化是一系列恶性触发的结果,而石漠化治理,则是通过“人为设计”的生态恢复手段,激发生态系统“自我设计”的功能,从而实现生态恢复的良性触发过程. 以湘西凤凰县喀斯特石漠化生态系统恢复治理为例,对触发模型进行了初步检验. 结果表明,以触发模型为指导的恢复措施明显改善了土壤的理化性质,显著提高了植被覆盖率与植物多样性,与当地石漠化生态系统形成了良性触发,初步验证了触发模型的科学性.     

The influence of invasive earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms

Recent studies on earthworm invasion of North American soils report dramatic changes in soil structure, nutrient dynamics and plant communities in ecosystems historically free of earthworms. However, the direct and indirect impacts of earthworm invasions on animals have been largely ignored. This paper summarizes the current knowledge on the impact of earthworm invasion on other soil fauna, vertebrates as well as invertebrates.Earthworm invasions can have positive effects on the abundance of other soil invertebrates, but such effects are often small, transient, and restricted to habitats with harsh climates or a long history of earthworm co-occurrence with other soil invertebrates. Middens and burrows can increase soil heterogeneity and create microhabitats with a larger pore size, high microbial biomass, and microclimates that are attractive to micro- and mesofauna. Under harsh climatic conditions, the aggregates formed by earthworms may increase the stability of soil microclimates. Positive effects can also be seen when comminution and mucus secretion increase the palatability of unpalatable organic material for microorganisms which are the main food of most micro- and mesofaunal groups. For larger invertebrates or small vertebrates, invasive earthworms may become important prey, with the potential to increase resource availability. In the longer-term, the activity of invading earthworms can have a strong negative impact on indigenous faunal groups across multiple trophic levels. Evidence from field and laboratory studies indicates that the restructuring of soil layers, particularly the loss of organic horizons, physical disturbance to the soil, alteration of understory vegetation, and direct competition for food resources, lead directly and indirectly to significant declines in the abundance of soil micro- and mesofauna. Though studies of invasive earthworm impacts on the abundance of larger invertebrates or vertebrates are generally lacking, recent evidence suggests that reduced abundance of small soil fauna and alteration of soil microclimates may be contributing to declines in vertebrate fauna such as terrestrial salamanders. Preliminary evidence also suggests the potential for earthworm invasions to interact with other factors such as soil pollution, to negatively affect vertebrate populations.     

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。