Elsevier

Applied Soil Ecology

Volume 50, October 2011, Pages 1-13
Applied Soil Ecology

Review
Earthworms as colonizers of natural and cultivated soil environments

https://doi.org/10.1016/j.apsoil.2011.07.008Get rights and content

Abstract

For cultivated soils, the important function of earthworms as ecosystem engineers and their major contribution to the composition and functioning of soil ecosystems with a varying species diversity has been extensively addressed. However, the role of earthworms as colonizers of virgin, uncultivated soil in the process of soil formation has been little researched and long underrated. To better understand this role, the following questions need to be considered: (1) what makes an early colonizer successful, what are its characteristics, and which species are the most successful and under what circumstances are they successful?; (2) what are the limiting factors in these colonization processes with respect to environmental conditions and also to interspecific interactions?; (3) what do earthworms contribute to the further colonization by other soil animals?; and (4) how do they impact the soil itself and what could therefore be the consequences for soil management and restoration?

These questions have recently been addressed from the perspective of new (or ‘alien’) earthworm species invading ecosystems, suggesting a massive influx of species, competitive to the originally present fauna. This idea is, however, contrary to colonization, which suggests a gradual exploration of a previously uninhabited area. Unlike recent research, this review approaches colonization primarily as a spatial dispersal process and part of natural succession processes, and is mainly illustrated with examples of Palearctic species, either in Europe or introduced elsewhere. To begin, the various stages of colonization: dispersal, establishment, population growth and interspecies relations are analysed. Next, the colonization processes, the possible limiting environmental factors and the sequence of the appearance and establishment of species are described. Dispersal rates and sequences of colonization by different earthworm species are given for different soil ecosystems. For colonization, limiting environmental factors such as pH, soil type and heavy metal contents as well as the presence of organic matter seem to play a more important role than inherent ecological characteristics like r/K selection. Finally, the role of earthworms in the early colonization of soils that are earthworm-free because of non-cosmopolitan distribution, drained former sea bottom, permanently water-logged soils or anaerobic, acid peaty soils are reviewed. If we understand the role of earthworms in succession, we will be able to improve their role in soil restoration and soil management.

Highlights

► This review paper analyses colonization of soils by earthworms, an ecological dispersal and succession process. ► It complements recent papers on the consequences of invasion of exotic, alien species to soil ecosystems. ► It gives quantitative data on spatial dispersal rates and describes processes and mechanisms in dispersal. ► It describes succesful colonizing species,their characteristics, and consequences on soil characteristics. ► Combining older papers in Russian, German, French and English with recent ones, it covers many decades of research.

Introduction

The role of colonizers in soil formation of virgin, uncultivated soil has long been underrated. This holds true both for virgin soil that has never been inhabited and for anthropogenically influenced soil that has become ‘sterile’ and then inhabited again, such as sanitized soils (Tamis and Udo de Haes, 1995) and dredged sediments (Eijsackers et al., 2009). Several laboratory experiments have shown the intrinsic relation between soil community structure (species diversity) and system functioning (Thompson et al., 1993, Naeem et al., 1994, Tilman and Downing, 1994, Heemsbergen et al., 2004, Hedde et al., 2010). Although Darwin (1882) had already described these underlying processes, it was not until Jones et al. (1994) coined the term ecosystem engineer that the role of the earthworm in soil formation was more accurately described. The term was then further defined by Lawton (1994), Anderson (1995) and Lavelle (1997), especially the major contribution of earthworms to the composition and functioning of soil ecosystems with varying species diversity. In all of these experiments, however, earthworms were added to cultivated, mixed soil. For this reason, two important questions still remain on the role of earthworms as ecosystem engineers, namely what role do earthworms play and how do they impact the soil as invaders or early colonizers under natural soil conditions?

This topic has recently received a good deal of attention from the perspective of the ecological consequences of new (‘exotic’ or ‘alien’) species invading ecosystems, especially in North America and elsewhere in the Nearctic, and has been impressively described in a special issue of Biological Invasions (Hendrix, 2006, Hendrix et al., 2006, Hendrix et al., 2008). In this issue also meta-distribution over time (decades to centuries) is discussed for different areas in the world. However, the idea of invasion suggests a massive influx of species competing with the local biota. In contrast to the gradual process of colonization, this influx can cause major changes in the structure and functioning of ecosystems especially for agronomic and forestry systems (Ljungström, 1972).

Unlike recent research this paper approaches colonization as part of a step-wise succession process and deals mainly with spatial dispersal processes and rates of Palearctic species, either within Europe or introduced in other continents to cultivated soils. A complementary review on the colonization of contaminated land and soil and sediment waste deposits has recently been published (Eijsackers, 2010). Moreover, this review only briefly treats the meta-distribution patterns and processes of earthworm species, as well as the consequences of earthworm colonization for soil ecosystems, as this has already been described in relation to the North American situation by Hendrix et al. (2006).

The paper starts with an analysis of Bradshaw's (1993) various stages of colonization: getting there, establishing, growth (including interspecies relations). In focusing on the role of earthworms as colonizers, the following questions are addressed:

  • (1)

    What makes an early colonizer successful, and what kind of characteristics play a role in their success? Are these population-biological characteristics such as reproductive system, reproductive capacity or growth rate, or are these ecological characteristics such as resilience against adverse conditions (freezing, desiccation) and pH-distribution range?

  • (2)

    Which species are the most successful and under what circumstances are they successful? Is success related to soil or humus type?

  • (3)

    What are the limiting factors in these colonization processes with respect to environmental conditions and interspecific interactions? Assuming that dispersal, more specifically primary introduction, is mostly human-driven, soil treatments and land use, in general, could be main steering factors. However, both interspecific competition and facilitation of the soil conditions could also play a role.

  • (4)

    What do earthworms contribute to the soil's further colonization by other soil animals? (this issue is not further treated in this paper because of excellent reviews by Hendrix (2006) and Hendrix et al. (2006)). How do earthworms impact the soil with respect to bulk density, organic matter content and distribution, and what are the consequences of this impact for soil management and restoration?

Section snippets

Colonization as a succession process

Begon et al. (1996) define succession as ‘the non-seasonal, directional and continuous pattern of colonization and extinction on a site by specific populations’. Primary succession deals with soils that have not been previously inhabited by soil life due to adverse conditions: permanently water-logged, recently drained sediments (although benthic fauna may have had a distinct impact on sediment structure); soils with extreme acidity or alkalinity; or deeper soil layers becoming available

Dispersal

Dispersal can be sub-divided into passive dispersal, either by anthropogenic or natural processes, and active dispersal over the soil surface or through the soil. In contrast to migration, dispersal is undirected, although environmental conditions influence the direction and rate of dispersal.

Colonization process and limiting factors

Most authors who have investigated colonization of primary soil substrates stress the importance of topsoil, i.e. a layer of organic matter should be available (Dunger, 1969). Surprisingly, few reports on earthworm succession after natural catastrophes such as fires, landslides or floods have been published. Lee (1981) reported earthworm recovery after a scrubland fire: after a rapid, temporary recovery of the topsoil species in the first few months after the incident, no earthworm colonization

Various scales of earthworm colonization

From the literature on colonization by earthworms, different scales can be distinguished: colonization of continents and isles, colonization of catchments, and colonization of habitats such as grasslands and forest stands. Each colonization has different spatial scales, time scales, mechanisms and success factors. For example, the colonization of Australia, New Zealand, and southern Africa by European earthworm species has occurred over centuries, is mainly anthropogenic and has been successful

Acknowledgements

The author gratefully acknowledges the support that he received from the University of Stellenbosch, especially Professors Sophie and Adriaan Reinecke, and from the JRC/IES, especially former director Professor Manfred Grasserbauer and Dr Jan Marco Muller. The comments of Sten Rundgren, Kees van Gestel and James Curry during the preparation of the paper, as well as from five anonymous reviewers and the linguistic editing by Peter Griffith greatly improved the paper.

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    This paper was prepared for a large part during study leaves at the Department of Zoology of the University of Stellenbosch, South Africa, and the Institute for Environment and Sustainability of the EU-Joint Research Centre, Ispra, Italy.

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