Harnessing The Drilosphere To Restore Ecosystem Functions In Degraded Soils

Drilospheres are one of several self-organized systems operated by ecosystem engineers that drive soil function. They have significant effects on soil-based supporting and regulating ecosystem services, especially plant production, carbon sequestration, and water infiltration and storage (Lavelle et al. 2006). Although drilospheric effects on organic matter dynamics are complex, and may have opposite directions depending on scales and specific organic fractions, there is some evidence that earthworm activities have positive effects on carbon sequestration in the long term (Lavelle and Spain 2006). Much research still is required, however, to answer this critical issue.

Drilospheric effects on plant growth and health and on soil physical properties are much better understood. Earthworms are legitimately considered important actors in the maintenance of adequate hydraulic properties in the upper 20 cm of soils, where infiltration and most detoxification processes operate. For these reasons, earthworms and their drilospheres long have been recognized as useful resources, and the potential for their management in agroecosystems is vast and diverse (Lavelle et al. 1999, Jimenez and Thomas 2001).

Soil degradation is most often associated with a depletion in biodiversity and abundance of earthworm and other invertebrate communities. Earthworms are greatly sensitive to land use intensification at plot and landscape levels. Ploughing and pesticide applications are especially harmful to them (Edwards and Bohlen 1996). Conversion of forests to pastures and cropped land and habitat fragmentation may eliminate a large proportion of native species where they still exist, although with variable and still poorly understood patterns (Fragoso et al. 1997, Lavelle and Lapied 2003, Hendrix et al. 2006). Natives are partly replaced by communities of exotic species, less than 50 species that form similar assemblages worldwide in comparable environment conditions. We thus are losing at a very fast rate the extraordinary diversity of native com munities generated by exceptional rates of endemism in highly sedentary organisms. In Amazonia, for example, the average ratio of local species richness to regional richness has been estimated at approximately 1%, compared to 20-30% on average for ants and termites and 80% for Sphingidae moths (Lavelle and Lapied 2004).

Communities of peregrine species or locally adapted species in turn tend to disappear when soil management makes the environment too difficult for them to survive. They suffer most from a lack of organic resources on which to feed, frequent destruction of their populations and habitats by ploughing, poisoning by pesticides, and water stress in soils when reduced plant and litter covers are reduced. In these soils, most ecosystem services associated with drilospheric activities tend to decline, even plant production that may require increasing amounts of chemical and other inputs to achieve the same crop yield level.

Management of ecosystem engineers is an important option in ecosystem restoration (Byers et al. 2006). Reconstitution of drilospheres,2 particularly, is an action to consider when re-creating or restoring soils, and several options already have been proposed to achieve this purpose (Senapati et al. 1999). The FBO (Fertilisation Bio Organique) patented method3 used in tree plantations creates hot spots of high fertility where organic residues of different qualities are buried in a specific order in the soil and inoculated with appropriate earthworms. A recent application of this method in India and China has allowed biodiversity of invertebrate communities and soil aggregation to significantly improve, while the organic tea thus produced had a significantly improved gustative quality (Pradeep Panigrahi unpublished data; Patrick Lavelle, Jun Dai, Nuria Ruiz-Camacho, Elena Velasquez unpublished data).

In general, drilosphere establishment first requires a restoration of organic inputs that provide adequate and sufficient feeding resources for the earthworms (Lavelle et al. 2001). Maintenance of permanent plant covers and organic amendments are practices that allow achieving, at least partly, this objective, provided the quality and location of organic materials are adequate for the earthworm species present. Such feeding resources eventually will allow local relict populations or inoculated earthworms to develop their digestive interactions with local microorganisms and increase their population density.

The quality of biological interactions within the new drilosphere thus created must be considered. In some cases, earthworm inoculation does

2 This process should not, however, be confounded with vermicomposting, which is the transformation of raw organic matter into a high-value compost by the Lumb-ricidae earthworm Eisenia fetida. This process is done outside the soil, and these worms are epigeics that cannot dig the soil.

3 PCT/FR 97/01363 for Sri Lanka; W0 98/03447.

fail, probably due to the inability of earthworms to adapt a microbial community that is too different from that of their original soil. This has been observed, for example, by Gilot-Villenave (1994), who showed that adult worms from the species R. omodeoi taken from a savannah site would not survive if transplanted in soil of an adjacent gallery forest; young worms issued from cocoons produced in savannah would survive, however, if they did hatch in the forest soil and interact from the beginning with the local soil microflora.

Once the interactions of organisms inside the drilosphere are re-established, the system will start to function and expand as biogenic structures are created. Interactions with other functional domains (drilospheres of other earthworm species, rhizospheres) restore the essential mechanisms that allow soils to provide the large range of functions used by human populations as ecosystem services.

Interactions of earthworms with plant roots are another important process to consider at that stage. It is likely that the topology of root systems that greatly differs among plant species has much to do with plant response to earthworm activities. Plants that have dense systems with a large proportion of very fine roots—e.g., the well-known tropical American plant Bixa orelana L. used by American Indians for their traditional face paintings—best respond to earthworm inoculations; conversely, plants with short systems or rather thick roots, such as the palm tree Bactris gasipaes Kunth, have limited responses (Brown et al. 1999).

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