Isabelle Barois

Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains.

Abstract The moment the soil enters into contact with an earthworm, both superficially and internally, physicochemical and biological changes take place. The drilosphere represents the whole soil volume under earthworm influence. Thus it includes the body surfaces, the gut and all the internal features of the worm that are in contact with the ingested soil, as well as the external structures (casts, burrows, middens) created by earthworm activities. The extent of the drilosphere and its particular characteristics depend on the species and ecological categories of the earthworm community present as well as the spatial and temporal scale of interest. Spatially, the drilosphere can interact with other soil functional domains and lead to significant changes in the litter system or detritusphere (generally decreasing litter stocks) and the rhizosphere (affecting both root biomass and density), the two main sources of organic matter (OM) additions to the soil, as well as in the aggregatusphere and the porosphere. Drilosphere effects on microbial activity and OM decomposition can be completely different (and opposite) depending on the spatio-temporal scale of observation. At the level of the gut, microbial activity is dramatically stimulated in a matter of a few hours via a mutualistic digestion system. In this process, water and soluble-C in the form of intestinal mucus (the Kiss) produced by the earthworm (Prince Charming) awakens the dormant microflora (Sleeping Beauties), thereby increasing decomposition of the stable forms of soil OM ingested. During gut passage populations of other organisms (e.g. protozoa, nematodes, fungi) may decline with digestion, although these organisms probably form a minor component of the earthworm’s energy needs. In the casts and on the burrow walls, the abundant nutrient resources for soil microflora continue the priming effect of the gut, increasing over a short time period mineralization rates and plant nutrient bio-availability. However as castings, particularly of the ‘compacting group’, and burrow walls begin to dry and stabilize with age (days to weeks), OM decomposition, nutrient mineralization and microbial activity decrease, often reaching levels lower than uningested soil due to ‘protection’. Finally at the scale of years to decades and soil profile, it appears that the drilosphere can exert an important regulation on OM incorporation and turnover rates, and soil C stocks.

A Hierarchical Model for Decomposition in Terrestrial Ecosystems: Application to Soils of the Humid Tropics

A general model is presented in which the dynamics of decomposition in terrestrial ecosystems are determined by a set of hierarchically organized factors which regulate microbial activity at decreasing scales of time and space in the following order: climate - clay mineralogy + nutrient status of soil - quality of decomposing resources - effect of macroorganisms (i.e., roots and invertebrates). At the lower scale of determination, biological systems of regulation based on mutualistic relationships between macro- and microorganisms ultimately determine the rates and pathways of decomposition. Four such systems are defined, i.e., the litter and surface roots system, the rhizosphere, the drilosphere and the termitosphere in which the regulating macroorganisms are respectively litter arthropods and surface roots, live subterranean roots, endogeic earthworms, and termites. In the humid tropics, this general model is often altered because climatic and edaphic constraints are in many cases not important and because high temperature and moisture conditions greatly enhance the activity of mutualistic biological systems of regulation which exert a much stronger control on litter and soil organic matter dynamics. This general hypothesis is considered in the light of available information from tropical rain forests and humid savannas. Theoretical and practical implications regarding the biodiversity issue and management practices are further discussed. It is concluded that biodiversity is probably determined, at least partly, by soil biological processes as a consequence of enhanced mutualistic interactions, which enlarge the resource base available to plants. It is also concluded that any effort to restore or rehabilitate degraded soils in the humid tropics is promised to fail unless optimum levels of root and invertebrate activities are promoted and the resulting regulation effects operate in the four abovedescribed biological systems of regulation. Research required to substantiate and adequately test the present set of concepts and hypotheses are expressed.

Mutualism and biodiversity in soils

Most soil invertebrates and roots have developed strong interactions with micro-organisms to exploit the organic and mineral resources of soil. Micro-fauna are mainly predators of microorganisms whereas larger organisms interact with micro-organisms through the “external rumen” or facultative endosymbiotic digestive systems. Mobilisation of nutrient and organic resources through mutualism with soil microflora seems to be all the more efficient as the organisms are large (like e.g., roots, termites or earthworms) and temperature is high. In the humid tropics, part of the existing species richness may have originated from an increased base of resources resulting from the development of mutualistic relationships. Evidence for this process is given for earthworm communities. Consequences for soil function and the species richness of plants and consumers are discussed.

Changes in respiration rate and some physicochemical properties of a tropical soil during transit through Pontoscolex corethrurus (Glossoscolecidae, Oligochaeta)

Soil ingested by Pontoscolex corethrurus Muller, a geophagous tropical earthworm, was transformed considerably during passage through the digestive tract. Readily-assimilable water-soluble compounds (mucus) with a high energy content represented 16 and 12.7% of the dry mass of soil in the anterior and posterior intestine respectively but comprised only 0.12% of the control soil and 0.43% of the fresh casts. Water content increased from 35% in the soil to 149% in the anterior part of the gut; it was 122% in the terminal part and 99% in the fresh casts. Ingested soil of pH 4.6 was neutralized in the anterior part of the gut (pH 6.8); the pH decreased to 6.0 in the posterior part and declined to 4.8 in the casts. These physicochemical modifications and the intense mixing within the gizzard and gut stimulated an increase in the respiratory activity of the microflora ranging from 1.37 fold in the anterior part of the gut to 7.30-fold in the posterior part and declining to 1.69-fold in the casts. Thus, the microbial activity is first strongly stimulated by more favourable physical conditions and it increases as intestinal mucus is expended. The microflora appears to become more able to digest the more complex organic matter of the soil for the benefit of the earthworm. A mutualistic relationship is proposed between microflora and earthworms for the exploitation of the complex organic matter of tropical soils.

Mucus production and microbial activity in the gut of two species of amynthas (megascolecidae) from cold and warm tropical climates

Abstract Amynihas gracilis inhabits warm lowlands and A. corticis tropical highlands; both are epigeic and their nutrition is largely based on soil. These species were used to test whether “the hypothesis of mutualism” is less intense in epigeic worms and to demonstrate the importance of temperature in this process. The mucus production of the anterior part of the gut contents of A. gracilis and A. corticis was 18 and 15% (of dry mass of gut content), respectively, which was the same as for Pontoscolex corethrurus . The water content in the gut of Amynthas was more than twice the field capacity of the control soil. The microbial activity (oxygen consumption) of the hindgut, measured at 28°C, was slightly higher for A. gracilis than for A. corticis (38 and 32 nl mg −1 dry soil h −1 respectively). The microbial activity decreased more than 3-fold, and more than 8-fold at 21 and 15°C respectively. When these oxygen consumptions are compared with those of the endogeic P. corethrurus (62 nl mg −1 dry soil h −1 ) it is noticed that the epigeic species have a lower microbial activity in their gut, and therefore a less intense relationship with the soil microflora than endogeic species. However, Amynthas spp tended to present a facultative mutualism because they have high content of mucus and water in their gut but the temperature should be above 21°C.

Andosol-forming process linked with soil fauna under the perennial grass Mulhembergia macroura

On the Cofre de Perote volcano, Mexico, at an elevation of 3000 m, vegetation is dominated by pine trees and Mulhembergia macroura grass. The grass undergoes a specific decomposition process whereby dead leaves and roots at different stages of decomposition accumulate below the plant, making a mat and forming a hummock of soil. Soil thin sections were prepared from the plant necromass and underlying soil to examine biological features by optical microscopy. Small organic fragments and soil aggregates were observed under a scanning electron microscope, coupled with a microprobe. C and N contents were measured, soil samples were analyzed by infrared spectroscopy and preliminary quantitative sampling of meso and macrofauna was executed in the plant residues and the underlying soil strata. Observations and analyses showed that soil microaggregates were faecal pellets from fauna, mainly Enchytraeids and Acari, living in the rooted soil below the grass. These biological aggregates exhibited a concentric internal structure and a silicon-rich coating which presumably protects them against microbial decomposition. Organic matter showed a predominance of aliphatic components upon aromatic components and appeared to be stable within the whole soil profile. As a consequence of plant die-off and mesofaunal activity, organic products accumulate and soil thickness and carbon storage increase with time.

Biological and mineralogical features of Andisols in the Mexican volcanic higlands

Abstract In the montane grasslands of Mexico, perennial grass and black Andisols are linked in a complex mechanism of soil formation in which both biogenic and mineral products interact. In this ecosystem, typical of the volcanic highlands, a sequence of profiles has been studied by macro- and micro-morphology, scanning and transmission electron microscopy (TEM), infra-red spectroscopy of soil samples and humic acid (HA) extracts, radiocarbon dating and pollen record, soil moisture and available water determinations and soil water analyses. The grass Muhlennberrgia macroura is important in the soil-forming process as it is the host of micro- and meso-fauna which produce abundant organic micro-aggregates. Soil formation began 7550 years ago and continued through several climatic and vegetation changes. The soil thickens as its age increases. Mineral neoformation is oriented towards allophane and halloysite, rather than Al-rich minerals such as imogolite and gibbsite, and high Si contents are observed in the soil water. The black Andisols have high water and carbon storage capacities and play a prominent role in regulating drainage. Presentday destruction of the grassland for potato cultivation will decrease the waterer reserve of these volcanic highlands.

Coffee Pulp Vermicomposting Treatment

The concept of vermicomposting began with the knowledge that certain species of epigeic earthworms, which live in the litter and primarily feed on pure organic matter (Bouche, 1977; Lavelle, 1981, Abdul and Abdul, 1994) grow in and consume organic waste materials, converting them into an earth-like soil-building substance that forms a beneficial growing environment for plant roots. Thus, the practice of vermicomposting could be defined as the combination of biological processes, designs and techniques used to systematically and intensively culture large quantities of certain species of earthworms in order to speed up the stabilization of organic waste materials, which are eaten, ground and digested by the earthworms with the help of aerobic and some anaerobic microbiota, and thereby naturally converted into much finer, humidified, microbially active faecal material, where important plant nutrients are held in a form much more soluble and available to plants than those in the parent compound (Aranda et al., 1999). The end product, a decomposed faecal material (earthworm faeces, vermicompost or “castings”) consists of very finely structured, uniform, stable and aggregated particles of humidified organic material with excellent porosity, aeration and water holding capacity, rich in available nutrients, hormones, enzymes and microbial populations. Thus, this product is a valuable, marketable and superior plant growth media (Edwards and Bohlen, 1996).