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Ingestion of charcoal by the Amazonian earthworm Pontoscolex corethrurus: a potential for tropical soil fertility

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Jean-François Ponge at Muséum National d'Histoire Naturelle
Jean-François Ponge
Stéphanie Topoliantz
Stéphanie Topoliantz
Sylvain Ballof
Sylvain Ballof
Sylvain Ballof
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Jean-Pierre Rossi at French National Institute for Agriculture, Food, and Environment (INRAE)
Jean-Pierre Rossi
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Abstract

It is now attested that a large part of the Amazonian rain forest has been cultivated during Pre-Colombian times, using charcoal as an amendment. The incorporation of charcoal to the soil is a starting point for the formation of fertile Amazonian Dark Earths, still selected by Indian people for shifting cultivation. We showed that finely separated charcoal was commonly incorporated in the topsoil by Pontoscolex corethrurus, a tropical earthworm which thrives after burning and clearing of the rain forest, and that this natural process could be used to improve tropical soil fertility. Our paper is a contribution to the present debate about (i) the origin of black carbon in fertile Dark Earths, (ii) the detrimental vs favourable role of Pontoscolex corethrurus in tropical agriculture, (iii) natural processes which might be used to increase tropical soil fertility
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Type of contribution: Letter to the Editor 1
Date of preparation: 19 December 2005 2
Number of text pages: 5 3
4
Title: Ingestion of charcoal by the Amazonian earthworm Pontoscolex corethrurus: a 5
potential for tropical soil fertility 6
7
Jean-François Ponge1, Stéphanie Topoliantz1, Sylvain Ballof2, Jean-Pierre Rossi3, Patrick 8
Lavelle4, Jean-Marie Betsch5, Philippe Gaucher6 9
10
1Muséum National d’Histoire Naturelle, CNRS Unité Mixte de Recherches 5176, 91800 11
Brunoy, France 12
2Office National des Forêts, 97370 Maripasoula, Guyane Française 13
3Institut National de la Recherche Agronomique, INRA, Unité Mixte de Recherches 14
BIOGECO, 33612 Cestas Cédex, France 15
4Institut de Recherche pour le Développement, Unité Mixte de Recherches BIOSOL 137, 16
93143 Bondy Cédex, France 17
5Muséum National d’Histoire Naturelle, Unité Scientifique 306, 91800 Brunoy, France 18
6Mission pour la Création du Parc de la Guyane, 97326 Cayenne Cédex, Guyane Française 19
20
Correspondence: Jean-François Ponge, Muséum National d‟Histoire Naturelle, CNRS UMR 5176, 4 avenue du
Petit-Château, 91800 Brunoy, France, E-mail: jean-francois.ponge@wanadoo.fr
Abstract 1
2
It is now attested that a large part of the Amazonian rain forest has been cultivated 3
during Pre-Colombian times, using charcoal as an amendment. The incorporation of charcoal 4
to the soil is a starting point for the formation of fertile Amazonian Dark Earths, still selected 5
by Indian people for shifting cultivation. We showed that finely separated charcoal was 6
commonly incorporated in the topsoil by Pontoscolex corethrurus, a tropical earthworm 7
which thrives after burning and clearing of the rain forest, and that this natural process could 8
be used to improve tropical soil fertility. Our paper is a contribution to the present debate 9
about (i) the origin of black carbon in fertile Dark Earths, (ii) the detrimental vs favourable 10
role of Pontoscolex corethrurus in tropical agriculture, (iii) natural processes which might be 11
used to increase tropical soil fertility 12
13
Keywords: Tropical earthworms, Tropical soil fertility, Slash-and-burn agriculture, Charcoal 14
15
Pontoscolex corethrurus (Annelida: Oligocheata: Glossoscolecidae) is a small 16
terrestrial earthworm which commonly inhabits rain forest soils over the whole Amazonian 17
basin (Römbke et al., 1999). Its important burrowing activity through the topsoil, associated 18
with its efficient digestive system (Zhang et al., 1993; Barros et al., 2001), allows it to thrive 19
in soils poor in organic matter, such as those found in areas now deforested for the need of 20
agriculture. In the absence of organic input to the soil, excessive casting activity of this 21
species may cause damage to permanent pastures through the coalescence of earthworm casts, 22
leading to appearance of a thick compact surface crust (Chauvel et al., 1999). However, the 23
detrimental influence of this species may be questioned when the agricultural use of the land 24
is only temporary, as in slash-and-burn shifting agriculture, or when available carbon is 25
regularly added to the soil. We hypothesized that P. corethrurus could be responsible for the 1
observed increase in soil fertility which has been reported to occur in Amazonian Dark Earths 2
formed during Pre-Colombian times (Myers et al., 2003; Steiner et al., 2004). 3
4
Using a quantitative optical method (Topoliantz et al., 2000), we investigated the 5
distribution of humus components in soils under shifting cultivation, still practised by 6
Wayana and Aluku people settled along the Maroni river, French Guiana (Topoliantz et al., 7
2005b). This method allowed us to estimate the relative volume of components of the soil 8
matrix, including plant tissues at varying stages of decomposition, mineral particles of 9
varying size and nature, aggregates of varying colour, size and shape. 10
11
The untouched old forest exhibited low contents of both charcoal and charred material, 12
representing 2% and 7% of the volume of the soil matrix, respectively. We showed that six 13
months after burning of the same forest for cultivation, the contents of charcoal and charred 14
material increased to 10% and 20% of the soil matrix, respectively, in the top 3 cm. After 15
three years of cultivation these amounts decreased to 6% and 15%, respectively. During the 16
cultivation period the amount of dark humus (mixture of charcoal and mineral soil in varying 17
proportion) increased steadily. The examination of dark humus revealed that it was mainly 18
comprised of faecal pellets of P. corethrurus, which contained a multitude of small charcoal 19
fragments of 10-100 µm admixed in a mineral paste. 20
21
Charcoal, ingested together with soil particles, is mixed with mucus secreted in the 22
oesophagus then finely ground in the muscular gizzard of earthworms. It is excreted as a 23
muddy paste which is further stabilized by Van der Wals forces after drying, thus forming 24
dark humus (Hayes, 1983). We also showed by laboratory experiments that P. corethrurus did 25
not ingest charcoal alone but rather added it to mineral soil. A mixture of charcoal and soil 1
was preferred to either pure charcoal or pure soil (Topoliantz and Ponge, 2003, 2005a). This 2
points to a positive feed-back which improves the habitat of P. corethrurus by increasing the 3
carbon content of the soil. 4
5
It has been demonstrated that finely divided charcoal (also called black carbon) was a 6
source of stable humus (Tryon, 1948; Chan et al., 1999). Slow oxidation and hydroxylation 7
increase donor/acceptor charges, giving the soil strong exchangeable properties. The positive 8
impact of charcoal in ameliorating the physical and chemical properties of tropical soils has 9
been reported in various situations (Glaser et al., 2002). To the light of our results we expect 10
the peregrine earthworm P. corethrurus to be the main agent for the incorporation of charcoal 11
to the topsoil in the form of fine particles of silt size, which favoured the formation of stable 12
humus in Amazonian Dark Earths or „Terra Preta‟ during Pre-Colombian times (Glaser et al., 13
2000). 14
15
The natural development of P. corethrurus, able to feed and reproduce in tropical soils 16
poor in organic matter, opens avenues for new agricultural practices better adapted to 17
permanent settlements, using charcoal in mixture with nutrient-rich amendment (Steiner et al., 18
2004). In situ experiments were conducted with the help of a local agriculturist at Maripasoula 19
(French Guiana), using waste products of slash-and-burn agriculture (charcoal and manioc 20
peels) as an amendment. We demonstrated that the addition of charcoal together with manioc 21
peels, known to be rich in phosphorus (a limiting nutrient in tropical soils), increased yard-22
long bean production at the natural population size of P. corethrurus, thus allowing 23
diversification of family agriculture without any additional cost (Topoliantz et al., 2002;; 24
Topoliantz et al., 2005). 25
1
Acknowledgements 2
3
This work was supported by the French Ministry of Ecology and Sustainable Development 4
(SOFT program) and by a grant from the Commission for the Creation of the Guiana Natural 5
Park. The authors warmly acknowledge Dr. C. Kerdelhué (INRA, Pierroton, France) and Dr. 6
L. Greenfield (Canterbury University, Christchurch, New Zealand) for language editing. 7
8
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  • Mar 2001
  • GEODERMA
In a central Amazonian pasture, a single earthworm species, Pontoscolex corethrurus, becomes very abundant (400 ind. m−2) after forest clearing. Its casts form a compact, continuous and impermeable crust with a thickness of 20 cm. To analyze the structural modifications, we established a field experiment in which soil blocks from the forest were implanted in the pasture, and soil blocks from the pasture were implanted in the forest. The objectives were (1) to verify the formation of the compact crust at the soil surface in pasture environment, (2) to evaluate the time necessary for the formation and the destruction of this crust, and (3) to find out if the crust formation was a reversible process. We used quantitative morphology to identify the biogenic structures formed by different fauna groups and to quantify the modifications in the solid phase as well as the resulting porosity. For the soil depth 0–5 cm, the measured porosity was 48% in the forest and 16% in the pasture. After 1 year, the blocks of forest soil installed in the pasture presented a porosity of 26%, and the blocks of pasture soil installed in the forest presented a porosity of 34%. There were significant differences between the control blocks and the exchanged blocks. The results demonstrate that the processes of formation and destruction of the biogenic structures are reversible. Approximately 1 year is necessary to re-establish the equilibrium between the exchanged blocks and the control blocks.This experiment illustrates the compacting effect of P. corethrurus. In addition, the small millimetric pores, which are formed by termites in the blocks of pasture soil implanted in the forest, show the decompacting effect of certain termite groups.
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Ameliorating Physical and Chemical Properties of Highly Weathered Soils in the Tropics with Charcoal – a Review
Article
Full-text available
  • Jun 2002
Rapid turnover of organic matter leads to a low efficiency of organic fertilizers applied to increase and sequester C in soils of the humid tropics. Charcoal was reported to be responsible for high soil organic matter contents and soil fertility of anthropogenic soils (Terra Preta) found in central Amazonia. Therefore, we reviewed the available information about the physical and chemical properties of charcoal as affected by different combustion procedures, and the effects of its application in agricultural fields on nutrient retention and crop production. Higher nutrient retention and nutrient availability were found after charcoal additions to soil, related to higher exchange capacity, surface area and direct nutrient additions. Higher charring temperatures generally improved exchange properties and surface area of the charcoal. Additionally, charcoal is relatively recalcitrant and can therefore be used as a long-term sink for atmospheric CO, Several aspects of a charcoal management system remain unclear, such as the role of microorganisms in oxidizing charcoal surfaces and releasing nutrients and the possibilities to improve charcoal properties during production under field conditions. Several research needs were identified, such as field testing of charcoal production in tropical agroecosystems, the investigation of surface properties of the carbonized materials in the soil environment, and the evaluation of the agronomic and economic effectiveness of soil management with charcoal.
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Earthworm Ecology
Chapter
  • Jan 1983
Darwin’s observations on earthworms can be regarded as a milestone in our understanding of soil biology and an enormous contribution to some aspects of the genesis of humus and of its role in soils. This chapter outlines Darwin’s conclusions on the role of earthworms in the formation of vegetable mould and his interpretations of its nature and properties, especially those of its organic constituents. It discusses modern concepts of the composition, structure and properties of humus substances and the role they play in soil, especially in stabilizing aggregates and retaining water and plant nutrients.
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Pasture damage by an Amazonian earthworm
Article
  • Mar 1999
Almost all cultivated soils undergo some reduction in the porosity of the surface layers, and nowhere is this more evident than in tropical rainforests that have been converted to pastures. Following deforestation in an area of Costa Rica, soil bulk density has been shown to increase rapidly after conversion to pasture, leading to poor drainage and a reduced rate of gaseous diffusion¹. These factors limit methane consumption and promote the anaerobic production of methane. A similar effect on methane flux has been found in upland soils in the Brazilian Amazonian basin after conversion from forest to pasture²,³. Increases in atmospheric methane are therefore not limited to emissions from flooded soils⁴, as forest-to-pasture conversion promotes the anaerobic mineralization of organic matter by changing the physical properties of soil.
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Oxidative reactivity of coal chars in relation to their structure
Article
  • Oct 1999
  • FUEL
During the oxidation of porous coal chars the internal surface area can increase as a function of the degree of conversion due to pore growth and the opening up of sealed internal pores or cavities. Consequently, rate expressions for their oxidation are more accurately described in terms of the intrinsic reactivity, where differences in surface area and porosity can be taken into account.The oxidative reactivity of coal chars is complicated by a number of different factors, which are explored in this paper. These include (i) the development of the pore structure during devolatilisation of the coal, (ii) the ash content, its distribution in the carbon matrix and effect on reactivity, (iii) the extent of the H and N functional groups present in the solid matrix, and their interrelation with residual volatile species which are present, (iv) the extent of the graphitic nature of the carbon surface and (v) the active surface area available for reaction.
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Black carbon in density fractions of anthropogenic soils of the Brazilian Amazon region
Article
  • Jul 2000
  • ORG GEOCHEM
Frequent charcoal findings together with black carbon concentrations in the soil organic matter (SOM) of up to 35% provided evidence that black carbon is important for the SOM stability in Terra Preta soils. This paper aims to investigate whether black carbon is additionally stabilised by organo-mineral complexation. For this purpose black carbon was analysed in density fractions using benzenecarboxylic acids as molecular markers. Density fractions were also studied by scanning electron microscopy and energy dispersive X-ray spectroscopy. Concentrations and total amounts of black carbon were generally highest in the light fraction indicating that a major part of black carbon is not chemically stabilised but intrinsically refractory. On the other hand, a large part of black carbon was also found in the heavier fractions, where it was partly embedded within plaques of iron and aluminium oxides on mineral surfaces. The major part of black carbon in the medium fraction seemed to be organo-mineral complexed because we found amounts of black carbon in this fraction by wet chemical analysis but not by scanning electron microscopy and energy dispersive X-ray spectroscopy. The spectroscopic analysis can only detect particulate black carbon. Black carbon was particularly enriched in 30–40 cm soil depth, and in all fractions of Terra Preta soils compared to adjacent Oxisols. The occurrence of particulate black carbon together with potsherds in the subsoil horizons of Terra Preta soils indicate that this might be due to turbation processes or the soils were covered by earthworm or termite activities. Further research, however, is needed to clarify the transport mechanisms of black carbon into deeper soil horizons.
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