07) 127–133www.elsevier.com/locate/geoderma

Geoderma 139 (20

Role of the fungus-growing termite Pseudacanthotermes spiniger(Isoptera, Macrotermitinae) in the dynamic of clay and soil

organic matter content. An experimental analysis

Pascal Jouquet a,⁎, Nicolas Bottinelli a, Jean-Christophe Lata b,Philippe Mora c, Sandrine Caquineau d

a Laboratoire d'Ecologie des Sols Tropicaux, UMR 137 Biosol, IRD, 32 Avenue H. Varagnat, 93143 Bondy Cedex, Franceb Laboratoire d'Ecologie, Systématique et Evolution, UMR 8079, Bât 362, Université Paris-Sud, 91405 Orsay Cedex, France

c Laboratoire d'Ecologie des Sols Tropicaux, UMR 137 Biosol, Université Paris 12, 61 avenue du Général de Gaulle, 94010 Créteil Cedex, Franced UR055 Paléotropique, IRD, 32 Avenue H. Varagnat, 93143 Bondy Cedex, France

Received 18 January 2006; received in revised form 15 September 2006; accepted 24 January 2007Available online 21 February 2007

Abstract

This work focuses on the interactions between fungus-growing termites (Isoptera, Macrotermitinae), clay particles and soil organic matter(SOM). As major bioturbators in tropical ecosystems, termites create biogenic structures (galleries, sheetings, nests, mounds, fungus-combchambers) that strongly influence the physical and chemical properties of soils. Different kinds of substrates were given to Pseudacanthotermesspiniger, one of the main famous Macrotermitinae termite species in West Africa: (i) clay (mainly illite), (ii) a mix of sand and clay, or (iii) sand.When we proposed both clay and sand, we observed a high selection of clay by termites. Observation of the properties of biogenic structures by X-ray analysis showed that illite contained in the sheetings was strongly modified when compared to the bulk soil. We argue that the termite's salivaand/or the action of stimulated associate microorganisms have extracted un-exchangeable potassium, then leading to the creation of smectitelayers. Thus, the termites P. spiniger, thanks to their building activity, can be seen as weathering agents of clay minerals. SOM content of thebiogenic structures was found to be highly variable depending on the type of soil used (clay vs. sand) with enriched or impoverished C and Ncontents. Finally, we discuss how the auto-ecological requirements of termites (the balance between the cost of organic matter incorporation andthe stability of the rehandled substrates) can affect soil and ecosystem functioning.© 2007 Elsevier B.V. All rights reserved.

Keywords: Termites; Clay weathering; Clay selection; SOM content; PCI; WCI

1. Introduction

Clay content, SOM quality and quantity play key roles incontrolling soil properties (Brady and Weil, 1999), andparticularly soil fertility, through their influence on soilaggregation as well as on the transfer and retention of ions andnutrient exchange (Brady and Weil, 1999). While there are manystudies describing how soil animals control and influence SOM(Lavelle and Spain, 2001), the effects on clay dynamics (i.e.,distribution along the soil profile and mineralogy) have morerarely been studied. Parameters that affect the transformation of

⁎ Corresponding author. Tel.: +33 1 48 02 59 60; fax: +33 1 48 02 59 70.E-mail address: pascal.jouquet@bondy.ird.fr (P. Jouquet).

0016-7061/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.geoderma.2007.01.011

clay are considered to be mainly abiotic (i.e., temperature,humidity and chemical environment). Soil organisms aretraditionally considered to have little or only indirect effects onclay mineralogy through the decomposition of their body and theproduction of acids (Robert and Berthelin, 1986; Barker et al.,1997). However, there is increasing evidence that livingorganisms are also able to act as weathering agents, modifyingclay properties in a significant manner (see Banfield et al., 1999;Landeweert et al., 2001, for microorganisms; Badraoui et al.,1992; Hinsinger et al., 1992, 1993; Augusto et al., 2001; Pernes-Debuyser et al., 2003, for plants; Jouquet et al., 2002b; Needhamet al., 2004, respectively for termites and earthworms).

In tropical soils, fungus-growing termites (Isoptera, Macro-termitinae) play an important role in soil fertility because of

Fig. 1. Termite colony (centre) was connected with wood sticks to three boxes tofilled in with clay, sand or a mixture of them (clay below, sand above in aproportion of 400/900 g). Few days after, termites covered the wood, soil andlitter (leaves of Platanus acerifolia) with soil. The behaviour of termites wasregularly followed during 6 weeks. At the end of the experiment, sheetings andsoil covering the subterranean galleries were collected and their propertiesdetermined.

128 P. Jouquet et al. / Geoderma 139 (2007) 127–133

their significant impact on soil physical and chemical prop-erties. The influence of Macrotermitinae termites on SOM andclay has mainly been related to above-ground mound materialsbuilt by Macrotermes sp. These termites significantly modifytheir environment by increasing the clay and SOM contents inorder to ensure the structural stability of their nest structures(Holt and Lepage, 2000; Jouquet et al., 2004). Conspicuousdifferences have also been observed in the mineralogicalproperties of clays collected and used by termites for buildingtheir nests (Leprun and Roy-Noël, 1976; Boyer, 1982; Mahaneyet al., 1999). As a consequence, it has been speculated thatMacrotermitinae termites are able to modify clay mineralogy.However, this hypothesis has been difficult to confirm becauseone major problem is to determine precisely the origin of thesoil selected by termites for building their nests. Becausetermites are able to transport orally clay particles from deepsoil horizon and to soften them with saliva, it remains verydifficult to determine if changes in mineralogical propertiesresult from a selection rather than a modification of these claymaterials.

Few studies have investigated the influence of subterraneanfungus-growing termites on SOM and clay properties, perhapsdue to their hidden localization. These species live insubterranean nests called “fungus-comb chambers”, where theexosymbiosis between termites and the fungus Termitomycestakes place. Using laboratory experiments with manipulation ofthe termite workers, Jouquet et al. (2002a,b) showed thatsubterranean fungus-growing termites are able to use preferen-tially fine particles for covering their exosymbiotic fungus-comb and to enhance SOM content (saliva). They alsodemonstrated that termite handling can lead to an increase inthe expandable layers of the component clay minerals and thatheating and saturation with potassium of modified clays do notcompletely close the newly formed clay layers. These effects oftermites on soil properties were however found to varyaccording to the type of construction (galleries or soil coveringthe fungus-comb) and the nature of the soil used. In order todetermine to what extent subterranean Macrotermitinae termitesinfluence soil properties, field analyses were investigated byJouquet et al. (2005). These authors found contradictory resultsto those obtained in laboratory conditions. They speculated thatclay mineral properties in the fungus-comb chamber walls werenot significantly different from those in the bulk soil but weresmaller. This study also shows varying SOM content in the wallof the fungus-comb chambers with higher or lower C and Ncontents according to the termite species and study sites.

Consequently, there is a real need to find laboratoryexperiments with in situ soil sampling in order to fullyunderstand the effects of subterranean fungus-growing termiteson clay and SOM content and properties. Most published workson soil modification by termites are purely descriptive,comparing in situ constructions and putative parent soils(Abbadie and Lepage, 1989; Jouquet et al., 2003, 2005).Conversely, laboratory experiments under controlled environ-ments can produce an overview of mechanisms that can beprocessed in the field (Jouquet et al., 2002a,b). However, themain disadvantage to laboratory-based studies is that termite

workers are stressed and their behaviour can be different to thatin the field. In this study, the influence of a subterranean fungus-growing termite species (Pseudacanthotermes spiniger) on themineralogy of clays and on SOM content was investigatedthrough an alternative experiment. A well developed termitecolony that was grown in laboratory for 6 years was used tohighlight how fungus-growing termites affect soil propertiesthrough their foraging activities (i.e., galleries and sheetingsbuilding).

2. Materials and methods

2.1. Colony manipulation in the laboratory

The termite utilised in this study was P. spiniger (Isoptera,Macrotermitinae). This species is one of the main termitespecies living in West Africa (Josens, 1972). It cultivates anexosymbiosis fungus (Termitomyces) in belowground unitscalled fungus-comb chambers. It also constructs coveredrunways in soil (i.e., galleries) and on the soil surface (i.e.,sheetings) so that it can safely collect plant materials. Thecolony was collected in Lopé forest (Gabon) in 1999 and grownin a rearing room (temperature 25 °C, humidity 50–70%) inbasins (1 m diameter and 50 cm deep) filled in with soil.Termites were fed exclusively with wood and leaves of Platanusacerifolia previously air-dried.

All manipulations were done in the rearing room with theavailable colony. Three plastic boxes (20⁎10⁎10 cm depth)were connected with wood sticks to the central basin thatcontained the colony (Fig. 1). The three boxes were then filledwith the same material during 6 weeks and covered by leaves ofP. acerifolia as follows: (i) 800 g clay (“French green clay” thatmainly contain illite, experiment 1), (ii) 1600 g sand (from

Table 1C and N content in the two different substrates (clay and sand) before (n=3) andafter the rehandling by termites (n=19 and 3, respectively for clay and sand,standard error in brackets)

C (%) N (%)

Before termitesClay 1.73 (0.02) 0.03 (0.01)Sand 0.01 (0.01) 0.01 (0.01)

After termitesClay 1.41 (0.31) 0.03 (0.01)Sand 0.70 (0.26) 0.03 (0.01)

Fig. 2. X-ray diffraction spectrum of control and termite-handled soils (sheetingsand galleries), showing the proportion of kaolinite (7 Å), illite (WCI+PCI: 10 Å)and chlorite (14 Å).

129P. Jouquet et al. / Geoderma 139 (2007) 127–133

Fontainebleau, France, experiment 2) or (iii) a mixture ofFrench green clay (400 g) in the bottom of the box covered bysand (900 g) (experiment 3). The experiment was done threetimes in order to have three repetitions. In the same room,control soils (clay or sand) were put in boxes, covered by leavesof P. acerifolia and wetted (n=3).

2.2. Measurements

Biogenic structures (sheetings covering the soil and the litter,and soil surrounding the belowground galleries) were air-driedand weighted (experiments 1 and 2). Because of the numeroussheetings built from clay and the few ones built from sand, thenumber of repetitions was n=19 for sheetings built from clayand n=3 for those built from sand. The percentage of organicmatter incorporated in the substrates was assessed by the totalorganic C and N content with an elemental analyser (NA 1500Series 2, Fisons). Soil pH was determined in soil:watersuspension (1:2.5).

Clay mineralogy was determined by X-ray diffraction(XRD) using a Siemens D500 diffractometer with Ni-filteredCu–Kα radiation at 40 kV and 30 mA. Air-dried samples fromexperiment 1 were scanned from 2 to 15°2θ at 0.6°2θ min−1.Spectra were decomposed using the DECOMPRX program ofLanson (1990) for a range of 4–13°2θ. Decomposition wasdone using Gaussian shapes for interstratified illite–smectite(IS) and poorly crystallized illite (PCI), and Lorentzian shapesfor well crystallized illite (WCI) (Meunier and Velde, 2004).The relative abundance of clay types was determined byestimating the peak area derived from the peak decompositionmethods. This method is only relative and should indicatechanges in the abundance of clay species present for similarmaterials (Lanson and Velde, 1992; Velde, 1995).

2.3. Observations and samplings of materials selected

Behaviour and soil selection by termites were followed inboxes with both clay and sand (experiment 3). Each week,pictures were taken to draw a general schema of the termiteforaging strategy. Soil selected by termites for buildingsheetings above the soil was easy to determine because of thegreen colour of clay and the white one of sand. At the end of theexperiment, soil sheetings were collected and separated intofour classes according to their constitutions: (i) only clay, (ii)

only sand, (iii) clay+soil from the basin, (iv) clay+sand+soilfrom the basin. Soils were thereafter air-dried and weighted.

2.4. Statistical analyses

Treatment effects on soil pH, C and N content, and therelative abundance of clay types were tested through analysis ofvariance (ANOVA). Prior to analysis data were inspected forhomogeneity of variance (Levene test) and log-transformed ifrequired. All statistical calculations were carried out usingStatistica 5.0 for Windows. Differences were consideredsignificant only when p values were lower than 0.05.

3. Results

3.1. Soil properties

The results did not show any significant effect of termites onthe pH of clay (mean value: 7.5) and sand (mean value: 5.5)( pN0.05 for both).

The influence of termites on SOM content is shown inTable 1. No difference in C and N content was found betweenboth sheetings and galleries in both treatments ( pN0.05). Whilethe carbon content was significantly lower in biogenicstructures built from clay than in the control clay-soil( pb0.001), an increasing C content was found when termitesused sand ( pb0.001). The N content was very low in controlclay-soil and no significant difference was obtained with clayused by termites ( pN0.05). Conversely, the N content wassignificantly higher in sand used by termites for buildingsheetings and galleries ( p=0.02).

3.2. Clay mineralogy

The decomposition of the clay X-ray spectrum before andafter the action of termites is shown in Fig. 2. In addition toillite, kaolinite and chlorite were detected in all samples, but in

Fig. 4. Soil selection by termites. Soil from the basin was first used by termites

130 P. Jouquet et al. / Geoderma 139 (2007) 127–133

minor proportions. Since these two minerals did not seem tochange significantly among the investigated samples, they werenot considered further in the assessment of mineral change overthe action of termites and we reported our findings for IS, PCIand WCI.

Three peaks can be observed at different positions in the 10–20Å regions: IS peak occurred at near 11 Å, PCI at near 10.3 Å andWCI at near 10 Å (Fig. 3). Clay mineralogy was not affected bytermites when they built the galleries (Fig. 3b) because theproportions of IS, PCI andWCIwere significantly similar to thoseobserved in the control soil ( pN0.05). However, inspection ofsheeting diagrams (Fig. 3c) shows that PCI and WCI peakschanged in character and intensity. PCI peak widened and itsproportion was significantly higher, indicating an increase insmectite content. Conversely, intensity of WCI peak diminished

Fig. 3. X-ray diffraction patterns of air-dried clay fractions of the “French greenclay” before (Control) and after (Termite) the action of termites. IS:interstratified illite–smectite; PCI: poorly crystallized illite; WCI: wellcrystallized illite. a: control samples; b: galleries; c: sheetings.

for building the sheetings. Sand (in white) was used as soon as termites arrivedin the box. Clay (in green) translocation occurred at the base of the wood incontact with the box substrate.

and its proportion was lower than the clay-soil ( pb0.001 for bothPCI and WCI). No significant differences were found with theproportion and the position (d-spacing) of IS ( pN0.05).

3.3. Soil selection by termites

Termites brought soil from the basin on the first half of thestick wood at the beginning of the experiment. They afterwards

Fig. 5. Soil selection by termites. Underground clay has been translocated to thesoil surface and was used by termites to consolidate sheetings (a). At the end ofthe experiment, all the sheetings in the box were replaced and/or consolidatedwith clay (b).

Fig. 6. Constitution of sheetings collected on wood and soil surface. Substrates:clay (95% clay), sand (95% sand), a mix of clay and soil from the basin(clay+soil), and a mix of clay, sand and soil from the basin (clay+ sand+soil)(n=3, bars indicate standard errors, histograms with the same letter are notdifferent at p=0.05).

131P. Jouquet et al. / Geoderma 139 (2007) 127–133

used sand for covering the second half of the stick (Fig. 4). Itwas only when termite found belowground clay that sheetingson the bridge-wood were replaced and/or consolidated with clay(Fig. 5a, b). At the end of the experiment, sheetings covering thesoil were collected. Fig. 6 indicated that they were mainly builtwith belowground clay.

4. Discussion

Our experimentation with a termite colony in the laboratorycan be seen as the best compromise between short timelaboratory experiments and field sample analyses. The colonyand the behaviour of termite workers were weakly disturbed andthe properties of soil that termites used for building theirsheetings were controlled. The main disadvantage is that we hadno access to the fungus-comb chamber walls that haveimportant functions in maintaining humidity and protectingexosymbiosis fungus and termites. Consequently, while fungus-comb chambers are sources of major care by termites, galleriesconstitute only temporary structures for foraging (Jouquet et al.,2002a).

4.1. Influence on clay properties

Among soil organisms, fungus-growing termites play animportant role in the dynamics of clays in tropical ecosystems.There are many studies that show that there is a higherproportion of clays in the termite-built structures (see Holt andLepage, 2000 for a review). Using laboratory experiments,Jouquet et al. (2002a,b) found not only an enrichment in claywithin the nest due to termite selection, but also a modificationof clay properties by termite action on 2:1 minerals with thecreation of smectite layers with small charges. In our currentstudy, termites increased the content of PCI at the expense ofWCI in building sheetings. According to Lanson (1998), PCIcan be considered as a highly illite phase with some (b5%)smectite layers, while WCI is a pure illite. More recentlyMeunier and Velde (2004) brought forward that WCI representscrystallites of greater than about 13–15 coherent diffractingdomains while PCI lies approximately between 8 and 10.Hence, our results stressed a slight but significant weatheringeffect of termites on the mineralogy of silicate clays through the

increase of the proportion of smectite layers and/or the decreaseof the number of layers in the crystallites.

This impact of P. spiniger on clay mineralogy was onlydemonstrated for sheetings and no difference was found betweenthe control clay-soil and the galleries. As discussed by Jouquetet al. (2002b), the effect of termites on clay varies according to thekind of constructions. These authors found a greater biologicalvermiculization (sensu Hinsinger, 1990) in the fungus-combchamber walls built by Odontotermes n. pauperans than in thegalleries. Although the impact of P. spiniger on the wall of thefungus-comb chamber was not identified in our current study,these results suggest species- and construction-specific effects oftermites on clay minerals.

The mineralogical alteration by termites could be explainedby the release of potassium to the outer solution (Meunier andVelde, 2004). This could be explained by either a direct effect oftermite saliva, either an indirect stimulation of microflora withsaliva or litter, or by a combination of these. Termite handlingcould also increase the contact area with soil and thus enhanceexchanges between clays and substrates incorporated bytermites. The transformation of illite into other mineralscontaining less potassium is observed in various types of soil-forming environments (Meunier and Velde, 2004). Illiteoccurring in soils is often found to be unstable in studies ofsoil genesis, being transformed into vermiculites (Wilke et al.,1984; Koch et al., 1992) or interstratified illite–smectites(Hughes et al., 1994) in soil profiles. However, the reactionobserved in our experiment appeared to take place on a muchfaster timescale than is normally associated with geologicalprocesses. Termites can thus be considered as accelerated agentsof clay alteration in tropical ecosystems. Hence, models thatconsider the dynamic of the illite-to-smectite transformationshould take into account the activity of termites and other soilengineers (sensu Jones et al., 1994; Jouquet et al., 2006).

4.2. Influence on SOM content

Characteristics that affect the dynamic of soil organic matter(SOM) in soil are considered to be mainly climate, soilaggregation, quality of the vegetation (litter), and the diversityand abundance of decomposers (microorganisms, microfauna).Despite their ecological importance, the function of termite-built structures in the SOM cycling in tropical ecosystemsremains poorly documented. In situ field analyses clearlyshowed that SOM content in constructions of fungus-growingtermites is highly variable, being similar (Robinson, 1958; Fallet al., 2001), higher (Watson, 1976; Gupta et al., 1981; Abbadieand Lepage, 1989; Jouquet et al., 2003), or lower (Arshad et al.,1988; Garnier-Sillam, 1991; Brauman et al., 2000; Contour-Ansel et al., 2000; Fall et al., 2001; Jouquet et al., 2004) thanthat in the bulk soil. Our experiment clearly showed thattermites are able to modulate the quantity of SOM that wasadded for building sheetings and galleries, depending on theoriginal soil types. Jouquet et al. (2002a) obtained a similarconclusion in a laboratory experiment and concluded thattermites are able to modulate the incorporation of SOM (viatheir saliva) according to the nature of the soil used and to the

132 P. Jouquet et al. / Geoderma 139 (2007) 127–133

type of construction (galleries vs. fungus-comb chamber walls)and probably according to the type of species. Our resultsindicated that no difference occurred in fine between sheetingsand galleries. However, the lower carbon and nitrogen contentsin the sheetings built from clay are surprising and could indicatea priming effect (sensu Bingemann et al., 1953), i.e., an increasein SOM mineralization after the addition of fresh organic matter(saliva). Priming effect is mainly considered to be induced bywater-soluble organic leachates percolating from the above-ground vegetation and leaf litter, and by root exudates (Lavelleand Spain, 2001). It has also been suggested that earthwormscan stimulate microbial activity through their cutaneous andintestinal mucus (Barois and Lavelle, 1986; Lavelle and Gilot,1994). From our experiment, we assume that fungus-growingtermites are also important regulators of soil organic matterdecomposition through their capacities for initiating primingeffects, creating patches of high recycling of nutrients.

4.3. Linking termite behaviour and soil translocation

Surface sheetings to soil translocation may, in manysituations, exceed the contribution of mound construction. InKenya, the quantity of soil material accumulated in sheetings byP. spinigerwas estimated about 1300 kg ha−1 year−1 (Kooymanand Onck, 1987). This study is the first to describe thebehaviour of termites and how they go deeply (only 10 cmdepth in our study but certainly far more in the field) toselectively collect clay and to bring it up to the soil surface forbuilding their sheetings. While termites were able to use bothclay and sand, they foraged in the soil for clay to bring up. Thisclay was used with a high preference for covering andreinforcing their constructions (sheetings on the wood). Thisbehaviour underlines the importance of termites in thedynamics, not only in transformation but also of translocation,of clays in tropical ecosystems. Especially in sandy soils, asmall but localized increase of clay could be of majorimportance in term of soil fertility.

The impact of termites on soils is closely related to theirecological requirements (Jouquet et al., 2006). A large number ofmound-building and subterranean termites forage on the soilsurface and, in order to protect themselves from desiccation andpredation, construct extensive surfaces of protective soil sheet-ings. The preference of termites for clay can be explained byeconomic principles. As demonstrated by Jouquet et al. (2002a),termites modulate the incorporation of supplementary material(i.e., saliva) according to the type of the soil used. The moretermites prefer a substrate (clay-soil in our study), the less theymust incorporate C and N. Clay-soil is probably a better substratein term of both stability (clay-sheetings are muchmore stable thansheetings produced with sands, data not show) and cost (less Cand N were incorporated). Some small aggregates made withgreen clay were also found associated to a fungus-comb in thebasin (data not shown). This means that clay, available in theboxes, has been collected, brought back inside the colony andassociated on a fungus-comb. One can therefore question if claycould also have a positive role in the growth of the symbioticfungus, for example, in enhancing the nutrient content.

Acknowledgements

We would like to thank Bruce Velde and Daniel Benest fortheir constructive comments and suggestions. We are alsograteful to the two anonymous reviewers who provided helpfulsuggestions on the draft manuscript. This project is financiallysupported by the Institute of Research for Development (IRD).

References

Abbadie, L., Lepage, M., 1989. The role of subterranean fungus-comb chambers(Isoptera, Macrotermitinae) in soil nitrogen cycling in a preforest savanna(Côte d'Ivoire). Soil Biol. Biochem. 21, 1067–1071.

Arshad, M.A., Schnitzer, M., Preston, C.M., 1988. Characterization of humicacids from termite mounds and surrounding soils, Kenya. Geoderma 42,213–225.

Augusto, L., Ranger, J., Turpault, M.P., Bonnaud, P., 2001. Experimental in situtransformation of vermiculites to study the weathering impact of tree specieson the soil. Eur. J. Soil Sci. 52, 81–92.

Badraoui, M., Bloom, P.R., Delmaki, A., 1992. Mobilization of non-exchangeable K by ryegrass in five Moroccan soils with and withoutmica. Plant Soil 140, 55–63.

Banfield, J.F., Barker, W.W., Welch, S.A., Taunton, A., 1999. Biological impacton mineral dissolution: application of the lichen model to understandmineral weathering in the rhizosphere. Proc. Natl. Acad. Sci. U. S. A. 96,3404–3411.

Barker, W.W., Welch, S.A., Banfield, J.F., 1997. Biogeochemical weathering ofsilicate minerals. In: Banfield, J.F., Nealson, K.H. (Eds.), Geomicrobiology:Interactions BetweenMicrobes and Minerals. Reviews inMineralogy, vol. 35.Mineral. Soc. Am., Washington, DC, pp. 391–428.

Barois, E., Lavelle, P., 1986. Changes in respiration rate and somephysicochemical properties of a tropical soil during transit throughPontoscolex corethrurus (Glossoscolecidae, Oligochaeta). Soil Biol. Biochem.18, 539–541.

Bingemann, C.W., Varner, J.E., Martin, W.P., 1953. The effect of the addition oforganic materials on the decomposition of an organic soil. Proc. Soil Soc.Am. 17, 34–38.

Boyer, P., 1982. Quelques aspects de l'action des termites du sol sur les argiles.Clay Miner. 17, 453–462.

Brady, N.C., Weil, R.R., 1999. The Nature and Properties of Soils, Twelfthedition. Prentice Hall. 881pp.

Brauman, A., Bignell, D.E., Tayasu, I., 2000. Soil feeding termites: biology,microbial associations and digestive mechanisms. In: Abe, T., Bignell, D.E.,Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology.Kluwer Academic Publishers, Dordrecht, pp. 233–259.

Contour-Ansel, D., Garnier-Sillam, E., Lachaux, M., Croci, V., 2000. Highperformance liquid chromatography studies on the polysaccharides in thewalls of the mounds of two species of termite in Senegal, Cubitermesoculatus and Macrotermes subhyalinus: their origin and contribution tostructural stability. Biol. Fertil. Soils 31, 508–516.

Fall, S., Brauman, A., Chotte, J.L., 2001. Comparative distribution of organicmatter in particule and aggregate size fractions in the mounds of termiteswith different feeding habits in Senegal: Cubitermes niokoloensis andMacrotermes bellicosus. Appl. Soil Ecol. 17, 131–140.

Garnier-Sillam, E., 1991. Comparative physico-chemical properties of soil-feeding Thoracotermes macrothorax and fungus-growing Macrotermesmülleri termite mounds. Biogeochemistry 48, 7–13.

Gupta, S.R., Rajvanshi, R., Singh, J.S., 1981. The role of the termite Odonto-termes gurdaspurensis (Isoptera: Termitidae) in plant decomposition in atropical grassland. Pedobiologia 22, 254–261.

Holt, J.A., Lepage,M., 2000. Termite and soil properties. In: Abe, T., Bignell, D.E.,Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbiosis, Ecology.Kluwer Academic Publishers, Dordrecht, pp. 389–407.

Hinsinger, P., 1990. Action des racines sur la libération du potassium etl'altération de minéraux silicatés—incidences agronomiques. Thèse deDoctorat, Ecole Nationale Supérieure Agronomique de Montpellier.

133P. Jouquet et al. / Geoderma 139 (2007) 127–133

Hinsinger, P., Jaillard, B., Dufey, J.E., 1992. Rapid weathering of a trioctahedralmica by the roots of ryegrass. Soil Sci. Soc. Am. J. 56, 977–982.

Hinsinger, P., Elsass, F., Jaillard, B., Robert, M., 1993. Root-induced irreversibletransformation of a trioctahedral mica in the rhizosphere of rape. J. Soil Sci.44, 535–545.

Hughes, R.E., Moore, D.M., Glass, H.D., 1994. Qualitative and quantitativeanalysis of clay minerals. Quantitative methods in soil mineralogy:proceedings of a symposium held in San-Antonio, Texas, USA, October23–24, pp. 330–359.

Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystemengineers. Oikos 69, 373–386.

Josens, G., 1972. Etude biologique des termites (Isoptères) de la savane deLamto-Pakobo (Côte d'Ivoire). PhD thesis, Université Libre de Bruxelles,Bruxelles, 285 pp.

Jouquet, P., Lepage, M., Velde, B., 2002a. Termite soil preferences and particleselections: strategies related to ecological requirements. Insect Soc. 49, 1–7.

Jouquet, P., Mamou, L., Lepage, M., Velde, B., 2002b. Effect of termites on clayminerals in tropical soils: fungus-growing termites as weathering agents.Eur. J. Soil Sci. 53, 521–527.

Jouquet, P., Mery, T., Rouland, C., Lepage, M., 2003. Modulated effect of thetermite Ancistrotermes cavithorax (Isoptera, Macrotermitinae) on soilproperties according to the structures built. Sociobiology 42, 403–412.

Jouquet, P., Tessier, D., Lepage, M., 2004. The soil structural stability of termitenests: role of clays in Macrotermes bellicosus (Isoptera, Macrotermitinae)mound soils. Eur. J. Soil Biol. 40, 23–29.

Jouquet, P., Barré, P., Lepage, M., Velde, B., 2005. Impact of subterraneanfungus-growing termites (Isoptera, Macrotermitinae) on soil properties in aWest African savanna. Biol. Fertil. Soil 41, 365–370.

Jouquet, P., Dauber, J., Lagerlof, J., Lavelle, P., Lepage, M., 2006. Soilinvertebrates as ecosystem engineers: intended and accidental effects on soiland feedback loops. Appl. Soil Ecol. 32, 153–164.

Koch, C.B., Bentzon, M.D., Larsen, E.W., Borggaard, O.K., 1992. Claymineralogy of two Ultisols from Central Kalimantan, Indonesia. Soil Sci.154, 158–167.

Kooyman, C., Onck, R.F.M., 1987. The interactions between termite activity,agricultural practices and soil characteristics in Kisii District, Kenya.Agricultural University Wageningen Papers. 120 pp.

Landeweert, R., Hoffland, E., Finlay, R.D., Kuyper, T.W., van Breemen, N.,2001. Linking plants to rocks: ectomycorrhizal fungi mobilize nutrientsfrom minerals. TREE 16, 248–254.

Lanson, B., 1990. Mise en évidence des mécanismes réactionnels desinterstratifiés illite/smectite au cours de la diagénèse. PhD thesis, UniversitéParis 6-Jussieu, France, 366 pp.

Lanson, B., 1998. Decomposition of experimental X-ray diffraction patterns(profile fitting): a convenient way to study clay minerals. Clays Clay Miner.45, 132–146.

Lanson, B., Velde, B., 1992. Decomposition of X-ray diffraction patterns: aconvenient way to describe complex I/S diagenetic evolution. Clays ClayMiner. 40, 629–643.

Lavelle, P., Gilot, C., 1994. Priming effects of macroorganisms on microflora: akey process of soil function? In: Ritz, K., Dighton, J., Giller, K.E. (Eds.),Beyond the Biomass. John Wiley and Sons, Chichester, pp. 173–180.

Lavelle, P., Spain, A.V., 2001. Soil Ecology. Kluwer Academic Publishers,Dordrecht, Netherlands. 654 pp.

Leprun, J.C., Roy-Noël, J., 1976. Minéralogie des argiles et répartition des nidsépigés de deux espèces du genre Macrotermes au Sénégal occidental(Presqu'île du Cap-Vert). Insect Soc. 23, 535–547.

Mahaney, W.C., Zippin, J., Milner, M.W., Sanmugadas, K., Hancock, R.G.V.,Aufreiter, S., Campbell, S., Huffman, M.A., Wink, M., Malloch, D., Kalm,V., 1999. Chemistry, mineralogy and microbiology of termite mound soileaten by the chimpanzees of the Mahale Mountains, Western Tanzania.J. Trop. Ecol. 15, 565–588.

Meunier, A., Velde, B., 2004. Illite. Springer. 286pp.Needham, S.J., Worden, R.H., McIlroy, D., 2004. Animal–sediment interac-

tions: the effect of ingestion and excretion by worms on mineralogy.Biogeosciences 1, 113–121.

Pernes-Debuyser, A., Pernes, M., Velde, B., Tessier, D., 2003. Soil mineralogyevolution in the INRA 42 plots experiment (Versailles, France). Clays ClayMiner. 51, 577–584.

Robert, M., Berthelin, J., 1986. Role of biological and biochemical factors insoil mineral weathering. In: Huang, P.M., Schnitzer, M. (Eds.), Interactionsof Soil Mineral with Natural Organics and Microbes, Special PublicationNumber 17. Soil Sci. Soc. Am., Madison, WI, pp. 453–495.

Robinson, J.B.D., 1958. Some chemical characteristics of ‘termite soils’ inKenya coffee fields. J. Soil Sci. 9, 58–65.

Velde, B., 1995. Origin and Mineralogy of Clays: Clays and the Environment.Springer-Verlag, Berlin. 334 pp.

Watson, J.P., 1976. The composition of mounds of the termite Macrotermesfalciger (Gerstäcker) on soil derived from granite in three rainfall zones ofRhodesia. J. Soil Sci. 27, 495–503.

Wilke, B.M., Mishra, V.K., Rehfuess, K.E., 1984. Clay mineralogy of a soilsequence in slope deposits derived from Hauptdolomit (dolomite) in theBavarian Alps. Geoderma 32, 103–116.