Geoderma 158 (2010) 233–241

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Termite bioturbation effects on electro-chemical properties of Ferralsols in the UpperKatanga (D.R. Congo)

B.B. Mujinya a,b, E. Van Ranst a,⁎, A. Verdoodt a, G. Baert c, L.M. Ngongo b

a Laboratory of Soil Science, Department of Geology and Soil Science (WE13), Faculty of Sciences, Ghent University, Krijgslaan 281/S8, B-9000 Gent, Belgiumb Laboratory of Soil Science, Faculty of Agronomical Sciences, University of Lubumbashi, P.O. Box: 1825, Lubumbashi, Congoc Department of Plant Production, University College Ghent, Schoonmeersstraat 52, B-9000 Gent, Belgium

⁎ Corresponding author. Tel.: +32 92644626; fax: +E-mail address: eric.vanranst@UGent.be (E. Van Ran

0016-7061/$ – see front matter © 2010 Elsevier B.V. Aldoi:10.1016/j.geoderma.2010.04.033

a b s t r a c t

a r t i c l e i n f o

Article history:Received 12 November 2009Received in revised form 14 April 2010Accepted 30 April 2010Available online 3 June 2010

Keywords:TermitesFerralsolsBioturbationElectro-chemical propertiesD.R. Congo

Although the significant impact of mound-building termites on physical, chemical and biochemical soilproperties over large areas of the (sub-) tropics has often been discussed, little is known about the influenceof termites on electro-chemical properties of Ferralsols. In this study, we compared the curves describing thetotal cation exchange capacity (CECT), the base cation exchange capacity (CECB), and the anion exchangecapacity (AEC) across a range of pH values (charge fingerprint) and point of zero charge (pH0) ofMacrotermesfalciger biogenic structures with soils not affected visually by termites (control soils). The results show thattermite activities lowered considerably the pH0 values, the actual AEC, the actual preferential adsorption ofAl on the exchange complex (CECT–CECB) and the AEC variability (dAEC/dpH); and increased considerablythe soil pH, the cation exchange capacities (CECB and CECT), the permanent negative charge (σp) and theCEC's variability (dCECB/dpH and dCECT/dpH). The lowering of pH0 values (1.6-fold) was attributed to thebonding of negatively charged organic matter with protonated oxide sites and largely to the enrichment inpermanent negative charge (about 2-fold), suggesting the termites' ability to change soil mineralogicalproperties. The mean pH0–pH0.002 values indicate the evolution of negative (−2.0 to −3.6 units) andpositive (+0.6 units) charges on the variable charge components of mound and control soils, respectively.The study demonstrates that Macrotermes biogenic structures have a mixed charge system with higherpermanent and variable charges than the surrounding Ferralsols.

32 92644997.st).

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© 2010 Elsevier B.V. All rights reserved.

1. Introduction

The presence of 3 to 5 dome-shaped (8 m in height; 15 m in width)termite mounds per hectare is one of the main features of the miombolandscape around Lubumbashi in southern D.R. Congo (Sys, 1957). Thefungus-growing termite Macrotermes falciger (Isoptera, Macrotermiti-nae) is the main occupant of primary active termitaria and the originalbuilder of thesemassive fortress-style nests (Goffinet, 1976).Among thesoil organisms, termites of the sub-family Macrotermitinae, character-ized by an obligate mutualism with fungus (Termitomyces sp), play aprimary role in tropical ecosystems (Holt and Lepage, 2000). Theimpressive ability of fungus-growing termites to regulate their nestenvironments as agriculturalists is also testament to their skills asarchitects (Korb, 2007). Termites are very vulnerable insects thatprotect their colonies by improving soil structural stability againstwaterflux or intrusion of soil invertebrate predators into the nests (Jouquetet al., 2004, 2006). Through their mound-building activities, termitesinevitably cause regional translocation of soil (Lepage and Darlington,

2000) leading to the development of distinctive patches in localecosystems, which contributes to ecological diversity (Lavelle et al.,1992). This is the reasonwhy termites are considered as “soil ecosystemengineers” (Jouquet et al., 2006). Soils handled by termites are oftenenriched in mineral nutrients such as ammonium and nitrate, inexchangeable basic cations, and in some cases in available phosphorus,and have a more alkaline pH (Brauman et al., 2000; Holt and Lepage,2000; López-Hernández et al., 2006; Brossard et al., 2007). Theproportion of organic matter and clay in the termite-built structures isalways greater than that in the bulk soil (Brauman et al., 2000; Jouquetet al., 2002; Jouquet et al., 2007) and conspicuous differences have alsobeen observed in their mineralogical properties (Boyer, 1982;Mahaneyet al., 1999). Consequently, the termite mounds are islands of higherchemical fertility within a chemically poor soilscape mostly dominatedby Ferralsols. Moreover, Ferralsols have a low and pH-dependent cationexchange capacity (CEC) because they are dominated by low-activityclays (mainly kaolinite) and sesquioxides (Yu, 1997; Qafoku et al.,2004). Up to the present, the influence of termite activity on the CEC hasbeen examined using mostly routine analyses (Jouquet et al., 2004;Mora et al., 2003; Brossard et al., 2007). However, to fully appreciate theimpact of termite activity on surface chargeproperties of variable chargesoils, a more appropriate methodology is needed. Measurements of

234 B.B. Mujinya et al. / Geoderma 158 (2010) 233–241

surface charge for soil particles must account explicitly for the diversityand conditional nature of the principal components (intrinsic, perma-nent structural and net proton surface charge density) that contribute tothis quantity (Chorover and Sposito, 1995; Sposito, 2008). In addition,the point of zero charge of the variable charge components (pH0) ofFerralsols is considered to be of fundamental significance because itsposition on the pH scale has great influence on the cation and anionexchange capacities of such soils (Gillman, 1985). This importantsurface property is often measured by potentiometric titration. At thepH0, there are equal numbers of protonated and deprotonated sites, andhence equal amounts of negative and positive variable charges, so thatsolution pH shows no change with electrolyte concentrations (ionicstrength). The latter point was aptly termed the point of zero salt effect,PZSE (Parker et al., 1979; Gillman, 2007; Sposito, 2008). Although theelucidation of the mechanisms by which electrical charge develops onsoil particle surfaces has been an active area of soil science research inrecent years (Gillman, 2007), the impact of termite building activity onsoil electro-chemical properties remains poorly investigated. Surfacecharge properties directly or indirectly control a range of physico-chemical reactions in soils (retention of exchangeable cations andanions, soil acidity, plant nutrient availability, soil water characteristics,etc.) (Qafoku et al., 2004; Gillman, 2007). However, so far, informationon surface charge properties of termite biogenic structures, such as theamounts of permanent and variable charges (sign and magnitude), thevariability of negative and positive surface charges, and the point of zerocharge of the variable charge components (pH0), is not available and,consequently, our knowledge on the possible role of termite-builtstructures as soil amendments is still very scarce.

This study investigated the effects of fungus-growing termites onsurface charge properties of Ferralsols in the Upper Katanga (D.R.Congo) applying the charge fingerprinting procedures (Gillman, 2007).The aim was to assess the impact of termite actions on the pH0, on theproportion of permanent and variable charges, and on the variabilityof surface charge components.

2. Materials and methods

2.1. Environmental setting

The study was conducted in the northeastern part of theLubumbashi region (Upper Katanga, D.R. Congo), located betweenabout 11°34′–11°37′S latitude and 27°28′–27°30′ E longitude. ThreeFerralsols derived from representative parent rocks in the regionwereselected for the present investigation. Site descriptions are summa-rized in Table 1. Pedons at site 1 and 3, derived respectively fromKakontwe and stratified dolomite, are characterized by red (2.5 YR 5/6 moist), deep, clayey or sandy clayey, well drained soils. The pedonsat site 2, derived from conglomerate, are characterized by yellowish-red (5 YR 5/6 moist), deep, sandy clayey, well drained soils (Sys andSchmitz, 1959). Fire is a very important factor in the miomboecosystem around Lubumbashi. Miombo is generally regarded assecondary growth, largely occurring after destruction of the dry

Table 1General information on the sites and classification of the selected pedons.

Site 1 Site 2 Site 3

Coordinates S 11° 36′1.1″ S 11° 35′ 34.0″ S 11° 34′18.18″E 027° 29′7″ E 027°28′47″ E 027° 29′2″

Parent rocks Kakontwe dolomite Conglomerate Stratified dolomiteINEACa Red Latosol Yellowish–red Latosol Red LatosolWRB, 2006b Rhodic Ferralsol Rhodic Ferralsol Rhodic FerralsolElevation 1281 m 1304 m 1323 mSlope positionc Lower slope Upper slope Crest or summit

a Sys and Schmitz (1959).b FAO (2006a).c FAO (2006b).

evergreen forest (Fanshawe, 1971). A second typical characteristic ofmiombo is the presence of large, sparsely distributed (3 to 5/ha)termite mounds, reaching 8 m in height and 15 m in width, andcovering about 4.3 to 7.8% of the miombo (Sys, 1957). The climate ofLubumbashi is characterized by one rainy season (November toMarch), one dry season (May to September), and two transitionmonths (October and April). July and August are always dry. Averageannual rainfall is about 1270 mm and the rainy season usually lasts118 days. The relative air humidity follows the rainfall pattern with aminimum in October and amaximum in February. The average annualtemperature is about 20 °C.

2.2. Mound and soil sampling

At each sampling site, one representative epigenous mound builtby termite species of the genus Macrotermes (Macrotermitinae) wasidentified. As illustrated in Fig. 1, a hole of ±7 m height/depth and±1.25 m width, extending from the top of the mound down throughthe different epigeal parts (outer crust, inner section and central‘hive’) into the mound foot has been manually dug through eachtermite mound. Hand drillings have also been executed at each of thethree sites approximately 7 m away from the termite mound (Fig. 1)in soils without noticeable termite activity (control soils). Bulk soilsamples were collected in the central hive, chamber walls and moundfoot of each of the termite mound profiles and in the control soils (at adepth of about 50 cm) for physico- and electro-chemical analyses.Sample description is summarized in Table 2.

2.3. Laboratory procedures

Analyses were performed on air-dried soil fractions (b2 mm). Thesand fraction (N63 µm) was separated by wet sieving; the silt and clayfractionswere determined by successive sedimentation after dispersionwith a solution of Na2CO3. The soil pHwasmeasured potentiometricallyin a 1:2.5 (W/V) suspension of H2O and 1 M KCl. Organic carboncontents (Corg, Walkley and Black), CEC and exchangeable basic cationsCa2+,Mg2+, K+ andNa+ (1 MNH4OAc at pH 7)were determined usingthe procedure outlined by Van Ranst et al. (1999). Dithionite–citrate–bicarbonate (DCB) extractable Fe and Al were determined according toMehra and Jackson (1960)andbyusingatomic absorption spectrometry(AAS) for quantification. The charge fingerprints, which are curvesdescribing the total cation exchange capacity (CECT), base cationexchange capacity (CECB), and anion exchange capacity (AEC) across arange of pH values, at solution ionic strength approximating fieldconditions, were determined using the methodology described byGillman (2007). In short, soils were Ca2+ saturated and brought toequilibrium in a 0.002 M CaCl2 matrix. Suspension pHwas adjusted to 6values ranging from approximately 3 to 7 and exchangeable Ca2+, Al3+

and Cl− displaced with 1 M NH4NO3. Ca2+ and Al3+ were measured byAAS and Cl− was determined with a chloride analyser. The CECB isoperationally defined as the Ca2+ adsorbed, CECT as the Ca2+ and Al3+

adsorbed, and the AEC, as the Cl− adsorbed. The point of zero charge ofthe variable charge components (pH0), also known as the point of zerosalt effect (PZSE), was estimated during the charge fingerprintingprocedure by identifying the point where changing the solution ionicstrength does not produce a corresponding change in solution pH(Gillman, 2007). The amount of permanent surface charge (σp),referring to any excess of CECT over AEC, or vice versa at pH0, was alsoestimated from the charge fingerprint (Gillman, 2007).

2.4. Statistical analyses

A Principal Component Analysis (PCA) was performed on the dataset consisting of 15 physical, chemical and electro-chemical variablesto discriminate control soils and different biogenic structures of thethree sampling sites. The effects of termites' activities on soil surface

Fig. 1. Schematic representation of the sampling strategy.

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charge properties were tested by means of a one-way ANOVA with“sampling units” as factor, and means were compared using theFisher's protected least significant difference (Fisher's PLSD) test.Correlation analyses were tested among selected soil properties bymeans of Pearson's correlation coefficient. All statistical calculationswere carried out using Statistica 7.1 for Windows and tests wereperformed at the 0.05 significance level. Curves associated with thecharge fingerprints were fitted and smoothed using Microsoft Excel'sfitting functions for Windows Vista.

3. Results and discussion

3.1. Multivariate analysis

The PCA analysis is presented in Fig. 2a and b. Only the first twoaxes of the PCA, which explained 64.83% of the total variance, were

Table 2Samples description.

Site Sampling units Symbol

Ferralsols derived from Kakontwe dolomite (K) Central hive (CH) KCHChamber wall (CW) KCWMound foot (MF) KMFControl soil KCS

Ferralsols derived from conglomerate (C) Central hive (CH) CCHChamber wall (CW) CCWMound foot (MF) CMFControl soil (CS) CCS

Ferralsols derived from stratified dolomite (D) Central hive (CH) DCHChamber wall (CW) DCWMound foot (MF) DMFControl soil (CS) DCS

retained for further analyses. Fig. 2a presents the correlation circle ofthe two axes. Axis 1 (47.38% of the total variability) discriminated soilsamples with high pH0, pH0–pH, ΔpH and sand content in oppositionto those samples with high CECB, σp, pH0.002, exchangeable basiccations (Ca2+, Mg2+ and K+) and clay content. Axis 2 (17.45% of thetotal variability) separated soil samples with high Corg, exchangeableNa+ and silt content from those with high AEC. This shows thatdifferences between sampling units were mainly explained bysurface charge variables which are correlated to axis 1. Projection ofsamples on the plane defined by the first two PCA axes clearlydifferentiated biogenic structures from the control soils and discrim-inated 3 groups (Fig. 2b). The first group (group a) was composed ofcontrol soils (CCS, KCS and DCS) characterized mainly by low CECB,σp, pH0.002 and high pH0 in comparison to the groups composed ofbiogenic structures (b and c). The biogenic structures built onFerralsols derived from conglomerate (group b) segregated from allthe other termite mound samples (group c) as a result of theirparticularly low pH0.002. All biogenic structures built on Ferralsolsderived from dolomitic parent rocks (group c) were characterized byhigh exchangeable Ca2+, Mg2+ and to a smaller extent K+. Theordination of sampling units on the plane defined by axes 1 and 2showed variation in surface charge properties essentially determinedby the influence of termite building activities, and this trend wasevident for all sampling sites.

3.2. Termite bioturbation effects

The physico- and electro-chemical data (mean values and standarderrors) for termite biogenic structures and control soil are presented inTables 3–5.

Fig. 2. Principal Component Analysis (PCA) on 15 physical, chemical and electro-chemical properties of mounds and control soils. (a) Correlation circle; (b) Projection ofsampling units on the plane defined by the axes 1 and 2.

Table 3Selected physical and chemical properties of termite biogenic structures and controlsoil. (n=3, S.E in parentheses).

Properties Sampling units

Central hive Chamberwall

Mound foot Control soil

Particle size distribution (%)Clay 46 (6.44)a 48 (3.33)a 49 (3.89)a 39 (6.47)aSilt 27 (1.36)a 30 (1.81)a 28 (2.94)a 28 (4.30)aSand 27 (5.28)a 23 (2.05)a 23 (0.95)a 33 (5.15)a

SBC (cmolc kg−1) 14.6 (5.47)a 13.9 (2.60)a 8.7 (2.13)ab 0.7 (0.45)bCECpH7(cmolckg−1) 12.0 (1.09)a 13.2 (1.30)a 12.1 (0.81)a 8.4 (0.43)b

Soil pHH2O 6.4 (1.39)a 7.0 (0.81)a 5.6 (0.84)a 5.0 (0.01)aKCl 5.8 (1.24)a 6.2 (0.81)a 4.9 (0.82)a 4.5 (0.31)aΔpH (KCl–H2O) −0.6 (0.18)a −0.7 (0.04)a −0.7 (0.10)a −0.5 (0.31)a

Corg (%) 0.2 (0.07)a 1.2 (0.23)a 0.7 (0.28)a 0.7 (0.49)aAlDCB (%) 0.4 (0.13)a 2.3 (0.44)a 1.4 (0.54)a 1.3 (0.93)aFeDCB (%) 0.63 (0.18)a 3.3 (0.63)a 2.0 (0.77)a 1.9 (1.33)a

Mean values with the same letter are not significantly different (Pb0.05).

Table 4pH0.002, point of zero charge (pH0), ΔpH and surface charge components (CECT, CECB,AEC, σp, CECT–CECB, CECT–AEC) at soil pH and pH0 for termite biogenic structures andcontrol soils. (n=3, S.E in parentheses).

Properties Sampling units

Central hive Chamberwall

Mound foot Control soil

pH0.002 6.7 (1.21)a 6.8 (0.73)a 5.9 (0.54)a 4.7 (0.15)apH0 3.3 (0.09)a 3.3 (0.06)a 3.3 (0.07)a 5.2 (0.66)bpH0–pH0.002 −3.4 (1.27)a −3.6 (0.68)a −2.6 (0.48)a 0.4 (0.79)b

At pH0

CECT (cmolc kg−1) 5.1 (0.40)a 5.1 (0.37)a 5.1 (0.20)a 2.7 (0.58)bAEC (cmolc kg−1) 0.2 (0.05)a 0.2 (0.03)a 0.1 (0.02)a 0.2 (0.03)aσp (cmolc kg−1) −4.9 (0.36)a −4.9 (0.39)a −5.0 (0.22)a −2.4 (0.55)b

At soil pHCECT (cmolc kg−1) 9.4 (2.46)a 9.6 (1.62)a 6.8 (0.77)a 2.4 (0.09)bCECB (cmolc kg−1) 9.0 (2.76)a 9.6 (1.62)a 6.7 (0.87)a 2.1 (0.18)bAEC (cmolc kg−1) 0.1 (0.01)a 0.1 (0.03)a 0.1 (0.01)a 0.5 (0.23)aCECT–CECB (cmolc kg−1) 0.4 (0.36)a 0.0 (0.00)a 0.1 (0.11)a 0.4 (0.27)aCECT–AEC (cmolc kg−1) 9.2 (2.45)a 9.5 (1.63)a 6.7 (0.77)a 2.0 (0.26)bσp/CECT (%) 59.8 (16.4)a 54.0(10.3)a 75.1(7.2)a 99.8(24.0)a

Mean values with the same letter are not significantly different (Pb0.05).

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3.3. Effect on soil pH

Compared to the control soil, the pH values in H2O, 1 M KCl and0.002 M CaCl2 of soil worked by termites (central hive, chamber walland mound foot) were higher (Tables 3 and 4), but statistically notsignificantly different (P=0.33). The pH values in 0.002 M CaCl2(pH0.002) of the central hive (6.7, S.E.: 1.21) and chamber wall (6.8, S.E.: 0.73) were neutral, those of the mound foot (5.9, S.E: 0.54) andcontrol soil (4.7, S.E.: 0.15)were acid (Table 4). Furthermore, the sumsof basic cations were 20.9, 19.9 and 12.4 times greater in the centralhive, chamber wall and mound foot, respectively, compared to thecontrol soil (Table 3). Thus the increased saturation status explainsthe trend of higher pH in the mound soil. This is in agreement withresults obtained by Jouquet et al. (2004). Accordingly, the values of pHin H2O, 1 M KCl and 0.002 M CaCl2 were all significantly (Pb0.05) andpositively correlated with the sum of basic cations (SBC) withcoefficients of determination (r) of 0.735, 0.741, and 0.816, respec-

tively. The ΔpH (KCl–H2O) did not discriminate (PN0.05) termitemound soils from control soils (Table 3).

3.4. Effect on the pH0

As evidenced in Table 4, termite actions had a significant(P=0.012) influence on soil pH0. The soil pH0 values of the centralhive (3.3, S.E.: 0.09), chamber wall (3.3, S.E.: 0.06) and mound foot(3.3, S.E.: 0.07) were lower than the control soil (5.2, S.E.: 0.66).Organic matter and sesquioxides have been reported to decrease andincrease pH0 values, respectively (Gillman, 1985; Van Ranst et al.,1998; Anda et al., 2008). Yet, the correlation analysis did not show anysignificant (PN0.05) interaction between pH0 and organic carbon(Corg) or DCB extractable Fe and Al. The mean Corg contents of thetermite mounds, being 0.2 (S.E: 0.07) % for the central hive, 1.2 (S.E.:0.23) % for the chamber wall and 0.7 (S.E.: 0.28) % for the mound foot,did not differ significantly (PN0.05) from those of the control soils(0.7%, S.E: 0.49), and thus Corg content played a negligible role in thepH0 shift. As the pH0 was significantly (r=0.6, P=0.037) correlatedwith the net permanent charge (σp), the low pH0 values (about 3.3) ofthe biogenic structures are partially attributed to the enrichment in

Table 5Surface charge components (CECT, CECB, and AEC), ratio of σp to CECT (%) at pH 4 and pH6, and exchange capacity variations/units pH for termite biogenic structures and controlsoils. (n=3, S.E in parentheses).

Sampling units

Central hive Chamber wall Mound foot Control soil

At pH 4CECT (cmolc kg−1) 5.79 (0.61) 5.73 (0.28) 5.17 (0.31) 2.12 (0.21)CECB (cmolc kg−1) 4.83 (0.73) 4.75 (0.24) 4.08 (0.38) 1.45 (0.14)AEC (cmolc kg−1) 0.17 (0.03) 0.13 (0.03) 0.16 (0.02) 0.66 (0.36)σp/CECT (%) 85.1 (5.32) 85.2 (2.77) 87.4 (0.59) 89.1 (20.2)

At pH 6CECT (cmolc kg−1) 7.66 (1.05) 7.96 (0.41) 7.32 (0.36) 3.25 (0.61)CECB (cmolc kg−1) 7.60 (1.07) 7.94 (0.41) 7.20 (0.30) 3.15 (0.63)AEC (cmolc kg−1) 0.10 (0.02) 0.08 (0.01) 0.07 (0.00) 0.23 (0.08)σp/CECT (%) 65.1 (6.07) 61.5 (3.96) 61.8 (3.31) 62.2 (17.2)

Exchange capacity variations/units pHdCECT/dpH 0.94 (0.22) 1.12 (0.14) 1.08 (0.16) 0.56 (0.28)dCECB/dpH 1.38 (0.17) 1.60 (0.17) 1.56 (0.17) 0.85 (0.31)dAEC/dpH 0.03 (0.02) 0.03 (0.01) 0.05 (0.01) 0.21 (0.14)

Fig. 3. Relationship between pH0–pH0.002 and CECB at soil pH (a), and CECT–AEC at soilpH (b) for termite mound soils.

Fig. 4. Average relative amounts of permanent and variables changes of control soil andbiogenic structures: central hive, chamber wall and mound foot (n=3).

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permanently charged clay minerals. This implies that the clay fractionof termite structures (central hive, chamber wall and mound foot)contains additional 2:1 type clay minerals which contribute topermanent charge density. This change in mineralogical propertiescan be explained by the bringing up of fine particles rather than amodification of these clay materials (Holt and Lepage, 2000; Jouquetet al., 2002; Jouquet et al., 2007). In addition, Corg content was verysignificantly (r=0.999, Pb0.001) and positively correlated with FeDCBand AlDCB contents. This would suggest that negatively chargedorganic matter was bonded to protonated oxide sites and this alsocauses pH0 to be lowered (Gillman, 1985). The pH0 values weresignificantly correlated with charge components interpolated at soilpH, negatively with the CECT (r=−0.62, P=0.032), and positivelywith the AEC (r=0.94, Pb0.001). Conversely, the high pH0 value ofthe control soil resulted in a significant high AEC at a pH wherebytermite mound fractions with lower pH0 have very small AEC(Table 4). The sign of (pH0–pH0.002) indicates the evolution of positiveand negative charges on the variable charge components (Gillman,1984). As summarized in Table 4, (pH0–pH0.002) provided significant(P=0.011) discrimination between the mounds and control soils.Whereas the control soil showed positive (pH0–pH0.002) values,averaging to +0.4 units (S.E.: 0.79), the central hive, chamber walland mound foot soil had strongly negative (pH0–pH0.002) valuesreaching −3.4 (S.E: 1.27), −3.6 (S.E: 0.68) and −2.6 (S.E.: 0.48)units, respectively. The considerable negative (pH0–pH0.002) values ofthe mound materials are in accordance with the high net negativecharges (9.2, 9.5 and 6.7cmolc kg−1, S.E.'s of 2.45, 1.63 and 0.77,respectively) at field conditions (Table 4). The small net negativecharge (2.0cmolc kg−1, S.E.: 0.26) of the control soils also consents tothe positive (pH0–pH0.002) value. Fig. 3 illustrates the significant(Pb0.01) exponential relationships, reported for the mound materi-als, between (pH0–pH0.002) values and net negative charge (CECT–AEC) and CECB interpolated at soil pH.

3.5. Effect on permanent charge

The amounts of permanent negative charge (σp), defined as theexcess of CECT over AEC at pH0, are listed in Table 4. All studiedsamples had a net negative permanent charge. The mean σp values ofthe central hive (−4.9 cmolc kg−1, S.E.: 0.36), chamber wall(−4.9cmolc kg−1, S.E.: 0.39), and mound foot (−5.0cmolc kg−1, S.E.:0.22) were very significantly (P=0.007) greater than the control soil(−2.4cmolc kg−1, S.E.: 0.55) in absolute value. However, the relation-ships between permanent and variable charge are of greater interestin these low-activity clay soils, especially as pH has changed (Gillman

and Sumpter, 1986). The ratios ofσp to CECT at soil pH, at pH4 and at pH6 are shown in Tables 4 and 5. At pH 4, the central hive, chamber walland mound foot samples develop, respectively, about 85.1 (S.E.: 5.32),85.2 (S.E.: 2.77) and 87.4 (S.E.: 0.59) % of their CECT from perma-nent negative charges. As the pH is raised to soil pH, the variable

Fig. 5. Average sum of basic cations of control soil and biogenic structures: central hive,chamber wall and mound foot (n=3).

Fig. 6. Charge fingerprints including pH0 and soil pH values for mound sampling units (

238 B.B. Mujinya et al. / Geoderma 158 (2010) 233–241

negative charge generated, aswell as the diminution of variable positivecharge, is enough to reduce the σp proportion to about 59.8 (S.E.:16.4),54.0 (S.E.: 10.3) and 75.1 (S.E.: 7.2) % of the CECT for the central hive,chamberwall andmound foot samples, respectively. These results wereunexpected since the mineralogical composition of Ferralsols isnormally dominated by variable charge constituents. The very signif-icant (r=0.99, Pb0.001) relationship between σp and the CECT at pH0

corroborates the high ratios (σp/CECT) observed at this pH for themound samples. Surrounding Ferralsols showed adifferent patternwiththeir pH0 well above soil pH indicating that the soil variable chargecomponents will be positively charged (Gillman, 1984). At pH 6, the σp

of the control soil constitutes about 62.2 (S.E.: 17.2) % of the CECT.Obviously, when pH is lowered to pH close to field conditions (4.7, S.E.:0.15) the generation of positive charge on variable charge surfaceswithin these control soils expands the σp contribution to about 99.81(S.E.: 20.2) % of the CECT (Table 4). At low pH (≤4.7), CECT valuesmeasured for some control soils were less than the σp quantified(99.81%, S.E.: 20.2), and according toGillman and Sumpter (1986) andGillman (2007) this phenomenon is associated with a relatively highAEC in highly oxidic soils. In this case some of the positive surfacecharge is balanced, not by adsorption of negatively charged diffuse

central hive, chamber wall and mound foot) and control soils on the 3 study sites.

Fig. 6 (continued).

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layer ions, but by repulsion of positively charged ions from the diffuselayer (Gillman, 2007). Thus, the low amounts of permanent negativecharge of the control soils are almost entirely responsible for theircapacity to retain cations (Fig. 4).

3.6. Effect on charge components

Fungus-growing termite mounds are known to have a greater CECthan the surrounding soils (Jouquet et al., 2004). This study gives thetotal CEC (CECT), basic CEC (CECB) and AEC values of Macrotermesmounds relative to control soils at field soil pH (Table 4). The CECB,which provides valuable information on the soil's ability to hold theagronomically important basic cations (Ca, Mg, and K) in an exchange-able form, discriminates very significantly (P=0.014) the mound fromthe control soils. Atfield soil pH, themeanCECB values of the central hive(9.0cmolc kg−1, S.E: 2.76), chamberwall (9.6cmolc kg−1, S.E: 1.62) andmound foot (6.7cmolc kg−1, S.E: 0.87) samples were all greater thanthose of the control soils (2.1cmolc kg−1, S.E: 0.18). The mean CECTvalues at soil pH were 4 times greater in the central hive and chamber

wall samples, and 3 times greater in the mount foot soil than in thecontrol soils. It is evident that themound soils are capable of holding andstoring far greater amounts of basic cations than the control soils. Theextremely low CECB values of the control soils imply that most appliednutrient cations will not be retained, but will be lost by leaching(Gillman and Sinclair, 1987; Auxtero et al., 2004). The high CECT andCECB values recorded in the mound soils agree with their greateramounts of exchangeable basic cations compared to the controlsoil (Table 4 and Fig. 5). The dominant exchangeable basic cationswere Ca2+ and Mg2+, K+ was generally low, whereas Na+ was almostcompletely absent (Fig. 5). Conversely, the CECB values at field pHweresignificantly and positively correlated with the exchangeable Ca2+

(r=0.91,Pb0.001),Mg2+(r=0.78, P=0.003), K+ (r=0.65,P=0.022)contents, and with the sum of basic cations (r=0.97, Pb0.001).However, the sums of basic cations of mound materials extracted by1 MNH4OAc at pH 7 (Table 3) are higher than the CECB values (Table 4).It is probable, therefore, that basic cations not associatedwith exchangesites have been extracted with the 1 M NH4OAc method at pH 7 (VanRanst et al., 1998; Gillman, 2007). The difference between CEC–NH4OAc

240 B.B. Mujinya et al. / Geoderma 158 (2010) 233–241

at pH 7 and CEC at soil pH, rising with increasing amounts of variablecharge minerals (Baert and Van Ranst, 1998), implies that termitemound samples had a much greater amount of variable charge colloidsthan the control soils (Fig. 4). In contrast to the conclusions drawn byJouquet et al. (2004), our results showed that the soil of Macrotermesmoundshas amixed charge systemwithhigher permanent and variablecharges than the surrounding Ferralsols. The significantly comparable(PN0.05) Corg contents in mounds and control soils imply that thedifference in CEC reflects the impact of the mineralogical composition.Furthermore, the AEC of Ferralsols may be important in preventingleaching of anionic nutrients such as sulphate and nitrate; the positivechargemay have significant consequences for themanagement of thesesoils (Gillman, 1984, 2007). The capacities to retain anions werestatistically similar (PN0.05) for all sampling units (mounds and controlsoils). But, even at low pH, the mean AEC values were lower in biogenicstructures (0.1cmolc kg−1, S.E.'s of 0.01 and 0.03) compared to thecontrol soils (0.5cmolc kg−1, S.E.: 0.23) (Table 4). At field soil pH, theAEC values of the mound samples were significantly and negativelyrelated (r=−0.73, P=0.026) to the AlDCB or FeDCB contents. Thisnegative relationship is also associated to the bonding of negativelycharged organic matter with protonated oxide sites. Moreover, at fieldsoil pH, the combination of a low negative surface charge and a sub-stantial positive surface charge in the control soils leads to significantly(P=0.013) lower mean net negative charges (CECT–AEC at field-pH)compared to the biogenic structures: 2.0 (S.E.: 0.26)cmolc kg−1 vs. 9.2(S.E.: 2.45), 9.5 (S.E.: 1.63) and 6.7 (S.E.: 0.77)cmolc kg−1 (Table 4) forthe central hive, chamber wall and mound foot, respectively.

3.7. Charge variation with pH

The charge fingerprints including pH0 and soil pH values formound and control soils of each of the 3 sampling sites are presentedin Fig. 6. Termite bioturbation clearly affected the overall shapes of thecharge fingerprints. The fitted curves of the mound samples showstronger variations in CECB and CECT with pH than the control soils.Whereas, within the same experimental pH range, the fitted curves ofCECB and AEC of control soils show inverse relationships. Moreover, atlow pH, almost all the CECT curves of the mound soils (KCH, KCW,KMF, CCH, CCW, CMF, DCH, DCW and DMF in Fig. 6) are asymptotic tothe pH axis and this agrees perfectly with the significant amounts ofpermanent negative charge and low pH0 values in those samples(Gillman and Sumpter, 1986; Gillman, 2007). This behaviour wouldalso be expected from soils containing some 2:1 clay minerals. In thecontrol soils, however, the CECT curves continue to diminish withdecreasing pH (KCS, CCS, and DCS in Fig. 6). The dCEC/dpH and dAEC/dpH (Table 5) show a shift of negative or positive charge per unit pH,respectively. The mean dCECB/dpH values were clearly greater inMacrotermesmounds (1.6-, 1.9- and 1.8-fold for central hive, chamberwall and mound foot, respectively) than in the control soils. Com-pared to the surrounding Ferralsols, the mean dAEC/dpH values of allbiogenic structures were 5 times smaller. However, the differencebetween CECB and CECT is an expression of the amount of Al on theexchange complex despite efforts to saturate the soil with Ca (Gillmanand Sinclair, 1987). Fig. 6 shows that the extents of preferentialoccupation of CEC by Al at lower pH in the mound samples are minor.In all sampling sites the difference between CECT and CECB of termitestructures was smaller than in the control soils. The differencesbetween CECT and CECB decrease in the order: control soilNcentralhiveNmound footNchamber wall.

4. Conclusions

This study clearly demonstrated that fungus-growing termites havea great influence on surface charge properties of Ferralsols. Throughtheir building activities, they lower significantly the pH0. Mean pH0

valueswere1.6 times lower in the termite biogenic structures compared

to the surrounding soils. The insignificant (PN0.05) difference in Corgcontent between mound and control soils coupled to the considerable(P=0.007) enrichment in permanent negative charge (about 2 times)within themounds soils, suggests that the lowpH0 (3.3) in termite-builtstructures can be principally attributed to the considerable amount ofpermanently charged 2:1 clay minerals. The very significant (Pb0.001)relationship between Corg and AlDCB or FeDCB content suggests that thebonding of negatively charged organic matter with protonated oxidesites also contributed to the lowering of pH0. Whereas, in the controlsoils, the mean difference between pH0 and actual soil pH0.002 waspositive (+0.4 units); the mound soils exhibited significant negative(pH0–pH0.002) values (−2.6 to−3.6 units). Termite mound soils had amuch greater (3.2 to 4.6-fold) actual capacity to hold nutrient basiccations (CECB) and lower (5-fold) actual AEC compared to the controlsoils. In the termite-built structures, the shifts of negative (dCECB/dpH)and positive (dAEC/dpH) charges per unit pH were, respectively, 1.6 to1.9 times greater and 4.2 to 7 times lower compared to the control soils.This study demonstrates that Macrotermes mound soils have a mixedcharge system with higher permanent and variable charges than thesurrounding Ferralsols.

Acknowledgements

This study was funded by the project G.0011.10 N of the Fund forScientific Research (Flanders), and by the project ZRDC2008MP059 ofthe Flemish University Council-University Development Co-operation(VLIR-UDC).

References

Anda, M., Shamshuddin, J., Fauziah, C.I., Omar, S.R.S., 2008. Mineralogy and factorscontrolling charge development of three Oxisols developed from different parentmaterials. Geoderma 143, 153–167.

Auxtero, E., Madeira, M., Sousa, E., 2004. Variable charge characteristics of selectedAndisols from the Azores, Portugal. Catena 56, 111–125.

Baert, G., Van Ranst, E., 1998. Exchange properties of highly weathered soils of thelower Congo. Malays. Soc. Soil Sci. 2, 31–44.

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

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

Brossard, M., López-Hernández, D., Lepage, M., Leprun, J.C., 2007. Nutrient storage insoils and nests of mound-building Trinervitermes termites in Central Burkina Faso:consequences for soil fertility. Biol. Fertil. Soils 43, 437–447.

Chorover, J., Sposito, G., 1995. Surface charge characteristics of kaolinitic tropical soils.Geochim. Cosmochim. Acta 59 (5), 875–884.

Fanshawe, D., 1971. The vegetation of Zambia. For. Res. Min. Rural Devel. Zambia 7,1–67.

FAO, 2006a. World Reference Base for Soil Resources. Food and AgricultureOrganization of the United Nations, Rome. 128 pp.

FAO, 2006b. Guidelines for Soil DescriptionFourth edition. Food and AgricultureOrganization of the United Nations, Rome. 97 pp.

Gillman, G.P., 1984. Using variable charge characteristics to understand the exchange-able cation status of oxic soils. Aust. J. Soil Res. 22, 71–80.

Gillman, G.P., 1985. Influence of organic matter and phosphate content on point of zerocharge of variable charge component in oxide soils. Aust. J. Soil Res. 23, 643–646.

Gillman, G.P., 2007. An analytical tool for understanding the properties and behavior ofvariable charge soils. Aust. J. Soil Res. 45, 83–90.

Gillman, G.P., Sinclair, D.F., 1987. The grouping of soils with similar charge properties asa basis for agrotechnology-transfer. Aust. J. Soil Res. 25, 275–285.

Gillman, G.P., Sumpter, E.A., 1986. Surface charge characteristics and lime requirementsof soils derived from basaltic, granitic, and metamorphic rocks in high-rainfalltropical Queensland. Aust. J. Soil Res. 24, 173–192.

Goffinet, G., 1976. Ecologie édaphique des écosystèmes naturels du Haut-Shaba (Zaire).Note III: Les peuplements en termites épigés au niveau des latosols. Bull. Ecol. 7 (3),335–352.

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

Jouquet, P., Mamou, L., Lepage, M., Velde, B., 2002. Effect of termites on clay minerals intropical soils fungus-growing termites as weathering agents. Eur. J. Soil Sci. 53,521–527.

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

241B.B. Mujinya et al. / Geoderma 158 (2010) 233–241

Jouquet, P., Dauber, J., Lagerlöf, J., 2006. Soil invertebrates asecosystemengineers: intendedand accidental effects on soil and feedback loops. Appl. Soil Ecol. 32, 153–164.

Jouquet, P., Bottinelli, N., Lata, J.-C., Mora, P., Caquineau, S., 2007. Role of the fungus-growing termite Pseudacanthotermes spiniger (Isoptera, Macrotermitinae) in thedynamic of clay and soil organic matter content. An experimental analysis.Geoderma 139, 127–133.

Korb, J., 2007. Termites. Curr. Biol. 17 (n° 23), R996 Regensburg, Germany.Lavelle, P., Blanchart, E., Martin, A., Spain, A.V., Martin, S., 1992. Impact of soil fauna on the

propertiesof soils in thehumid tropics.Myths and scienceof soils of the tropics. Soil Sc.Soc. Amer. and Amer. Soc. of Agr., Special publication N° 29. Madison, pp. 157–185.

Lepage, M., Darlington, J.P.E.C., 2000. Population dynamics of termites. In: Abe, T.,Bignell, D.E., Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology.Kluwer Academic Publishers, Dordrecht, pp. 333–361.

López-Hernández, D., Brossard, M., Fardeau, J.C., Lepage, M., 2006. Effect of differenttermite feeding groups on P sorption and P availability in African and SouthAmerican savannas. Biol. Fertil. Soils 42, 207–214.

Mahaney, W.C., Zippin, J., Milner, M.W., Sanmugadas, K., Hancock, R.G.V., Aufreiter, S.,1999. Chemistry, mineralogy and microbiology of termite mound soil eaten by thechimpanzees of the Mahale Mountains, Western Tanzania. J. Trop. Ecol. 15, 565–588.

Mehra, B.P., Jackson, H.L., 1960. Iron oxide removal from soils and clays by a dithionite–citrate system buffered with sodium bicarbonate. Clays Clay Miner. 7, 317–327.

Mora, P., Seugé, C., Chotte, J.L., Rouland, C., 2003. Physico-chemical typology of thebiogenic structures of termites, and earthworms: a comparative analysis. Biol.Fertil. Soils 37, 245–249.

Parker, J.C., Zelazny, L.W., Sampath, S., Harris, W.G., 1979. A critical evaluation of theextension of zero point of charge (zpc) theory to soil systems. Soil Sci. Soc. Amer. J.43, 668–674.

Qafoku, N.P., Van Ranst, E., Noble, A., Baert, G., 2004. Variable charge soils: theirmineralogy, chemistry and management. Adv. Agron. 84, 159–215.

Sposito, G., 2008. TheChemistry of Soils2nd Ed. OxfordUniversity Press, NewYork. 330 pp.Sys, C., 1957. L'aménagement des sols de la région d'Elisabethville d'après leurs

caractéristiques morphologiques et analytiques. Bull. Agr. Congo belge 48 (6),1425–1432.

Sys, C., Schmitz, A., 1959. Note explicative des cartes de sol et de la végétation duCongo-Belge et du Rwanda-Urundi; région d'Elisabethville (Haut-Katanga), N° 9; A,B et C. Publication INEAC, Bruxelles, pp. 10–11.

Van Ranst, E., Shamshuddin, J., Baert, G., Dzwowa, P.K., 1998. Charge characteristics inrelation to free iron and organic matter of soils from Bambouto Mountains.Western Cameroon. Eur. J. Soil Sci. 49, 243–252.

Van Ranst, E., Verloo, M., Demeyer. A. and Pauwels. J.M., 1999. Manual for the soilchemistry and fertility laboratory—analytical methods for soils and plants,equipment, and management of consumables. NUGI 835, Belgium (ISBN 90-76603-01-4), 243 pp.

Yu, T.R., 1997. Chemistry of Variable Charge Soils. Oxford University Press, New York,pp. 29–38.